Publications in peer reviewed journals

142 Publications found
  • Climate change impacts on soil biology

    2023 - Encyclopedia of Soils in the Environment, 1: 578-586



    Human activities have caused a rapid climate change affecting all parts of the biosphere, including soils. Soil organisms from all three domains of life, their interactions, and all soil processes for which they are responsible are influenced by and in turn respond to climate change. The understanding of how soil organisms and their processes react to climate changes, is thus central to our ability to manage ecosystems and develop strategies to mitigate climate change. This chapter examines the current state of soil biology (from organisms and communities to the processes they control) in the context of climate change and identifies current gaps in knowledge and promising ways forward.

  • Beyond PLFA: Concurrent extraction of neutral and glycolipid fatty acids provides new insights into soil microbial communities

    Gorka S, Darcy S, Horak J, Imai B, Mohrlok M, Salas E, Richter A, Schmidt H, Wanke W, Kaiser C, Canarini A
    2023 - Soil Biology and Biochemistry, 187: Article 109205


    The analysis of phospholipid fatty acids (PLFAs) is one of the most common methods used to quantify the abundance, and analyse the community structure, of soil microbes. The PLFA extraction method can yield two additional lipid fractions—neutral lipids and glycolipids—which potentially hold additional, valuable information on soil microbial communities. Yet its quantitative sensitivity on complete neutral lipid (NLFA) and glycolipid fatty acid (GLFA) profiles has never been validated. In this study we tested (i) if the high-throughput PLFA method can be expanded to concurrently extract complete NLFA and GLFA profiles, as well as sterols, (ii) whether taxonomic specificities of signature fatty acids are retained across the three lipid fractions in pure culture strains, and (iii) whether NLFAs and GLFAs allow soil-specific fingerprinting to the same extent as PLFA analysis. By adjusting the polarity of chloroform with 2% ethanol for solid phase extraction, pure lipid standards were fully fractionated into neutral lipidsglycolipids, and phospholipids. Sterols eluted in the neutral lipid fraction, and a betaine lipid co-eluted with phospholipids. We found consistent taxonomic specificities of fatty acid markers across the three lipid fractions by analysing pure culture extracts representative of soil microbes. Fatty acid profiles from soil extracts, however, showed stronger differences between PLFAs, NLFAs, and GLFAs than between soil types. This indicates that PLFAs and NLFAs signify different community properties (biomass vs. carbon storage, putatively), and that GLFAs are sensitive markers for community traits which behave differently than PLFAs. Although we consistently found high abundances of characteristic sterols in fungal extracts, the PLFA extraction method only yielded miniscule amounts of ergosterol from soil extracts. We argue that concomitant measurement of fatty acid profiles from all three lipid fractions is a low-effort and potentially information-rich addition to the PLFA method, and discuss its applicability for soil microbial community analyses.

  • Microbial growth under drought is confined to distinct taxa and modified by potential future climate conditions

    Metze M, Schnecker J, Canarini A, Fuchslueger L, Koch BJ, Stone BW, Hungate BA, Hausmann B, Schmidt H, Schaumberger A, Bahn M, Kaiser C, Richter A
    2023 - Nature Communication, 14: Article 5895


    Climate change increases the frequency and intensity of drought events, affecting soil functions including carbon sequestration and nutrient cycling, which are driven by growing microorganisms. Yet we know little about microbial responses to drought due to methodological limitations. Here, we estimate microbial growth rates in montane grassland soils exposed to ambient conditions, drought, and potential future climate conditions (i.e., soils exposed to 6 years of elevated temperatures and elevated CO2 levels). For this purpose, we combined 18O-water vapor equilibration with quantitative stable isotope probing (termed ‘vapor-qSIP’) to measure taxon-specific microbial growth in dry soils. In our experiments, drought caused >90% of bacterial and archaeal taxa to stop dividing and reduced the growth rates of persisting ones. Under drought, growing taxa accounted for only 4% of the total community as compared to 35% in the controls. Drought-tolerant communities were dominated by specialized members of the Actinobacteriota, particularly the genus Streptomyces. Six years of pre-exposure to future climate conditions (3 °C warming and + 300 ppm atmospheric CO2) alleviated drought effects on microbial growth, through more drought-tolerant taxa across major phyla, accounting for 9% of the total community. Our results provide insights into the response of active microbes to drought today and in a future climate, and highlight the importance of studying drought in combination with future climate conditions to capture interactive effects and improve predictions of future soil-climate feedbacks.

  • Tree stem and soil methane and nitrous oxide fluxes, but not carbon dioxide fluxes, switch sign along a topographic gradient in a tropical forest

    Daniel W, Stahl C, Burban B, Goret J-Y, Cazal J, Richter A, Janssens IA, Bréchet LM
    2023 - Plant and soil, 488: 533-549



    Tropical forests exchange large amounts of greenhouse gases (GHGs: carbon dioxide, CO2; methane, CH4; and nitrous oxide, N2O) with the atmosphere. Forest soils and stems can be either sources or sinks for CH4 and N2O, but little is known about what determines the sign and magnitude of these fluxes. Here, we aimed to study how stem and soil GHG fluxes vary along a topographic gradient in a tropical forest.


    Fluxes of GHG from 56 individual tree stems and adjacent soils were measured with manual static chambers. The topographic gradient was characterized by a soil moisture gradient, with one end in a wetland area (“seasonally flooded”; SF), the other end in an upland area (“terra firme”; TF) and in between a transitional area on the slope (SL).


    Tree stems and soils were always sources of CO2 with higher fluxes in SF compared to TF and SL. Fluxes of CH4 and N2O were more variable, even within one habitat. Results showed that, in TF, soils acted as sinks for N2O whereas, in SF and SL, they acted as sources. In contrast, tree stems which were predominantly sources of N2O in SF and TF, were sinks in SL. In the soil, N2O fluxes were significantly influenced by both temperature and soil water content, whereas CH4 fluxes were only significantly correlated with soil water content.


    SF areas were major sources of the three gases, whereas SL and TF soils and tree stems acted as either sources or sinks for CH4 and N2O. Our results indicate that tree stems represent overlooked sources of CH4 and N2O in tropical forests that need to be further studied to refine GHG budgets.

  • Long-term warming-induced trophic downgrading in the soil microbial food web

    Borg Dahl M, Söllinger A, Sigurðsson P, Janssens I, Peñuelas J, Sigurdsson BD, Richter A, Tveit AT, Urich T
    2023 - Soil Biology and Biochemistry, 181: Article 109044


    Climatic warming has been hypothesized to accelerate organic matter decomposition by soil microorganisms and thereby enhance carbon (C) release to the atmosphere. However, the long-term consequences of soil warming on belowground biota interactions are poorly understood. Here we investigate how geothermal warming by 6 °C for more than 50 years affects soil microbiota. Using metatranscriptomics we obtained comprehensive profiles of the prokaryotic, eukaryotic and viral players of the soil microbial food web. When compared to ambient soil temperature conditions, we found pronounced differences in taxa abundances within and between trophic modules of the soil food web. Specifically, we observed a ‘trophic downgrading’ at elevated temperature, with soil fauna decreasing in abundance, while predatory bacteria and viruses became relatively more abundant. We propose that the drivers for this shift are previously observed decreases in microbial biomass and soil organic carbon, and the increase in soil bulk density (decrease in soil porosity) at elevated temperature. We conclude that a trophic downgrading may have important implications for soil carbon sequestration and nutrient dynamics in a warming world.

  • Nutrient controls on carbohydrate and lignin decomposition in beech litter

    Kohl L, Wanek W, Keiblinger K, Hämmerle I, Fuchslueger L, Schneider T, Riedel K, Eberl L, Zechmeister-Boltenstern S, Richter A
    2023 - Geoderma, 429: Article 116276


    Nutrient pollution has increased plant litter nutrient concentrations in many ecosystems, which may profoundly impact litter decomposition and change the chemical composition of litter inputs to soils. Here, we report on a mesocosm experiment to study how variations in the nitrogen (N) and phosphorus (P) concentrations in Fagus sylvatica (European beech) litter from four sites differing in bedrock, atmospheric deposition, and climate affect lignin and carbohydrate loss rates and residual litter chemistry. We show with pyrolysis GC/MS and elemental analysis that nutrient concentrations had a strong influence on changes in litter chemistry during early decomposition (0–181 days), when greater lignin loss rates were associated with low P concentrations, whereas carbohydrate and bulk C loss were associated with high N concentrations. Nutrient concentrations, in contrast, did not influence changes in litter chemistry in the later decomposition stage (181–475 days), where the decomposition rates of lignin, carbohydrates, and bulk C all increased with litter N concentration and no differences in decomposition rates between major compound classes were detected. Our data indicate that these differences were related to the transition from increasing to constant or declining microbial biomass, and an associated decrease in microbial dependence on the mobilization of nutrients from the insoluble litter fraction.

  • High resolution mapping shows differences in soil carbon and nitrogen stocks in areas of varying landscape history in Canadian lowland tundra

    Wagner J, Martin V, Speetjens NJ, A'campo W, Durstewitz L, Lodi R, Fritz M, Tanski G, Vonk JE, Richter A, Bartsch A, Lantuit H, Hugelius G
    2023 - Geoderma, 438: Article 116652


    Soil organic carbon (SOC) in Arctic coastal polygonal tundra is vulnerable to climate change, especially in soils with occurrence of large amounts of ground ice. Pan-arctic studies of mapping SOC exist, yet they fail to describe the high spatial variability of SOC storage in permafrost landscapes. An important factor is the landscape history which determines landform development and consequently the spatial variability of SOC. Our aim was to map SOC stocks, and which environmental variables that determine SOC, in two adjacent coastal areas along Canadian Beaufort Sea coast with different glacial history. We used the machine learning technique random forest and environmental variables to map the spatial distribution of SOC stocks down to 1 m depth at a spatial resolution of 2 m for depth increments of 0–5, 5–15, 15–30, 30–60 and 60–100 cm.

    The results show that the two study areas had large differences in SOC stocks in the depth 60–100 cm due to high amounts of ground ice in one of the study areas. There are also differences in variable importance of the explanatory variables between the two areas. The area low in ground ice content had with 66.6 kg C/m−2 more stored SOC than the area rich in ground ice content with 40.0 kg C/m−2. However, this SOC stock could be potentially more vulnerable to climate change if ground ice melts and the ground subsides. The average N stock of the area low in ground ice is 3.77 kg m−2 and of the area rich in ground ice is 3.83 kg m−2.

    These findings support that there is a strong correlation between ground ice and SOC, with less SOC in ice-rich layers on a small scale. In addition to small scale studies of SOC mapping, detailed maps of ground ice content and distribution are needed for a validation of large-scale quantifications of SOC stocks and transferability of models.

  • Decadal soil warming decreased vascular plant above and belowground production in a subarctic grassland by inducing nitrogen limitation

    Fang C, Verbrigghe N, Sigurdsson BD, Ostonen I, Leblans NIW, Marañon-Jimenez S, Fuchslueger L, Sigurðsson P, Meeran K, Portillo-Estrada M, Verbruggen E, Richter A, Sardans J, Peñuelas J, Bahn M, Vicca S, Janssens IA
    2023 - New Phytologist, 240: 565-576


    • Below and aboveground vegetation dynamics are crucial in understanding how climate warming may affect terrestrial ecosystem carbon cycling. In contrast to aboveground biomass, the response of belowground biomass to long-term warming has been poorly studied.
    • Here, we characterized the impacts of decadal geothermal warming at two levels (on average +3.3°C and +7.9°C) on below and aboveground plant biomass stocks and production in a subarctic grassland.
    • Soil warming did not change standing root biomass and even decreased fine root production and reduced aboveground biomass and production. Decadal soil warming also did not significantly alter the root–shoot ratio. The linear stepwise regression model suggested that following 10 yr of soil warming, temperature was no longer the direct driver of these responses, but losses of soil N were. Soil N losses, due to warming-induced decreases in organic matter and water retention capacity, were identified as key driver of the decreased above and belowground production. The reduction in fine root production was accompanied by thinner roots with increased specific root area.
    • These results indicate that after a decade of soil warming, plant productivity in the studied subarctic grassland was affected by soil warming mainly by the reduction in soil N.
    • Below and aboveground vegetation dynamics are crucial in understanding how climate warming may affect terrestrial ecosystem carbon cycling. In contrast to aboveground biomass, the response of belowground biomass to long-term warming has been poorly studied.
    • Here, we characterized the impacts of decadal geothermal warming at two levels (on average +3.3°C and +7.9°C) on below and aboveground plant biomass stocks and production in a subarctic grassland.
    • Soil warming did not change standing root biomass and even decreased fine root production and reduced aboveground biomass and production. Decadal soil warming also did not significantly alter the root–shoot ratio. The linear stepwise regression model suggested that following 10 yr of soil warming, temperature was no longer the direct driver of these responses, but losses of soil N were. Soil N losses, due to warming-induced decreases in organic matter and water retention capacity, were identified as key driver of the decreased above and belowground production. The reduction in fine root production was accompanied by thinner roots with increased specific root area.
    • These results indicate that after a decade of soil warming, plant productivity in the studied subarctic grassland was affected by soil warming mainly by the reduction in soil N.
  • Soil organic carbon accumulation and microbial carbon use efficiency in subalpine coniferous forest as influenced by forest floor vegetative communities

    Xiong J, Wang G, Richter A, DeLuca TH, Zhang W, Sun H, Hu Z, Sun X, Sun S
    2023 - Geoderma, 438: Article 11664



    The importance of forest floor plants (herbs and mosses) and understory communities on soil C dynamics has been grossly understudied in forest ecosystems; however, there is currently very little knowledge on the impact of forest floor vegetation composition on soil organic C (SOC) accumulation and the microbial metabolic processes. To bridge this gap of knowledge, a forest floor vegetation-removal experiment involving nonvascular mosses (Pleurozium schreberi (PS); Rhizomnium tuomikoskii (RT); and Hylocomiastrum pyrenaicum (HP)) and vascular sedges (Carex sp., CS) was conducted in a subalpine coniferous forest on the eastern edge of Tibetan Plateau, to investigate the associations of different forest floor vegetation communities with mineral soil C accumulation and microbial physiology (C use efficiency (CUE) and microbial biomass turnover). Soils beneath the forest floor vegetative communities differed in soil C and nitrogen (N) concentrations and had distinctively different microbial community structure and physiology. Compared to bare soils, sedge soils had significantly greater SOC and dissolved organic C (DOC) accumulation, greater microbial DNA, biomass C and phospholipid fatty acids (PLFAs) concentrations, and higher microbial CUE and shorter microbial biomass turnover time. While effects of mosses differed among species, P. schreberi had similar effects as sedges, but the effects of H. pyrenaicum and R. tuomikoskii were minimal. Relative to bare soil, P. schreberi and Carex sp. soils were 61.5% and 51.6% higher in microbial CUE and had an obviously shorter microbial biomass turnover time. Variations in the level of DOC and PLFAs (rather than their portion relative to SOC) were the most important regulators of microbial CUE and biomass turnover rate in soils with different forest floor vegetation covers. These results highlight how differences in soil organic matter quality that are directly related to the forest floor vegetation community influence the microbial CUE and biomass turnover and the long-term soil C dynamics.

  • Responses of soil hexapod communities to warming are mediated by microbial carbon and nitrogen in a subarctic grassland

    Ferrín M. Peñuelas J, Gargallo-Garriga A, Iribar A, Janssens IA, Marañon-Jimenez S, Murienne J, Richter A, Sigurdsson BD, Peguero G
    2023 - European Journal of Soil Biology, 117: Article 103513


    Warming in subarctic ecosystems will be two-fold higher compared to lower latitudes under current climate change projections. While the effects of warming in northern ecosystems on plants and microorganisms have been extensively studied, the responses of soil fauna have received much less attention, despite their important role in regulating key soil processes. We analyzed the response of soil hexapod communities in a subarctic grassland exposed to a natural geothermal gradient in Iceland with increases of +3 and + 6 °C above ambient temperature. We characterized hexapod communities using environmental DNA (eDNA) metabarcoding. We analyzed the amounts of microbial carbon (Cmic), microbial N (Nmic), dissolved organic C (DOC) and dissolved organic N (DON) and then assessed whether these variables could help to account for the compositional dissimilarity of ground hexapod communities across temperatures. The increases in soil temperature did lead to changes in the composition of hexapod communities. The compositional differences caused by +6 °C plots were correlated with a decrease in Cmic and Nmic, soil DOC and DON. Our results highlight the response of soil hexapods to warming, and their interaction with microbial biomass ultimately correlated with changes in the availabilities of soil C and N.

  • How temperature and aridity drive lignin decomposition along a latitudinal transect in western Siberia

    Dao TT, Mikutta R, Wild B, Sauheitl L, Gentsch N, Shibistova O, Schnecker J, Lashchinskiy N, Richter A, Guggenberger G
    2023 - European Journal of Soil Science, 74: e13408


    Climate change drives a northward shift of biomes in high-latitude regions. This might have consequences on the decomposition of plant litter entering the soil, including its lignin component, which is one of the most abundant components of vascular plants. In order to elucidate the combined effect of climate and soil characteristics on the decomposition pattern of lignin, we investigated lignin contents and its degree of oxidative decomposition within soil profiles along a climosequence in western Siberia. Soil samples were collected from organic topsoil to mineral subsoil at six sites along a 1500-km latitudinal transect, stretching from tundra, through taiga and forest steppe to typical steppe. The stage of lignin degradation, as mirrored by decreasing organic carbon-normalized lignin contents and increasing oxidative alteration of the remnant lignin (acid-to-aldehyde ratios of vanillyl- and syringyl-units [(Ac/Al)V and (Ac/Al)S]) within soil horizons, increased from tundra to forest steppe and then decreased to the steppe. Principal component analysis, involving also climatic conditions such as mean annual temperature and aridity index, showed that the different states of lignin degradation between horizons related well to the activity of phenoloxidases and peroxidases, enzymes involved in lignin depolymerization that are produced primarily by fungi and less importantly by bacteria. The low microbial lignin decomposition in the tundra was likely due to low temperature and high soil moisture, which do not favour the fungi. Increasing temperature and decreasing soil moisture, facilitating a higher abundance of fungi, led to increased fungal lignin decomposition towards the forest-steppe biome, while drought and high pH might be responsible for the reduced lignin decomposition in the steppe. We infer that a shift of biomes to the north, driven by climate change, might promote lignin decomposition in the northern parts, whereas in the south a further retardation might be likely.



    • Lack of lignin contribution to soil organic matter and its degradation in different Siberian biomes.
    • The dependency of lignin decomposition predicts the fate of lignin under climate warming.
    • Climate warming accelerates lignin degradation at high latitude, while in the south it is likely retarded.
    • Lignin alteration with climate change has impacted on long-term development of soil carbon stock.

  • Taurine as a key intermediate for host-symbiont interaction in the tropical sponge Ianthella basta

    Moeller FU, Herbold CW, Schintlmeister A, Mooshammer M, Motti C, Glasl B, Kitzinger K, Behnam F, Watzka M, Schweder T, Albertsen M, Richter A, Webster NS, Wagner M
    2023 - The ISME Journal, 17: 1208-1223


    Marine sponges are critical components of marine benthic fauna assemblages, where their filter-feeding and reef-building capabilities provide bentho-pelagic coupling and crucial habitat. As potentially the oldest representation of a metazoan-microbe symbiosis, they also harbor dense, diverse, and species-specific communities of microbes, which are increasingly recognized for their contributions to dissolved organic matter (DOM) processing. Recent omics-based studies of marine sponge microbiomes have proposed numerous pathways of dissolved metabolite exchange between the host and symbionts within the context of the surrounding environment, but few studies have sought to experimentally interrogate these pathways. By using a combination of metaproteogenomics and laboratory incubations coupled with isotope-based functional assays, we showed that the dominant gammaproteobacterial symbiont, ‘Candidatus Taurinisymbion ianthellae’, residing in the marine sponge, Ianthella basta, expresses a pathway for the import and dissimilation of taurine, a ubiquitously occurring sulfonate metabolite in marine sponges. ‘Candidatus Taurinisymbion ianthellae’ incorporates taurine-derived carbon and nitrogen while, at the same time, oxidizing the dissimilated sulfite into sulfate for export. Furthermore, we found that taurine-derived ammonia is exported by the symbiont for immediate oxidation by the dominant ammonia-oxidizing thaumarchaeal symbiont, ‘Candidatus Nitrosospongia ianthellae’. Metaproteogenomic analyses also suggest that ‘Candidatus Taurinisymbion ianthellae’ imports DMSP and possesses both pathways for DMSP demethylation and cleavage, enabling it to use this compound as a carbon and sulfur source for biomass, as well as for energy conservation. These results highlight the important role of biogenic sulfur compounds in the interplay between Ianthella basta and its microbial symbionts.

  • Microbial responses to soil cooling might explain increases in microbial biomass in winter

    SchneckerJ, Spiegel F, Li Y, Richter A, Sandén T, Spiegel H, Zechmeister-Boltenstern S, Fuchslueger L
    2023 - Biogeochemistry, 164: 521-535


    In temperate, boreal and arctic soil systems, microbial biomass often increases during winter and decreases again in spring. This build-up and release of microbial carbon could potentially lead to a stabilization of soil carbon during winter times. Whether this increase is caused by changes in microbial physiology, in community composition, or by changed substrate allocation within microbes or communities is unclear. In a laboratory incubation study, we looked into microbial respiration and growth, as well as microbial glucose uptake and carbon resource partitioning in response to cooling. Soils taken from a temperate beech forest and temperate cropland system in October 2020, were cooled down from field temperature of 11 °C to 1 °C. We determined microbial growth using 18O-incorporation into DNA after the first two days of cooling and after an acclimation phase of 9 days; in addition, we traced 13C-labelled glucose into microbial biomass, CO2 respired from the soil, and into microbial phospholipid fatty acids (PLFAs). Our results show that the studied soil microbial communities responded strongly to soil cooling. The 18O data showed that growth and cell division were reduced when soils were cooled from 11 to 1 °C. Total respiration was also reduced but glucose uptake and glucose-derived respiration were unchanged. We found that microbes increased the investment of glucose-derived carbon in unsaturated phospholipid fatty acids at colder temperatures. Since unsaturated fatty acids retain fluidity at lower temperatures compared to saturated fatty acids, this could be interpreted as a precaution to reduced temperatures. Together with the maintained glucose uptake and reduced cell division, our findings show an immediate response of soil microorganisms to soil cooling, potentially to prepare for freezing events. The discrepancy between C uptake and cell division could explain previously observed high microbial biomass carbon in temperate soils in winter.

  • Exo- and endophytic fungi enable rapid transfer of nutrients from ant waste to orchid tissue

    Gegenbauer C, Bellaire A, Schintlmeister A, Schmid MC, Kubicek M, Voglmayr H, Zotz G, Richter A, Mayer VE
    2023 - New Phytologist, 238: 2210-2223




    • The epiphytic orchid Caularthron bilamellatum sacrifices its water storage tissue for nutrients from the waste of ants lodging inside its hollow pseudobulb. Here, we investigate whether fungi are involved in the rapid translocation of nutrients.
    • Uptake was analysed with a 15N labelling experiment, subsequent isotope-ratio mass spectrometry (IRMS) and secondary ion mass spectrometry (ToF-SIMS and NanoSIMS).
    • We encountered two hyphae types: a thick melanized type assigned to “black fungi” (Chaetothyriales, Cladosporiales, Mycosphaerellales) in ant waste, and a thin endophytic type belonging to Hypocreales. In few cell layers both hyphae types co-occurred. 15N accumulation in both hyphae types was conspicuous, while for translocation to the vessels only Hypocreales were involved. There is evidence that the occurrence of the two hyphae types result in a synergism in terms of nutrient uptake.
    • Our study provides the first evidence that a pseudobulb (=stem)-born endophytic network of Hypocreales is involved in the rapid translocation of nitrogen from insect derived waste to the vegetative and reproductive tissue of the host orchid. For C. bilamellatum that has no contact with the soil, ant waste in the hollow pseudobulbs serves as equivalent to soil in terms of nutrient sources.
  • Rapid nitrification involving comammox and canonical Nitrospira at extreme pH in saline-alkaline lakes

    Daebler A, Güell-Bujons Q, Mooshammer M, Zechmeister T, Herbold CW, Richter A, Wagner M, Daims H
    2023 - Environmental Microbiology, 25: 1055-1067


    Nitrite-oxidizing bacteria (NOB) catalyse the second nitrification step and are the main biological source of nitrate. The most diverse and widespread NOB genus is Nitrospira, which also contains complete ammonia oxidizers (comammox) that oxidize ammonia to nitrate. To date, little is known about the occurrence and biology of comammox and canonical nitrite oxidizing Nitrospira in extremely alkaline environments. Here, we studied the seasonal distribution and diversity, and the effect of short-term pH changes on comammox and canonical Nitrospira in sediments of two saline, highly alkaline lakes. We identified diverse canonical and comammox Nitrospira clade A-like phylotypes as the only detectable NOB during more than a year, suggesting their major importance for nitrification in these habitats. Gross nitrification rates measured in microcosm incubations were highest at pH 10 and considerably faster than reported for other natural, aquatic environments. Nitrification could be attributed to canonical and comammox Nitrospira and to Nitrososphaerales ammonia-oxidizing archaea. Furthermore, our data suggested that comammox Nitrospira contributed to ammonia oxidation at an extremely alkaline pH of 11. These results identify saline, highly alkaline lake sediments as environments of uniquely strong nitrification with novel comammox Nitrospira as key microbial players.

  • Nitrogen fixation by diverse diazotrophic communities can support population growth of arboreal ants

    Nepel M, Pfeifer J, Oberhauser FB, Richter A, Woebken D, Mayer VE
    2022 - BMC Biology, 20: Article 135



    Symbiotic ant-plant associations, in which ants live on plants, feed on plant-provided food, and protect host trees against threats, are ubiquitous across the tropics, with the Azteca-Cecropia associations being amongst the most widespread interactions in the Neotropics. Upon colonization of Cecropia’s hollow internodes, Azteca queens form small patches with plant parenchyma, which are then used as waste piles when the colony grows. Patches—found in many ant-plant mutualisms—are present throughout the colony life cycle and may supplement larval food. Despite their initial nitrogen (N)-poor substrate, patches in Cecropia accommodate fungi, nematodes, and bacteria. In this study, we investigated the atmospheric N2 fixation as an N source in patches of early and established ant colonies.


    Via 15N2 tracer assays, N2 fixation was frequently detected in all investigated patch types formed by three Azteca ant species. Quantified fixation rates were similar in early and established ant colonies and higher than in various tropical habitats. Based on amplicon sequencing, the identified microbial functional guild—the diazotrophs—harboring and transcribing the dinitrogenase reductase (nifH) gene was highly diverse and heterogeneous across Azteca colonies. The community composition differed between early and established ant colonies and partly between the ant species.


    Our data show that N2 fixation can result in reasonable amounts of N in ant colonies, which might not only enable bacterial, fungal, and nematode growth in the patch ecosystems but according to our calculations can even support the growth of ant populations. The diverse and heterogeneous diazotrophic community implies a functional redundancy, which could provide the ant-plant-patch system with a higher resilience towards changing environmental conditions. Hence, we propose that N2 fixation represents a previously unknown potential to overcome N limitations in arboreal ant colonies.

  • Stoichiometric regulation of priming effects and soil carbon balance by microbial life strategies

    Zhu Z, Fang Y, Liang Y, Li Y, Liu S, Li B, Gao W, Yuan H, Kuzyakov Y, Wu J, Richter A, Ge T
    2022 - Soil Biology and Biochemistry, 169: Article 108669


    Carbon and nutrient inputs are required to stimulate the formation and mineralization of soil organic carbon (SOC) through processes related to microbial growth and priming effects (PEs). PEs are thought to affect microbial life strategies, however, the mechanisms underlying their role in SOC formation and microbial dynamics remain largely unknown, particularly in paddy soils. Here, we examined the underlying strategies and response mechanisms of microorganisms in regulating PEs and C accumulation in flooded paddy soil. Levels and stoichiometric ratios of resources were evaluated over a 60-day incubation period. Low (equivalent to 50% soil microbial biomass C [MBC]) and high (500% MBC) doses of 13C-labeled glucose were added to the soil, along with mineral N, P, and S (NPS) fertilizers at five concentrations. Glucose mineralization increased linearly with NPS concentration under both low and high glucose inputs. However, glucose addition without nutrients induced the preferential microbial utilization of the readily available C, leading to negative PEs. Under high-glucose input, the intensity of negative PEs increased with increasing NPS addition (PE: from −460 to −710 mg C kg−1 soil). In contrast, under low-glucose inputs, the intensity of positive PEs increased with increasing NPS addition (PE: 60–100 mg C kg−1 soil). High-glucose input with NPS fertilization favored high-yield microbial strategists (Y-strategists), increasing glucose-derived SOC accumulation. This phenomenon was evidenced by the large quantities of 13C detected in microbial biomass and phospholipid fatty acids (PLFAs), increasing the soil net C balance (from 0.76 to 1.2 g C kg−1). In contrast, low levels of glucose and NPS fertilization shifted the microbial community composition toward dominance of resource-acquisition strategists (A-strategists), increasing SOC mineralization. This was evidenced by 13C incorporation into the PLFAs of gram-positive bacteria, increased activity of N- and P-hydrolases, and positive PEs for acquiring C and nutrients from soil organic matter. Consequently, the soil net C balance decreased from 0.31 to 0.01 g C kg−1 soil. In conclusion, high C input (i.e., 500% MBC), particularly alongside hig NPS addition, increases SOC content via negative priming and microbial-derived C accumulation due to the shift toward Y-strategist communities which efficiently utilize resources. This study highlights the importance of mineral fertilization management when incorporating organic supplements in paddy soils to stimulate microbial turnover and C sequestration.

  • Contrasting drivers of belowground nitrogen cycling in a montane grassland exposed to a multifactorial global change experiment with elevated CO, warming, and drought

    Maxwell TL, Canarini A, Bogdanovic I, Böckle T, Martin V, Noll L, Prommer J, Séneca J, Simon E, Piepho HP, Herndl M, Pötsch EM, Kaiser C, Richter A, Bahn M, Wanek W
    2022 - Global Change Biology, 28: 2425-2441


    Depolymerization of high-molecular weight organic nitrogen (N) represents the major bottleneck of soil N cycling and yet is poorly understood compared to the subsequent inorganic N processes. Given the importance of organic N cycling and the rise of global change, we investigated the responses of soil protein depolymerization and microbial amino acid consumption to increased temperature, elevated atmospheric CO2, and drought. The study was conducted in a global change facility in a managed montane grassland in Austria, where elevated CO2 (eCO2) and elevated temperature (eT) were stimulated for 4 years, and were combined with a drought event. Gross protein depolymerization and microbial amino acid consumption rates (alongside with gross organic N mineralization and nitrification) were measured using 15N isotope pool dilution techniques. Whereas eCO2 showed no individual effect, eT had distinct effects which were modulated by season, with a negative effect of eT on soil organic N process rates in spring, neutral effects in summer, and positive effects in fall. We attribute this to a combination of changes in substrate availability and seasonal temperature changes. Drought led to a doubling of organic N process rates, which returned to rates found under ambient conditions within 3 months after rewetting. Notably, we observed a shift in the control of soil protein depolymerization, from plant substrate controls under continuous environmental change drivers (eT and eCO2) to controls via microbial turnover and soil organic N availability under the pulse disturbance (drought). To the best of our knowledge, this is the first study which analyzed the individual versus combined effects of multiple global change factors and of seasonality on soil organic N processes and thereby strongly contributes to our understanding of terrestrial N cycling in a future world.

  • Plant-microbial linkages underpin carbon sequestration in contrasting mountain tundra vegetation types

    Gavazov K, Canarini A, Jassey VEJ, Mills R, Richter A, Sundqvist MK, Väisänen M, Walker TWN, Wardle DA, Dorrepaal E
    2022 - Soil Biology and Biochemistry, Article 108530


    Tundra ecosystems hold large stocks of soil organic matter (SOM), likely due to low temperatures limiting rates of microbial SOM decomposition more than those of SOM accumulation from plant primary productivity and microbial necromass inputs. Here we test the hypotheses that distinct tundra vegetation types and their carbon supply to characteristic rhizosphere microbes determine SOM cycling independent of temperature. In the subarctic Scandes, we used a three-way factorial design with paired heath and meadow vegetation at each of two elevations, and with each combination of vegetation type and elevation subjected during one growing season to either ambient light (i.e., ambient plant productivity), or 95% shading (i.e., reduced plant productivity). We assessed potential above- and belowground ecosystem linkages by uni- and multivariate analyses of variance, and structural equation modelling. We observed direct coupling between tundra vegetation type and microbial community composition and function, which underpinned the ecosystem's potential for SOM storage. Greater primary productivity at low elevation and ambient light supported higher microbial biomass and nitrogen immobilisation, with lower microbial mass-specific enzymatic activity and SOM humification. Congruently, larger SOM at lower elevation and in heath sustained fungal-dominated microbial communities, which were less substrate-limited, and invested less into enzymatic SOM mineralisation, owing to a greater carbon-use efficiency (CUE). Our results highlight the importance of tundra plant community characteristics (i.e., productivity and vegetation type), via their effects on soil microbial community size, structure and physiology, as essential drivers of SOM turnover. The here documented concerted patterns in above- and belowground ecosystem functioning is strongly supportive of using plant community characteristics as surrogates for assessing tundra carbon storage potential and its evolution under climate and vegetation changes.

  • Both abundant and rare fungi colonizing Fagus sylvatica ectomycorrhizal root-tips shape associated bacterial communities

    Dietrich M, Montesinos-Navarro A, Gabriel R, Strasser F, Meier DV, Mayerhofer W, Gorla S, Wiesenbauer J, Martin V, Weidinger M, Richter A, Kaiser C, Woebken D
    2022 - Communications Biology, 5: Article 1261


    Ectomycorrhizal fungi live in close association with their host plants and form complex interactions with bacterial/archaeal communities in soil. We investigated whether abundant or rare ectomycorrhizal fungi on root-tips of young beech trees (Fagus sylvatica) shape bacterial/archaeal communities. We sequenced 16S rRNA genes and fungal internal transcribed spacer regions of individual root-tips and used ecological networks to detect the tendency of certain assemblies of fungal and bacterial/archaeal taxa to inhabit the same root-tip (i.e. modularity). Individual ectomycorrhizal root-tips hosted distinct fungal communities associated with unique bacterial/archaeal communities. The structure of the fungal-bacterial/archaeal association was determined by both, dominant and rare fungi. Integrating our data in a conceptual framework suggests that the effect of rare fungi on the bacterial/archaeal communities of ectomycorrhizal root-tips contributes to assemblages of bacteria/archaea on root-tips. This highlights the potential impact of complex fine-scale interactions between root-tip associated fungi and other soil microorganisms for the ectomycorrhizal symbiosis.

  • Negative erosion and negative emissions: Combining multiple land-based carbon dioxide removal techniques to rebuild fertile topsoils and enhance food production

    Janssens IA, Roobroeck D, Sardans J, Obersteiner M, Peñuelas J, Richter A, Smith P, Verbruggen E, Vicca S
    2022 - Frontiers in Climate, 4: Article 928403


    Carbon dioxide removal (CDR) that increases the area of forest cover or bio-energy crops inherently competes for land with crop and livestock systems, compromising food security, or will encroach natural lands, compromising biodiversity. Mass deployment of these terrestrial CDR technologies to reverse climate change therefore cannot be achieved without a substantial intensification of agricultural output, i.e., producing more food on less land. This poses a major challenge, particularly in regions where arable land is little available or severely degraded and where agriculture is crucial to sustain people's livelihoods, such as the Global South. Enhanced silicate weathering, biochar amendment, and soil carbon sequestration are CDR techniques that avoid this competition for land and may even bring about multiple co-benefits for food production. This paper elaborates on the idea to take these latter CDR technologies a step further and use them not only to drawdown CO2 from the atmosphere, but also to rebuild fertile soils (negative erosion) in areas that suffer from pervasive land degradation and have enough water available for agriculture. This way of engineering topsoil could contribute to the fight against malnutrition in areas where crop and livestock production currently is hampered by surface erosion and nutrient depletion, and thereby alleviate pressure on intact ecosystems. The thrust of this perspective is that synergistically applying multiple soil-related CDR strategies could restore previously degraded soil, allowing it to come back into food production (or become more productive), potentially alleviating pressure on intact ecosystems. In addition to removing CO2 from the atmosphere, this practice could thus contribute to reducing poverty and hunger and to protection of biodiversity.

  • Microbiome assembly in thawing permafrost and its feedbacks to climate

    Ernakovich JG, Barbato RA, Rich VI, Schädel C, Hewitt RE, Doherty SJ, Whalen ED, Abbott BW, Barta J, Biasi C, Chabot CL, Hultman J, Knoblauch C, Lau Vetter MCY, Leewis M-C, Liebner S, Mackelprang R, Onstott TC, Richter A, Schütte UME, Siljanen HMP, Taş N, Timling I, Vishnivetskaya TA, Waldrop MP, Winkel M
    2022 - Global Change Biology, in press


    The physical and chemical changes that accompany permafrost thaw directly influence the microbial communities that mediate the decomposition of formerly frozen organic matter, leading to uncertainty in permafrost–climate feedbacks. Although changes to microbial metabolism and community structure are documented following thaw, the generality of post-thaw assembly patterns across permafrost soils of the world remains uncertain, limiting our ability to predict biogeochemistry and microbial community responses to climate change. Based on our review of the Arctic microbiome, permafrost microbiology, and community ecology, we propose that Assembly Theory provides a framework to better understand thaw-mediated microbiome changes and the implications for community function and climate feedbacks. This framework posits that the prevalence of deterministic or stochastic processes indicates whether the community is well-suited to thrive in changing environmental conditions. We predict that on a short timescale and following high-disturbance thaw (e.g., thermokarst), stochasticity dominates post-thaw microbiome assembly, suggesting that functional predictions will be aided by detailed information about the microbiome. At a longer timescale and lower-intensity disturbance (e.g., active layer deepening), deterministic processes likely dominate, making environmental parameters sufficient for predicting function. We propose that the contribution of stochastic and deterministic processes to post-thaw microbiome assembly depends on the characteristics of the thaw disturbance, as well as characteristics of the microbial community, such as the ecological and phylogenetic breadth of functional guilds, their functional redundancy, and biotic interactions. These propagate across space and time, potentially providing a means for predicting the microbial forcing of greenhouse gas feedbacks to global climate change.

  • Growth of soil microbes is not limited by the availability of nitrogen and phosphorus in a Mediterranean oak-savanna

    Morris KA, Richter A, Migliavacca M, Schrumpf M
    2022 - Soil Biology and Biochemistry, 169: Article 108680


    The environmental conditions under which the availability of inorganic nutrients such as nitrogen (N) and phosphorus (P) influence soil microbial growth are poorly understood, especially with regards to how fertilization changes specific aspects of microbial growth such as carbon-use efficiency (CUE). Microbial CUE is the fraction of C converted into biomass out of all C taken in and plays a critical role in global C budgets. Using the 18O labeled water method we tested short vs. long-term effects of N and/or P fertilization on microbial growth, CUE, and C, N, and P-acquiring enzyme activities in two soils from an oak-savanna, which differ in their soil organic matter (SOM) content. We hypothesized that soils with more SOM (from under tree canopies) would have higher microbial growth rates than soils with less SOM (from open grassland), and that microbial growth and CUE would increase with fertilization. We further hypothesized that these increases would be associated with a decrease in enzyme activity and a shift towards older SOM substrates in the short-term, in contrast to substrates from recently fixed C resulting from increased plant productivity in the long-term. We found that nutrient additions did not affect microbial growth or CUE in the relatively high SOM habitat on either time scale. In contrast, the low SOM habitat had lower growth and CUE when single nutrients were added, with significantly reduced growth when P alone was added, but was unchanged when N and P were added together. Our results show that short-term, stoichiometric imbalances can reduce microbial growth and that microbial growth at this site is limited not by nutrients but by the amount of C available to soil microbes.

  • Long-term warming reduced microbial biomass but increased recent plant-derived C in microbes of a subarctic grassland

    Verbrigghe N, Meeran K, Bahn M, Canarini A, Fransen E, Fuchslueger L, Ingrisch J, Janssens IA, Richter A, Sigurdsson BD, Soong JL, Vicca S
    2022 - Soil Biology and Biochemistry, 167: Article 108590


    Long-term soil warming and nitrogen (N) availability have been shown to affect microbial biomass and community composition. Altered assimilation patterns of recent plant-derived C and changes in soil C stocks following warming as well as increased N availability are critical in mediating the direction and magnitude of these community shifts. A 13C pulse labelling experiment was done on a warming gradient in an Icelandic grassland (Sigurdsson et al., 2016), to investigate the role of recent plant-derived C and warming on the microbial community structure and size. We observed an overall increase of microbial 13C (e.g., root-exudate) uptake, while warming led to significant microbial biomass loss in all microbial groups. The increase of microbial 13C uptake with warming differed between microbial groups: an increase was only observed in the general and Gram-positive bacterial phospholipid fatty acid (PLFA) markers and in the PLFA and neutral lipid fatty acid (NLFA) markers of arbuscular mycorrhizal fungi (AMF). Nitrogen addition of 50 kg ha−1 y−1 for two years had no effect on the microbial uptake, microbial biomass or community composition, indicating that microbes were not N limited, and no plant-mediated N addition effects occurred. Additionally, we show that both warming and soil C depletion were responsible for the microbial biomass loss. Soil warming caused stronger loss in microbial groups with higher 13C uptake. In our experiment, warming caused a general reduction of microbial biomass, despite a relative increase in microbial 13C uptake, and altered microbial community composition. The warming effects on microbial biomass and community composition were partly mediated through soil C depletion with warming and changes in recent plant-derived C uptake patterns of the microbial community.

  • Decay of similarity across tropical forest communities: integrating spatial distance with soil nutrients

    Peguero G, Ferrín M, Sardans J, Verbruggen E, Ramírez-Rojas I, Van Langenhove L, Verryckt LT, Murienne J, Iribar A, Zinger L, Grau O, Orivel J, Stahl C, Courtois EA, Asensio D, Gargallo-Garriga A, Llusià J, Margalef O, Ogaya R, Richter A, Janssens IA, Peñuelas J
    2022 - Ecology, 103: Article e03599


    Understanding the mechanisms that drive the change of biotic assemblages over space and time is the main quest of community ecology. Assessing the relative importance of dispersal and environmental species selection in a range of organismic sizes and motilities has been a fruitful strategy. A consensus for whether spatial and environmental distances operate similarly across spatial scales and taxa, however, has yet to emerge. We used censuses of four major groups of organisms (soil bacteria, fungi, ground insects, and trees) at two observation scales (1-m2 sampling point vs. 2,500-m2 plots) in a topographically standardized sampling design replicated in two tropical rainforests with contrasting relationships between spatial distance and nutrient availability. We modeled the decay of assemblage similarity for each taxon set and site to assess the relative contributions of spatial distance and nutrient availability distance. Then, we evaluated the potentially structuring effect of tree composition over all other taxa. The similarity of nutrient content in the litter and topsoil had a stronger and more consistent selective effect than did dispersal limitation, particularly for bacteria, fungi, and trees at the plot level. Ground insects, the only group assessed with the capacity of active dispersal, had the highest species turnover and the flattest nonsignificant distance−decay relationship, suggesting that neither dispersal limitation nor nutrient availability were fundamental drivers of their community assembly at this scale of analysis. Only the fungal communities at one of our study sites were clearly coordinated with tree composition. The spatial distance at the smallest scale was more important than nutrient selection for the bacteria, fungi, and insects. The lower initial similarity and the moderate variation in composition identified by these distance-decay models, however, suggested that the effects of stochastic sampling were important at this smaller spatial scale. Our results highlight the importance of nutrients as one of the main environmental drivers of rainforest communities irrespective of organismic or propagule size and how the overriding effect of the analytical scale influences the interpretation, leading to the perception of greater importance of dispersal limitation and ecological drift over selection associated with environmental niches at decreasing observation scales.

  • A high-spatial resolution soil carbon and nitrogen dataset for the northern permafrost region, based on circumpolar land cover upscaling

    Palmtag J, Obu J, Kuhry P, Richter A, Siewert MB, Weiss N, Westermann S, Hugelius G
    2022 - Earth Systems Science Data, 14: 4095–4110


    Soils in the northern high latitudes are a key component in the global carbon cycle; the northern permafrost region covers 22 % of the Northern Hemisphere land surface area and holds almost twice as much carbon as the atmosphere. Permafrost soil organic matter stocks represent an enormous long-term carbon sink which is in risk of switching to a net source in the future. Detailed knowledge about the quantity and the mechanisms controlling organic carbon storage is of utmost importance for our understanding of potential impacts of and feedbacks on climate change. Here we present a geospatial dataset of physical and chemical soil properties calculated from 651 soil pedons encompassing more than 6500 samples from 16 different study areas across the northern permafrost region. The aim of our dataset is to provide a basis to describe spatial patterns in soil properties, including quantifying carbon and nitrogen stocks. There is a particular need for spatially distributed datasets of soil properties, including vertical and horizontal distribution patterns, for modeling at local, regional, or global scales. This paper presents this dataset, describes in detail soil sampling; laboratory analysis, and derived soil geochemical parameters; calculations; and data clustering. Moreover, we use this dataset to estimate soil organic carbon and total nitrogen storage estimates in soils in the northern circumpolar permafrost region (17.9×106 km2) using the European Space Agency's (ESA's) Climate Change Initiative (CCI) global land cover dataset at 300 m pixel resolution. We estimate organic carbon and total nitrogen stocks on a circumpolar scale (excluding Tibet) for the 0–100 and 0–300 cm soil depth to be 380 and 813 Pg for carbon, and 21 and 55 Pg for nitrogen, respectively. Our organic carbon estimates agree with previous studies, with most recent estimates of 1000 Pg (−170 to +186 Pg) to 300 cm depth. Two separate datasets are freely available on the Bolin Centre Database repository (, Palmtag et al., 2022a; and, Palmtag et al., 2002b).

  • Dissolved organic matter characterization in soils and streams in a small coastal low-Arctic catchment

    Speetjens NJ, Tanski G, Martin V, Wagner J, Richter A, Hugelius G, Boucher C, Lodi R, Knoblauch C, Koch BP, Wünsch U, Lantuit H, Vonk JE
    2022 - Biogeosciences, 19: 3073-3097


    Ongoing climate warming in the western Canadian Arctic is leading to thawing of permafrost soils and subsequent mobilization of its organic matter pool. Part of this mobilized terrestrial organic matter enters the aquatic system as dissolved organic matter (DOM) and is laterally transported from land to sea. Mobilized organic matter is an important source of nutrients for ecosystems, as it is available for microbial breakdown, and thus a source of greenhouse gases. We are beginning to understand spatial controls on the release of DOM as well as the quantities and fate of this material in large Arctic rivers. Yet, these processes remain systematically understudied in small, high-Arctic watersheds, despite the fact that these watersheds experience the strongest warming rates in comparison. Here, we sampled soil (active layer and permafrost) and water (porewater and stream water) from a small ice wedge polygon (IWP) catchment along the Yukon coast, Canada, during the summer of 2018. We assessed the organic carbon (OC) quantity (using dissolved (DOC) and particulate OC (POC) concentrations and soil OC content), quality (δ13C DOC, optical properties and source apportionment) and bioavailability (incubations; optical indices such as slope ratio, Sr; and humification index, HIX) along with stream water properties (temperature, T; pH; electrical conductivity, EC; and water isotopes). We classify and compare different landscape units and their soil horizons that differ in microtopography and hydrological connectivity, giving rise to differences in drainage capacity. Our results show that porewater DOC concentrations and yield reflect drainage patterns and waterlogged conditions in the watershed. DOC yield (in mg DOC g−1 soil OC) generally increases with depth but shows a large variability near the transition zone (around the permafrost table). Active-layer porewater DOC generally is more labile than permafrost DOC, due to various reasons (heterogeneity, presence of a paleo-active-layer and sampling strategies). Despite these differences, the very long transport times of porewater DOC indicate that substantial processing occurs in soils prior to release into streams. Within the stream, DOC strongly dominates over POC, illustrated by 

     ratios around 50, yet storm events decrease that ratio to around 5. Source apportionment of stream DOC suggests a contribution of around 50 % from permafrost/deep-active-layer OC, which contrasts with patterns observed in large Arctic rivers (12 ± 8 %; Wild et al., 2019). Our 10 d monitoring period demonstrated temporal DOC patterns on multiple scales (i.e., diurnal patterns, storm events and longer-term trends), underlining the need for high-resolution long-term monitoring. First estimates of Black Creek annual DOC (8.2 ± 6.4 t DOC yr−1) and POC (0.21 ± 0.20 t yr−1) export allowed us to make a rough upscaling towards the entire Yukon Coastal Plain (34.51 ± 2.7 kt DOC yr−1 and 8.93 ± 8.5 kt POC yr−1). Rising Arctic temperatures, increases in runoff, soil organic matter (OM) leaching, permafrost thawing and primary production are likely to increase the net lateral OC flux. Consequently, altered lateral fluxes may have strong impacts on Arctic aquatic ecosystems and Arctic carbon cycling.

  • Lowland plant arrival in alpine ecosystems facilitates a decrease in soil carbon content under experimental climate warming

    Walker TWN, Gavazov K, Guillaume T, Lambert T, Mariotte P, Routh D, Signarbieux C, Block S, Münkemüller T, Nomoto H, Crowther TW, Richter A, Buttler A, Alexander JM
    2022 - eLife, 11: Article e78555


    Climate warming is releasing carbon from soils around the world, constituting a positive climate feedback. Warming is also causing species to expand their ranges into new ecosystems. Yet, in most ecosystems, whether range expanding species will amplify or buffer expected soil carbon loss is unknown. Here, we used two whole-community transplant experiments and a follow-up glasshouse experiment to determine whether the establishment of herbaceous lowland plants in alpine ecosystems influences soil carbon content under warming. We found that warming (transplantation to low elevation) led to a negligible decrease in alpine soil carbon content, but its effects became significant and 52% ± 31% (mean ± 95% confidence intervals) larger after lowland plants were introduced at low density into the ecosystem. We present evidence that decreases in soil carbon content likely occurred via lowland plants increasing rates of root exudation, soil microbial respiration, and CO2 release under warming. Our findings suggest that warming-induced range expansions of herbaceous plants have the potential to alter climate feedbacks from this system, and that plant range expansions among herbaceous communities may be an overlooked mediator of warming effects on carbon dynamics.

  • Lignin Preservation and Microbial Carbohydrate Metabolism in Permafrost Soils

    Dao TT, Mikutta R, Sauheitl L, Gentsch N, Shibistova O, Wild B, Schnecker J, Barta J, Capek P, Gittel A, Lashchinskiy N, Urich T, Santruckova H, Richter A, Guggenberger G
    2022 - JGR Biogeosciences, 127: Article e2020JG00618


    Permafrost-affected soils in the northern circumpolar region store more than 1,000 Pg soil organic carbon (OC), and are strongly vulnerable to climatic warming. However, the extent to which changing soil environmental conditions with permafrost thaw affects different compounds of soil organic matter (OM) is poorly understood. Here, we assessed the fate of lignin and non-cellulosic carbohydrates in density fractionated soils (light fraction, LF vs. heavy fraction, HF) from three permafrost regions with decreasing continentality, expanding from east to west of northern Siberia (Cherskiy, Logata, Tazovskiy, respectively). In soils at the Tazovskiy site with thicker active layers, the LF showed smaller OC-normalized contents of lignin-derived phenols and plant-derived sugars and a decrease of these compounds with soil depth, while a constant or even increasing trend was observed in soils with shallower active layers (Cherskiy and Logata). Also in the HF, soils at the Tazovskiy site had smaller contents of OC-normalized lignin-derived phenols and plant-derived sugars along with more pronounced indicators of oxidative lignin decomposition and production of microbial-derived sugars. Active layer deepening, thus, likely favors the decomposition of lignin and plant-derived sugars, that is, lignocelluloses, by increasing water drainage and aeration. Our study suggests that climate-induced degradation of permafrost soils may promote carbon losses from lignin and associated polysaccharides by abolishing context-specific preservation mechanisms. However, relations of OC-based lignin-derived phenols and sugars in the HF with mineralogical properties suggest that future OM transformation and carbon losses will be modulated in addition by reactive soil minerals.

  • Negative priming of soil organic matter following long-term in situ warming of sub-arctic soils

    Verbrigghe N, Meeran K, Bahn M, Fuchslueger L, Janssens IA, Richter A, Sigurdsson BD, Soong JL, Vicca A
    2022 - Geoderma, 410: Article 115652


    Priming is the change of microbial soil organic matter (SOM) decomposition induced by a labile carbon (C) source. It is recognised as an important mechanism influencing soil C dynamics and C storage in terrestrial ecosystems. Microbial nitrogen (N) mining in SOM and preferential substrate utilisation, i.e., a shift in microbial carbon use from SOM to more labile energy sources, are possible, counteracting, mechanisms driving the priming effect. Climate warming and increased N availability might affect these mechanisms, and thus determine the direction and magnitude of the priming effect. Hence, these abiotic factors can indirectly affect soil C stocks, which makes their understanding crucial for predicting the soil C feedback in a warming world. We conducted a short-term incubation experiment (6 days) with soils from a subarctic grassland that had been subjected to long-term geothermal warming (

    >55 years) by 2-4°C above unwarmed soil. Soil samples were amended with 13C-labelled glucose and 15N-labelled NH4NO3. We found a significantly negative relationship between in situ warming and cumulative primed C, with negative priming in the warmed soils. The negative priming suggests that preferential substrate utilisation was a key mechanism in our experiment. Our results indicate that changes in SOM characteristics associated with the in situ warming gradient can play a major role in determining the rate and direction of the priming effect. Additionally, we found that neither microbial N limitation nor N addition affected the priming effect, providing evidence that in our experiment, N mining did not lead to positive priming.

  • Impaired mucosal homeostasis in short-term fiber deprivation is due to reduced mucus production rather than overgrowth of mucus-degrading bacteria

    Overbeeke A, Lang M, Hausmann B, Watzka M, Nikolov G, Schwarz J, Kohl G, De Paepe K, Eislmayr K, Decker T, Richter A, Berry D
    2022 - Nutrients, 14: Article 3802


    The gut mucosal environment is key in host health; protecting against pathogens and providing a niche for beneficial bacteria, thereby facilitating a mutualistic balance between host and microbiome. Lack of dietary fiber results in erosion of the mucosal layer, suggested to be a result of increased mucus-degrading gut bacteria. This study aimed to use quantitative analyses to investigate the diet-induced imbalance of mucosal homeostasis. Seven days of fiber-deficiency affected intestinal anatomy and physiology, seen by reduced intestinal length and loss of the colonic crypt-structure. Moreover, the mucus layer was diminished, muc2 expression decreased, and impaired mucus secretion was detected by stable isotope probing. Quantitative microbiome profiling of the gut microbiota showed a diet-induced reduction in bacterial load and decreased diversity across the intestinal tract, including taxa with fiber-degrading and butyrate-producing capabilities. Most importantly, there was little change in the absolute abundance of known mucus-degrading bacteria, although, due to the general loss of taxa, relative abundance would erroneously indicate an increase in mucus degraders. These findings underscore the importance of using quantitative methods in microbiome research, suggesting erosion of the mucus layer during fiber deprivation is due to diminished mucus production rather than overgrowth of mucus degraders. View Full-Text

  • Soil carbon loss in warmed subarctic grasslands is rapid and restricted to topsoil

    Verbrigghe N, Leblans NIW, Sigurdsson BD, Vicca S, Fang C, Fuchslueger L, Soong JL, Weedon JT, Poeplau C, Ariza-Carricondo C, Bahn M, Guenet B, Gundersen P, Gunnarsdóttir GE, Kätterer T, Liu Z, Maljanen M, Marañon-Jimenez S, Meeran K, Oddsdóttir ES, Ostonen I, Peñuelas J, Richter A, Sardans J, Sigurðsson P, Torn MS, Van Bodegom PM, Verbruggen E, Walker TWN, Wallander H, Janssens IA
    2022 - Biogeosciences, 19: 3381-3393


    Global warming may lead to carbon transfers from soils to the atmosphere, yet this positive feedback to the climate system remains highly uncertain, especially in subsoils (Ilyina and Friedlingstein2016Shi et al.2018). Using natural geothermal soil warming gradients of up to +6.4C in subarctic grasslands (Sigurdsson et al.2016), we show that soil organic carbon (SOC) stocks decline strongly and linearly with warming (−2.8 t ha−1C−1). Comparison of SOC stock changes following medium-term (5 and 10 years) and long-term (>50 years) warming revealed that all SOC stock reduction occurred within the first 5 years of warming, after which continued warming no longer reduced SOC stocks. This rapid equilibration of SOC observed in Andosol suggests a critical role for ecosystem adaptations to warming and could imply short-lived soil carbon–climate feedbacks. Our data further revealed that the soil C loss occurred in all aggregate size fractions and that SOC stock reduction was only visible in topsoil (0–10 cm). SOC stocks in subsoil (10–30 cm), where plant roots were absent, showed apparent conservation after >50 years of warming. The observed depth-dependent warming responses indicate that explicit vertical resolution is a prerequisite for global models to accurately project future SOC stocks for this soil type and should be investigated for soils with other mineralogies.

  • Down-regulation of the bacterial protein biosynthesis machinery in response to weeks, years, and decades of soil warming

    Söllinger A, Séneca J, Dahl MB, Motleleng LL, Prommer J, Verbruggen E, Sigurdsson BD, Janssens I, Peñuelas J, Urich T, Richter A, Tveit AT
    2022 - Science Advances, 12: eabm3230


    How soil microorganisms respond to global warming is key to infer future soil-climate feedbacks, yet poorly understood. Here, we applied metatranscriptomics to investigate microbial physiological responses to medium-term (8 years) and long-term (>50 years) subarctic grassland soil warming of +6°C. Besides indications for a community-wide up-regulation of centralmetabolic pathways and cell replication, we observed a down-regulation of the bacterial protein biosynthesis machinery in the warmed soils, coinciding with a lower microbial biomass, RNA, and soil substrate content. We conclude that permanently accelerated reaction rates at higher temperatures and reduced substrate concentrations result in cellular reduction of ribosomes, the macromolecular complexes carrying out protein biosynthesis. Later efforts to test this, including a short-term warming experiment (6 weeks, +6°C), further supported our conclusion. Down-regulating the protein biosynthesis machinery liberates energy and matter, allowing soil bacteria to maintain high metabolic activities and cell division rates even after decades of warming.

  • Responses of grassland soil CO2 production and fluxes to drought are shifted in a warmer climate under elevated CO2

    Reinthaler D, Harris E, Richter A, Herndl M, Pötsch E, Wachter H, Bahn M
    2021 - Soil Biology and Biochemistry, 163: Article 108436


    As the climate warms, drought events are expected to increase in intensity and frequency, with consequences for the carbon cycleSoil respiration (Rs) accounts for the largest flux of CO2 from terrestrial ecosystems to the atmosphere. While the drought responses of Rs have been well studied, it is uncertain how they will be modified in a future world, when higher temperatures will occur in combination with elevated atmospheric CO2 concentrations. In a global change experiment in a managed temperate grassland, we studied drought and post-drought responses of Rs dynamics under current versus likely future conditions (+3°, +300 ppm CO2). Furthermore, to understand the soil CO2 production (Ps) and transport dynamics underlying Rs fluxes we continuously monitored in-situ soil CO2 concentrations across the soil profile. Our results show that Rs was higher and that drought-induced reductions in Rs were delayed under future compared to current conditions. Peak drought reductions and post-drought pulses of Rs were more pronounced in the future scenario. Annual Rs was reduced by drought only under current but not under future conditions. An in-depth analysis of soil CO2 gradients and fluxes across the soil profile showed that elevated CO2 stimulated Ps primarily in the main rooting horizon and that warming affected Ps also in deeper soil layers. We found that both in the current and the future scenario drought led to the strongest reductions of Ps in the most productive soil layers, which also exhibited the largest depletion of soil moisture. We conclude that a future warmer climate under elevated CO2 amplifies soil CO2 production and efflux and their peak drought and post-drought responses, but delays the onset of the drought responses and thereby eliminates the overall drought effect on annual soil CO2 emissions.

  • Microbial responses to herbivory-induced vegetation changes in a high-Arctic peatland

    Bender KM, Svenning MM, Hu Y, Richter A, Schückel J, Liebner S, Tveit AT
    2021 - Polar Biology, 44: 899-911


    Herbivory by barnacle geese (Branta leucopsis) alters the vegetation cover and reduces ecosystem productivity in high-Arctic peatlands, limiting the carbon sink strength of these ecosystems. Here we investigate how herbivory-induced vegetation changes affect the activities of peat soil microbiota using metagenomics, metatranscriptomics and targeted metabolomics in a comparison of fenced exclosures and nearby grazed sites. Our results show that a different vegetation with a high proportion of vascular plants developed due to reduced herbivory, resulting in a larger and more diverse input of polysaccharides to the soil at exclosed study sites. This coincided with higher sugar and amino acid concentrations in the soil at this site as well as the establishment of a more abundant and active microbiota, including saprotrophic fungi with broad substrate ranges, like Helotiales (Ascomycota) and Agaricales (Basidiomycota). A detailed description of fungal transcriptional profiles revealed higher gene expression for cellulose, hemicellulose, pectin, lignin and chitin degradation at herbivory-exclosed sites. Furthermore, we observed an increase in the number of genes and transcripts for predatory eukaryotes such as Entomobryomorpha (Arthropoda). We conclude that in the absence of herbivory, the development of a vascular vegetation alters the soil polysaccharide composition and supports larger and more active populations of fungi and predatory eukaryotes.

  • A critical perspective on interpreting amplicon sequencing data in soil ecological research

    Alteio L, Séneca J, Canarini A, Angel R, Jansa J, Guseva K, Kaiser C, Richter A, Schmidt H
    2021 - Soil Biology and Biochemistry, 160: Article 108357


    Microbial community analysis via marker gene amplicon sequencing has become a routine method in the field of soil research. In this perspective, we discuss technical challenges and limitations of amplicon sequencing and present statistical and experimental approaches that can help addressing the spatio-temporal complexity of soil and the high diversity of organisms therein. We illustrate the impact of compositionality on the interpretation of relative abundance data and discuss effects of sample replication on the statistical power in soil community analysis. Additionally, we argue for the need of increased study reproducibility and data availability, as well as complementary techniques for generating deeper ecological insights into microbial roles and our understanding thereof in soil ecosystems. At this stage, we call upon researchers and specialized soil journals to consider the current state of data analysis, interpretation, and availability to improve the rigor of future studies.

  • Increased microbial expression of organic nitrogen cycling genes in long-term warmed grassland soils

    Séneca J, Söllinger A, Herbold C, Pjevac P, Prommer J, Verbruggen E, Sigurdssaon BD, Peñuelas J, Janssens IA, Urich T, Tveit AT, Richter A
    2021 - ISME Communications, 1: Article 69


    Global warming increases soil temperatures and promotes faster growth and turnover of soil microbial communities. As microbial cell walls contain a high proportion of organic nitrogen, a higher turnover rate of microbes should also be reflected in an accelerated organic nitrogen cycling in soil. We used a metatranscriptomics and metagenomics approach to demonstrate that the relative transcription level of genes encoding enzymes involved in the extracellular depolymerization of high-molecular-weight organic nitrogen was higher in medium-term (8 years) and long-term (>50 years) warmed soils than in ambient soils. This was mainly driven by increased levels of transcripts coding for enzymes involved in the degradation of microbial cell walls and proteins. Additionally, higher transcription levels for chitin, nucleic acid, and peptidoglycan degrading enzymes were found in long-term warmed soils. We conclude that an acceleration in microbial turnover under warming is coupled to higher investments in N acquisition enzymes, particularly those involved in the breakdown and recycling of microbial residues, in comparison with ambient conditions.

  • Permafrost causes unique fine-scale spatial variability across tundra soils

    Siewert MB., Lantuit H, Richter A, Hugelius G
    2021 - Global Biogeochemical Cycles, 35: e2020GB006659


    Spatial analysis in earth sciences is often based on the concept of spatial autocorrelation, expressed by W. Tobler as the first law of geography: “everything is related to everything else, but near things are more related than distant things." Here, we show that subsurface soil properties in permafrost tundra terrain exhibit tremendous spatial variability. We describe the subsurface variability of soil organic carbon (SOC) and ground ice content from the centimeter to the landscape scale in three typical tundra terrain types common across the Arctic region. At the soil pedon scale, that is, from centimeters to 1–2 m, variability is caused by cryoturbation and affected by tussocks, hummocks and nonsorted circles. At the terrain scale, from meters to tens of meters, variability is caused by different generations of ice‐wedges. Variability at the landscape scale, that is, ranging hundreds of meters, is associated with geomorphic disturbances and catenary shifts. The co‐occurrence and overlap of different processes and landforms creates a spatial structure unique to permafrost environments. The coefficient of variation of SOC at the pedon scale (21%–73%) exceeds that found at terrain (17%–66%) and even landscape scale (24%–67%). Such high values for spatial variation are otherwise found at regional to continental scale. Clearly, permafrost soils do not conform to Tobler's law, but are among the most variable soils on Earth. This needs to be accounted for in mapping and predictions of the permafrost carbon feedbacks through various ecosystem processes. We conclude that scale deserves special attention in permafrost regions.

  • Impact of Nutrient Additions on Free-Living Nitrogen Fixation in Litter and Soil of Two French-Guianese Lowland Tropical Forests

    Van Langenhove L, Depaepe T, Verryckt LT, Vallicrosa H, Fuchslueger L, Lugli LF, Bréchet L, Ogaya R, Llusià J, Urbina I, Gargallo-Garriga A, Grau O, Richter A, Peñuelas J, Van Der Straeten D, Janssens IA
    2021 - Journal of Geophysical Research: Biogeosciences, 126: Article e2020JG00602


    Lakes receive and transform significant amounts of terrestrial carbon and are often considered a source of atmospheric carbon dioxide (CO2). Yet, continuous direct measurements of lake-atmosphere CO2 exchange with high temporal resolution are sparse. In this study, we measured the CO2 exchange of a mountain lake in the eastern Austrian Alps continuously for one year using the eddy covariance (EC) and the boundary layer model (BLM) approaches. Results from both the EC and the BLM methods indicated the lake to be a small source of atmospheric CO2 with highest emissions in fall. EC flux measurements were affected by low-frequency contributions especially during low wind conditions. The CO2 concentration gradient at the air-water interface decreased during night-time due to an increase in atmospheric CO2 above the lake, likely caused by cold and CO2-rich air draining from the surrounding land. Consequently, BLM fluxes were lower during night-time than during daytime. This diel pattern was lacking in the EC flux measurements because the EC instruments deployed at the shore of the lake did not capture low nocturnal lake CO2 fluxes due to the local wind regime. Overall, this study illustrates the effect of the surrounding landscape on lake-atmosphere flux measurements. We conclude that estimating CO2 evasion from lakes situated in complex topography needs to explicitly account for biases in EC flux measurements caused by low-frequency contributions and local wind regimes.

  • Genomic insights into diverse bacterial taxa that degrade extracellular DNA in marine sediments 

    Wasmund K, Pelikan C, Schintlmeister A, Wagner M, Watzka M, Richter A, Bhatnagar S, Noel A, Hubert CRJ, Rattei T, Hofmann T, Hausmann B, Herbold CW, Loy A
    2021 - Nature Microbiology, 6: 885-898


    While best known as the code for genetic information, DNA is also a nutrient for specialised microbes. An international team of researchers led by Ken and Alex from DOME has discovered several bacteria in sediment samples from the Atlantic Ocean that use DNA as a food source. One bacterium newly named by the team in fact is a true expert in degrading DNA. The study provides new insights into the diversity and ecological function of the still largely undescribed microscopic world in the oceans.

  • Cyanate is a low abundance but actively cycled nitrogen compound in soil

    Mooshammer M, Wanek W, Jones S, Richter A, Wagner W
    2021 - Communications Earth & Environment, 2: Article 161


    Cyanate can serve as a nitrogen and/or carbon source for different microorganisms and as an energy source for autotrophic ammonia oxidizers. However, the extent of cyanate availability and utilisation in terrestrial ecosystems and its role in biogeochemical cycles is poorly known. Here we analyse cyanate concentrations in soils across a range of soil types, land management practices and climates. Soil cyanate concentrations were three orders of magnitude lower than ammonium or nitrate. We determined cyanate consumption in a grassland and rice paddy soil using stable isotope tracer experiments. We find that cyanate turnover was rapid and dominated by biotic processes. We estimated that in-situ cyanate production rates were similar to those associated with urea fertilizer decomposition, a major source of cyanate in the environment. We provide evidence that cyanate is actively turned over in soils and represents a small but continuous nitrogen/energy source for soil microbes.

  • Ecological memory of recurrent drought modifies soil processes via changes in soil microbial community

    Canarini A, Schmidt H, Fuchslueger L, Martin V, Herbold CW, Zezula D, Gündler P, Hasibeder R, Jecmenica M, Bahn M, Richter A
    2021 - Nature Communications, 12: Article 5308


    Climate change is altering the frequency and severity of drought events. Recent evidence indicates that drought may produce legacy effects on soil microbial communities. However, it is unclear whether precedent drought events lead to ecological memory formation, i.e., the capacity of past events to influence current ecosystem response trajectories. Here, we utilize a long-term field experiment in a mountain grassland in central Austria with an experimental layout comparing 10 years of recurrent drought events to a single drought event and ambient conditions. We show that recurrent droughts increase the dissimilarity of microbial communities compared to control and single drought events, and enhance soil multifunctionality during drought (calculated via measurements of potential enzymatic activities, soil nutrients, microbial biomass stoichiometry and belowground net primary productivity). Our results indicate that soil microbial community composition changes in concert with its functioning, with consequences for soil processes. The formation of ecological memory in soil under recurrent drought may enhance the resilience of ecosystem functioning against future drought events.

  • How can fertilization regimes and durations shape earthworm gut microbiota in a long-term field experiment?

    Bi Q-F, Jin B-J, Zhu D, Jiang Y-G, Zheng B-X, O’Connor P, Yang X-R, Richter A, Lin X-Y, Zhu Y-H 
    2021 - Ecotoxicology and Environmental Safety, 224: Article 112643


    The positive roles of earthworms on soil functionality has been extensively documented. The capacity of the earthworm gut microbiota on decomposition and nutrient cycling under long-term fertilization in field conditions has rarely been studied. Here, we report the structural, taxonomic, and functional responses of Eisenia foetida and Pheretima guillelmi gut microbiota to different fertilization regimes and durations using 16S rRNA gene-based Illumina sequencing and high-throughput quantitative PCR techniques. Our results revealed that the core gut microbiota, especially the fermentative bacteria were mainly sourced from the soil, but strongly stimulated with species-specificity, potential benefits for the host and soil health. The functional compositions of gut microbiota were altered by fertilization with fertilization duration being more influential than fertilization regimes. Moreover, the combination of organic and inorganic fertilization with the longer duration resulted in a higher richness and connectivity in the gut microbiota, and also their functional potential related to carbon (C), nitrogen, and phosphorus cycling, particularly the labile C decomposition, denitrification, and phosphate mobilization. We also found that long-term inorganic fertilization increased the abundance of pathogenic bacteria in the P. guillelmi gut. This study demonstrates that understanding earthworm gut microbiota can provide insights into how agricultural practices can potentially alte

  • The effect of global change on soil phosphatase activity

    Margalef O, Sardans J, Maspons J, Molowny-Horas R, Fernández-Martínez M, Janssens IA, Ciais P, Richter A, Obersteiner M, Peñuelas J
    2021 - Global Change Biology, 27: 5681-6003


    Soil phosphatase enzymes are produced by plant roots and microorganisms and play a key role in the cycling of phosphorus (P), an often-limiting element in terrestrial ecosystems. The production of these enzymes in soil is the most important biological strategy for acquiring phosphate ions from organic molecules. Previous works showed how soil potential phosphatase activity is mainly driven by climatic conditions and soil nitrogen (N) and carbon. Nonetheless, future trends of the activity of these enzymes under global change remain little known. We investigated the influence of some of the main drivers of change on soil phosphatase activity using a meta-analysis of results from 97 published studies. Our database included a compilation of N and P fertilization experiments, manipulation experiments with increased atmospheric CO2 concentration, warming, and drought, and studies comparing invaded and non-invaded ecosystems. Our results indicate that N fertilization leads to higher phosphatase activity, whereas P fertilization has the opposite effect. The rise of atmospheric CO2 levels or the arrival of invasive species also exhibits positive response ratios on the activity of soil phosphatases. However, the occurrence of recurrent drought episodes decreases the activity of soil phosphatases. Our analysis did not reveal statistically significant effects of warming on soil phosphatase activity. In general, soil enzymatic changes in the reviewed experiments depended on the initial nutrient and water status of the ecosystems. The observed patterns evidence that future soil phosphatase activity will not only depend on present-day soil conditions but also on potential compensations or amplifications among the different drivers of global change. The responses of soil phosphatases to the global change drivers reported in this study and the consideration of cost–benefit approaches based on the connection of the P and N cycle will be useful for a better estimation of phosphatase production in carbon (C)–N–P models.

  • Shifts in the abundances of saprotrophic and ectomycorrhizal fungi at altered leaf litter inputs

    Marañon-Jimenez S, Radujkovic D, Verbruggen E, Grau O, Cuntz M, Peñuelas J, Richter A, Schrumpf M, Rebmann C
    2021 - Frontiers in Plant Science, 12: Article 682142


    Ectomycorrhizal (EcM) and saprotrophic fungi interact in the breakdown of organic matter, but the mechanisms underlying the EcM role on organic matter decomposition are not totally clear. We hypothesized that the ecological relations between EcM and saprotroph fungi are modulated by resources availability and accessibility, determining decomposition rates. We manipulated the amount of leaf litter inputs (No-Litter, Control Litter, Doubled Litter) on Trenched (root exclusion) and Non-Trenched plots (with roots) in a temperate deciduous forest of EcM-associated trees. Resultant shifts in soil fungal communities were determined by phospholipid fatty acids and DNA sequencing after 3 years, and CO2 fluxes were measured throughout this period. Different levels of leaf litter inputs generated a gradient of organic substrate availability and accessibility, altering the composition and ecological relations between EcM and saprotroph fungal communities. EcM fungi dominated at low levels of fresh organic substrates and lower organic matter quality, where short-distances exploration types seem to be better competitors, whereas saprotrophs and longer exploration types of EcM fungi tended to dominate at high levels of leaf litter inputs, where labile organic substrates were easily accessible. We were, however, not able to detect unequivocal signs of competition between these fungal groups for common resources. These results point to the relevance of substrate quality and availability as key factors determining the role of EcM and saprotroph fungi on litter and soil organic matter decay and represent a path forward on the capacity of organic matter decomposition of different exploration types of EcM fungi.

  • Recently photoassimilated carbon and fungus-deliverd nitrogen are spatially correlated in the ectomycorrhizal tissue of Fagus sylvatica

    Mayerhofer W, Schintelmeister A, Dietrich M, Gorka S, Wiesenbauer J, Martin V, Gabriel R, Reipert S, Weidinger M, Clode P, Wagner M, Wöbken D, Richter A, Kaiser C
    2021 - New Phytologist, 232: 2457-2474


    Ectomycorrhizal plants trade plant-assimilated carbon for soil nutrients with their fungal partners. The underlying mechanisms, however, are not fully understood. Here we investigate the exchange of carbon for nitrogen in the ectomycorrhizal symbiosis of Fagus sylvatica across different spatial scales from the root system to the cellular level. We provided 15 N-labelled nitrogen to mycorrhizal hyphae associated with one half of the root system of young beech trees, while exposing plants to a 13 CO2 atmosphere. We analysed the short-term distribution of 13 C and 15 N in the root system with isotope-ratio mass spectrometry, and at the cellular scale within a mycorrhizal root tip with nanoscale secondary ion mass spectrometry (NanoSIMS). At the root system scale, plants did not allocate more 13 C to root parts that received more 15 N. Nanoscale secondary ion mass spectrometry imaging, however, revealed a highly heterogenous, and spatially significantly correlated distribution of 13 C and 15 N at the cellular scale. Our results indicate that, on a coarse scale, plants do not allocate a larger proportion of photoassimilated C to root parts associated with N-delivering ectomycorrhizal fungi. Within the ectomycorrhizal tissue, however, recently plant-assimilated C and fungus-delivered N were spatially strongly coupled. Here, NanoSIMS visualisation provides an initial insight into the regulation of ectomycorrhizal C and N exchange at the microscale.

  • Warming and elevated CO2 intensify drought and recovery responses of grassland carbon allocation to soil respiration

    Meeran K, Ingrisch J, Reinthaler D, Canarini A, Müller L, Pötsch E, Richter A, Wanek W, Bahn M
    2021 - Global Change Biology, 27: 3230-3243


    Photosynthesis and soil respiration represent the two largest fluxes of CO2 in terrestrial ecosystems and are tightly linked through belowground carbon (C) allocation. Drought has been suggested to impact the allocation of recently assimilated C to soil respiration; however, it is largely unknown how drought effects are altered by a future warmer climate under elevated atmospheric CO2 (eT_eCO2). In a multifactor experiment on managed C3 grassland, we studied the individual and interactive effects of drought and eT_eCO2 (drought, eT_eCO2, drought × eT_eCO2) on ecosystem C dynamics. We performed two in situ 13CO2 pulse-labeling campaigns to trace the fate of recent C during peak drought and recovery. eT_eCO2 increased soil respiration and the fraction of recently assimilated C in soil respiration. During drought, plant C uptake was reduced by c. 50% in both ambient and eT_eCO2 conditions. Soil respiration and the amount and proportion of 13C respired from soil were reduced (by 32%, 70% and 30%, respectively), the effect being more pronounced under eT_eCO2 (50%, 84%, 70%). Under drought, the diel coupling of photosynthesis and SR persisted only in the eT_eCO2 scenario, likely caused by dynamic shifts in the use of freshly assimilated C between storage and respiration. Drought did not affect the fraction of recent C remaining in plant biomass under ambient and eT_eCO2, but reduced the small fraction remaining in soil under eT_eCO2. After rewetting, C uptake and the proportion of recent C in soil respiration recovered more rapidly under eT_eCO2 compared to ambient conditions. Overall, our findings suggest that in a warmer climate under elevated CO2 drought effects on the fate of recent C will be amplified and the coupling of photosynthesis and soil respiration will be sustained. To predict the future dynamics of terrestrial C cycling, such interactive effects of multiple global change factors should be considered.

  • Empirical support for the biogeochemical niche hypothesis in forest trees

    Sardans J, Vallicrosa H, Zuccarini P, Farré-Armengol G, Fernández-Martínez M, Guille P, Gargallo-Garriga A, Ciais P, Janssens IA, Obersteiner M, Richter A, Peñuelas J
    2021 - Nature Ecology & Evolution, 5: 184-194


    The possibility of using the elemental compositions of species as a tool to identify species/genotype niche remains to be tested at a global scale. We investigated relationships between the foliar elemental compositions (elementomes) of trees at a global scale with phylogeny, climate, N deposition and soil traits. We analysed foliar N, P, K, Ca, Mg and S concentrations in 23,962 trees of 227 species. Shared ancestry explained 60–94% of the total variance in foliar nutrient concentrations and ratios whereas current climate, atmospheric N deposition and soil type together explained 1–7%, consistent with the biogeochemical niche hypothesis which predicts that each species will have a specific need for and use of each bio-element. The remaining variance was explained by the avoidance of nutritional competition with other species and natural variability within species. The biogeochemical niche hypothesis is thus able to quantify species-specific tree niches and their shifts in response to environmental changes.

  • Acidobacteria are active and abundant members of diverse atmospheric H2-oxidizing communities detected in temperate soils

    Eichorst S, Giguere A, Meier D, Herbold C, Richter A, Greening C, Woebken D
    2021 - ISME Journal, 15: 363-376


    Significant rates of atmospheric dihydrogen (H2) consumption have been observed in temperate soils due to the activity of high-affinity enzymes, such as the group 1h [NiFe]-hydrogenase. We designed broadly inclusive primers targeting the large subunit gene (hhyL) of group 1h [NiFe]-hydrogenases for long-read sequencing to explore its taxonomic distribution across soils. This approach revealed a diverse collection of microorganisms harboring hhyL, including previously unknown groups and taxonomically not assignable sequences. Acidobacterial group 1h [NiFe]-hydrogenase genes were abundant and expressed in temperate soils. To support the participation of acidobacteria in H2 consumption, we studied two representative mesophilic soil acidobacteria, which expressed group 1h [NiFe]-hydrogenases and consumed atmospheric H2 during carbon starvation. This is the first time mesophilic acidobacteria, which are abundant in ubiquitous temperate soils, have been shown to oxidize H2 down to below atmospheric concentrations. As this physiology allows bacteria to survive periods of carbon starvation, it could explain the success of soil acidobacteria. With our long-read sequencing approach of group 1h [NiFe]-hydrogenase genes, we show that the ability to oxidize atmospheric levels of H2 is more widely distributed among soil bacteria than previously recognized and could represent a common mechanism enabling bacteria to persist during periods of carbon deprivation.

  • Lability classification of soil organic matter in the northern permafrost region

    Kuhry P, Barta J, Blok D, Elberling B, Faucherre S, Hugelius G, Jørgensen C J, Richter A, Santruckova H, Weiss N
    2020 - Biogeosciences, 17: 361-379


    The large stocks of soil organic carbon (SOC) in soils and deposits of the northern permafrost region are sensitive to global warming and permafrost thawing. The potential release of this carbon (C) as greenhouse gases to the atmosphere does not only depend on the total quantity of soil organic matter (SOM) affected by warming and thawing, but it also depends on its lability (i.e., the rate at which it will decay). In this study we develop a simple and robust classification scheme of SOM lability for the main types of soils and deposits in the northern permafrost region. The classification is based on widely available soil geochemical parameters and landscape unit classes, which makes it useful for upscaling to the entire northern permafrost region. We have analyzed the relationship between C content and C-CO2 production rates of soil samples in two different types of laboratory incubation experiments. In one experiment, ca. 240 soil samples from four study areas were incubated using the same protocol (at 5 C, aerobically) over a period of 1 year. Here we present C release rates measured on day 343 of incubation. These long-term results are compared to those obtained from short-term incubations of ca. 1000 samples (at 12 C, aerobically) from an additional three study areas. In these experiments, C-CO2 production rates were measured over the first 4 d of incubation. We have focused our analyses on the relationship between C-CO2 production per gram dry weight per day (µgC-CO2 gdw−1 d−1) and C content (%C of dry weight) in the samples, but we show that relationships are consistent when using C ∕ N ratios or different production units such as µgC per gram soil C per day (µgC-CO2 gC−1 d−1) or per cm3 of soil per day (µgC-CO2 cm−3 d−1). C content of the samples is positively correlated to C-CO2 production rates but explains less than 50 % of the observed variability when the full datasets are considered. A partitioning of the data into landscape units greatly reduces variance and provides consistent results between incubation experiments. These results indicate that relative SOM lability decreases in the order of Late Holocene eolian deposits to alluvial deposits and mineral soils (including peaty wetlands) to Pleistocene yedoma deposits to C-enriched pockets in cryoturbated soils to peat deposits. Thus, three of the most important SOC storage classes in the northern permafrost region (yedoma, cryoturbated soils and peatlands) show low relative SOM lability. Previous research has suggested that SOM in these pools is relatively undecomposed, and the reasons for the observed low rates of decomposition in our experiments need urgent attention if we want to better constrain the magnitude of the thawing permafrost carbon feedback on global warming.

  • Assessing microbial residues in soil as a potential carbon sink and moderator of carbon use efficiency

    Geyer K, Schnecker J, Grand AS, Richter A, Frey S
    2020 - Biogeochemistry, 151: 237-249


    A longstanding assumption of glucose tracing experiments is that all glucose is microbially utilized during short incubations of ≤2 days to become microbial biomass or carbon dioxide. Carbon use efficiency (CUE) estimates have consequently ignored the formation of residues (non-living microbial products) although such materials could represent an important sink of glucose that is prone to stabilization as soil organic matter. We examined the dynamics of microbial residue formation from a short tracer experiment with frequent samplings over 72 h, and conducted a meta-analysis of previously published glucose tracing studies to assess the generality of these experimental results. Both our experiment and meta-analysis indicated 30–34% of amended glucose-C (13C or 14C) was in the form of residues within the first 6 h of substrate addition. We expand the conventional efficiency calculation to include residues in both the numerator and denominator of efficiency, thereby deriving a novel metric of the potential persistence of glucose-C in soil as living microbial biomass plus residues (‘carbon stabilization efficiency’). This new metric indicates nearly 40% of amended glucose-C persists in soil 180 days after amendment, the majority as non-biomass residues. Starting microbial biomass and clay content emerge as critical factors that positively promote such long term stabilization of labile C. Rapid residue production supports the conclusion that non-growth maintenance activity can illicit high demands for C in soil, perhaps equaling that directed towards growth, and that residues may have an underestimated role in the cycling and sequestration potential of C in soil.

  • C:N:P stoichiometry regulates soil organic carbon mineralization and concomitant shifts in microbial community composition in paddy soil

    Wei X, Zhu Z, Liu Y, Luo Y, Deng Y, Xu X, Liu S, Richter A, Shibistova O, Guggenberger G, Wu J, Ge T
    2020 - Biology and Fertility of Soils, 56: 1093-1107


    Stoichiometric control of input substrate (glucose) and native soil organic C (SOC) mineralization was assessed by performing a manipulation experiment based on N or P fertilization in paddy soil. Glucose mineralization increased with nutrient addition up to 11.6% with combined N and P application compared with that without nutrient addition. During 100 days of incubation, approximately 4.5% of SOC was mineralized and was stimulated by glucose addition. Glucose and SOC mineralization increased exponentially with dissolved organic C (DOC):NH4+-N, DOC:Olsen P, and microbial biomass (MB)C:MBN ratios. The relative abundances of Clostridia and β-Proteobacteria (r-strategists) were increased with combined C and NP application at the beginning of the experiment, while the relative abundances of Acidobacteria (K-strategists) were enhanced with the exhaustion of available resource at the end of incubation. The bacteria abundance and diversity were negatively related to the DOC:NH4+-N and DOC:Olsen P, which had direct positive effects (+ 0.63) on SOC mineralization. Combined glucose and NP application decreased the network density of the bacterial community. Moreover, P addition significantly decreased the negative associations among bacterial taxa, which suggested that microbial competition for nutrients was alleviated. The relative abundances of keystone species showed significant positive correlations with SOC mineralization in the soils without P application, revealing that microbes increased their activity for mining of limited nutrients from soil organic matter. Hence, bacteria shifted their community composition and their interactions to acquire necessary elements by increasing SOC mineralization to maintain the microbial biomass C:N:P stoichiometric balance in response to changes in resource stoichiometry.

  • Increased microbial growth, biomass, and turnover drive soil organic carbon accumulation at higher plant diversity

    Prommer J, Walker TWN, Wanek W, Braun J, Zezula D, Hu Y, Hofhansl F, Richter A
    2020 - Global Change Biology, 2: 669-681


    Species‐rich plant communities have been shown to be more productive and to exhibit increased long‐term soil organic carbon (SOC) storage. Soil microorganisms are central to the conversion of plant organic matter into SOC, yet the relationship between plant diversity, soil microbial growth, turnover as well as carbon use efficiency (CUE) and SOC accumulation is unknown. As heterotrophic soil microbes are primarily carbon limited, it is important to understand how they respond to increased plant‐derived carbon inputs at higher plant species richness (PSR). We used the long‐term grassland biodiversity experiment in Jena, Germany, to examine how microbial physiology responds to changes in plant diversity and how this affects SOC content. The Jena Experiment considers different numbers of species (1–60), functional groups (1–4) as well as functional identity (small herbs, tall herbs, grasses, and legumes). We found that PSR accelerated microbial growth and turnover and increased microbial biomass and necromass. PSR also accelerated microbial respiration, but this effect was less strong than for microbial growth. In contrast, PSR did not affect microbial CUE or biomass‐specific respiration. Structural equation models revealed that PSR had direct positive effects on root biomass, and thereby on microbial growth and microbial biomass carbon. Finally, PSR increased SOC content via its positive influence on microbial biomass carbon. We suggest that PSR favors faster rates of microbial growth and turnover, likely due to greater plant productivity, resulting in higher amounts of microbial biomass and necromass that translate into the observed increase in SOC. We thus identify the microbial mechanism linking species‐rich plant communities to a carbon cycle process of importance to Earth's climate system.

  • A systemic overreaction to years versus decades of warming in a subarctic grassland ecosystem

    Walker TWN, Janssens IA, Weedon JT, Sigurdsson BD, Richter A, Peñuelas J, Leblans NI Bahn M, Bartrons M, De Jonge C, Fuchslueger L, Gargallo-Garriga A, Gunnarsdóttir GE, Marañon-Jimenez S, Oddsdóttir ES, Ostonen I, Poeplau C, Prommer J, Radujković D, Sardans J, Sigurðsson P, Soong JL, Vicca S, Wallander H, Ilieva-Makulec K, Verbruggen E
    2020 - Nature Ecology & Evolution, 4: 101-108


    Temperature governs most biotic processes, yet we know little about how warming affects whole ecosystems. Here we examined the responses of 128 components of a subarctic grassland to either 5–8 or >50 years of soil warming. Warming of >50 years drove the ecosystem to a new steady state possessing a distinct biotic composition and reduced species richness, biomass and soil organic matter. However, the warmed state was preceded by an overreaction to warming, which was related to organism physiology and was evident after 5–8 years. Ignoring this overreaction yielded errors of >100% for 83 variables when predicting their responses to a realistic warming scenario of 1 °C over 50 years, although some, including soil carbon content, remained stable after 5–8 years. This study challenges long-term ecosystem predictions made from short-term observations, and provides a framework for characterization of ecosystem responses to sustained climate change.

  • Regulation of nitrogen fixation from free-living organisms in soil and leaf litter of two tropical forests of the Guiana shield

    Van Langenhove L, Depaepe T, Vicca S, Van den Berge J, Stahl C, Courtois E, Weedon J, Urbina I, Grau O, Asensio D, Peñuelas J, Boeckx P, Richter A, Van Der Straeten D, Janssens IA
    2020 - Plant and soil, 450: 93-110


    Background and aims

    Biological fixation of atmospheric nitrogen (N2) is the main pathway for introducing N into unmanaged ecosystems. While recent estimates suggest that free-living N fixation (FLNF) accounts for the majority of N fixed in mature tropical forests, the controls governing this process are not completely understood. The aim of this study was to quantify FLNF rates and determine its drivers in two tropical pristine forests of French Guiana.


    We used the acetylene reduction assay to measure FLNF rates at two sites, in two seasons and along three topographical positions, and used regression analyses to identify which edaphic explanatory variables, including carbon (C), nitrogen (N), phosphorus (P) and molybdenum (Mo) content, pH, water and available N and P, explained most of the variation in FLNF rates.


    Overall, FLNF rates were lower than measured in tropical systems elsewhere. In soils seasonal variability was small and FLNF rates differed among topographies at only one site. Water, P and pH explained 24% of the variation. In leaf litter, FLNF rates differed seasonally, without site or topographical differences. Water, C, N and P explained 46% of the observed variation. We found no regulatory role of Mo at our sites.


    Rates of FLNF were low in primary rainforest on poor soils on the Guiana shield. Water was the most important rate-regulating factor and FLNF increased with increasing P, but decreased with increasing N. Our results support the general assumption that N fixation in tropical lowland forests is limited by P availability.

  • Microbial carbon limitation: The need for integrating microorganisms into our understanding of ecosystem carbon cycling

    Soong JL, Fuchslueger L, Marañon‐Jimenez S, Torn MS, Janssens IA, Peñuelas J, Richter A
    2020 - Global Change Biology, 4: 1953-1961


    Numerous studies have demonstrated that fertilization with nutrients such as nitrogen, phosphorus, and potassium increases plant productivity in both natural and managed ecosystems, demonstrating that primary productivity is nutrient limited in most terrestrial ecosystems. In contrast, it has been demonstrated that heterotrophic microbial communities in soil are primarily limited by organic carbon or energy. While this concept of contrasting limitations, that is, microbial carbon and plant nutrient limitation, is based on strong evidence that we review in this paper, it is often ignored in discussions of ecosystem response to global environment changes. The plant‐centric perspective has equated plant nutrient limitations with those of whole ecosystems, thereby ignoring the important role of the heterotrophs responsible for soil decomposition in driving ecosystem carbon storage. To truly integrate carbon and nutrient cycles in ecosystem science, we must account for the fact that while plant productivity may be nutrient limited, the secondary productivity by heterotrophic communities is inherently carbon limited. Ecosystem carbon cycling integrates the independent physiological responses of its individual components, as well as tightly coupled exchanges between autotrophs and heterotrophs. To the extent that the interacting autotrophic and heterotrophic processes are controlled by organisms that are limited by nutrient versus carbon accessibility, respectively, we propose that ecosystems by definition cannot be ‘limited’ by nutrients or carbon alone. Here, we outline how models aimed at predicting non‐steady state ecosystem responses over time can benefit from dissecting ecosystems into the organismal components and their inherent limitations to better represent plant–microbe interactions in coupled carbon and nutrient models.

  • Carbon loss from northern circumpolar permafrost soils amplified by rhizosphere priming

    Keuper F, Wild B, Kummu M, Beer C, Blume-Werry G, Fontaine S, Gavazov K, Gentsch N, Guggenberger G, Hugelius G, Jalava M, Koven C, Krab EJ, Kuhry P, Monteux S, Richter A, Shahzad T, Weedon J, Dorrepaal E
    2020 - Nature Geoscience, 13: 560-565


    As global temperatures continue to rise, a key uncertainty of climate projections is the microbial decomposition of vast organic carbon stocks in thawing permafrost soils. Decomposition rates can accelerate up to fourfold in the presence of plant roots, and this mechanism—termed the rhizosphere priming effect—may be especially relevant to thawing permafrost soils as rising temperatures also stimulate plant productivity in the Arctic. However, priming is currently not explicitly included in any model projections of future carbon losses from the permafrost area. Here, we combine high-resolution spatial and depth-resolved datasets of key plant and permafrost properties with empirical relationships of priming effects from living plants on microbial respiration. We show that rhizosphere priming amplifies overall soil respiration in permafrost-affected ecosystems by ~12%, which translates to a priming-induced absolute loss of ~40 Pg soil carbon from the northern permafrost area by 2100. Our findings highlight the need to include fine-scale ecological interactions in order to accurately predict large-scale greenhouse gas emissions, and suggest even tighter restrictions on the estimated 200 Pg anthropogenic carbon emission budget to keep global warming below 1.5 °C.

  • Microbial growth and carbon use efficiency show seasonal responses in a multifactorial climate change experiment

    Simon E, Canarini A, Martin V, Séneca J, Böckle T, Reinthaler D, Pötsch E M, Piepho H-P, Bahn M, Wanek W, Richter A
    2020 - Communications Biology, 3: article 584


    Microbial growth and carbon use efficiency (CUE) are central to the global carbon cycle, as microbial remains form soil organic matter. We investigated how future global changes may affect soil microbial growth, respiration, and CUE. We aimed to elucidate the soil microbial response to multiple climate change drivers across the growing season and whether effects of multiple global change drivers on soil microbial physiology are additive or interactive. We measured soil microbial growth, CUE, and respiration at three time points in a field experiment combining three levels of temperature and atmospheric CO2, and a summer drought. Here we show that climate change-driven effects on soil microbial physiology are interactive and season-specific, while the coupled response of growth and respiration lead to stable microbial CUE (average CUE = 0.39). These results suggest that future research should focus on microbial growth across different seasons to understand and predict effects of global changes on soil carbon dynamics.

  • Composition and activity of nitrifier communities in soil are unresponsive to elevated temperature and CO2, but strongly affected by drought

    Séneca J, Pjevac P, Canarini A, Herbold CW, Zioutis C, Dietrich M, Simon E, Prommer J, Bahn M, Pötsch EM, Wagner M, Wanek W, Richter A
    2020 - The ISME Journal, 14: 3038-3053


    Nitrification is a fundamental process in terrestrial nitrogen cycling. However, detailed information on how climate change affects the structure of nitrifier communities is lacking, specifically from experiments in which multiple climate change factors are manipulated simultaneously. Consequently, our ability to predict how soil nitrogen (N) cycling will change in a future climate is limited. We conducted a field experiment in a managed grassland and simultaneously tested the effects of elevated atmospheric CO2, temperature, and drought on the abundance of active ammonia-oxidizing bacteria (AOB) and archaea (AOA), comammox (CMX) Nitrospira, and nitrite-oxidizing bacteria (NOB), and on gross mineralization and nitrification rates. We found that N transformation processes, as well as gene and transcript abundances, and nitrifier community composition were remarkably resistant to individual and interactive effects of elevated CO2 and temperature. During drought however, process rates were increased or at least maintained. At the same time, the abundance of active AOB increased probably due to higher NH4+ availability. Both, AOA and comammox Nitrospira decreased in response to drought and the active community composition of AOA and NOB was also significantly affected. In summary, our findings suggest that warming and elevated CO2 have only minor effects on nitrifier communities and soil biogeochemical variables in managed grasslands, whereas drought favors AOB and increases nitrification rates. This highlights the overriding importance of drought as a global change driver impacting on soil microbial community structure and its consequences for N cycling.

  • Variation in rhizosphere priming and microbial growth and carbon use efficiency caused by wheat genotypes and temperatures

    Yin L, Corneo PE, Richter A, Wang P, Cheng W, Dijkstra FA
    2019 - Soil Biology and Biochemistry, 134: 54-61


    Living roots can influence microbial decomposition of soil organic matter, which has been referred to as the rhizosphere priming effect (RPE). Both microbial carbon efficiency (CUE) and microbial growth and turnover rates are associated with microbial decomposition and respiration of soil-derived C, but their linkage to the RPE remains poorly understood. Here we used a natural 13C tracer method to determine the RPE in soils planted with two wheat genotypes (249 or IAW2013) grown at high (30/24 °C during day/night) and low temperature (25/17 °C during day/night). We also determined microbial CUE, growth and biomassturnover rate using a substrate-independent H218O labeling method. The RPE varied from −2 to +455%, with significant effects of genotype, sampling date and their interaction with temperature. Compared to the unplanted control, microbial biomass C and growth/turnover rate were both enhanced in planted pots, with an average increase of 17% and 70%, respectively. Microbial CUE was lowest in pots planted with IAW2013 at low temperature, but there were no significant main effects of planting and temperature. Microbial biomass growth/turnover rate together with CUE accounted for 83% of the variation in soil-derived CO2, with a relatively larger contribution of microbial biomass growth/turnover rate (52%) than CUE (31%). Furthermore, using linear regression, we demonstrated that the RPE was significantly positively related to microbial biomass growth/turnover rate. No net soil organic C (SOC) loss or gain was detected, indicating that any increase in SOC due to increased microbial growth/turnover was counteracted by C loss caused by a higher RPE during the relatively short time of planting. These findings suggest that microbial biomass turnover associated with growth could control the loss of SOC with planting. We highlight the importance of plant-induced changes in microbial CUE and biomass growth/turnover for long-term soil C dynamics.

  • Characterization of a thaumarchaeal symbiont that drives incomplete nitrification in the tropical sponge Ianthella basta

    Moeller FU, Webster NS, Herbold CW, Behmann F, Domman D, Albertsen M, Mooshammer M, Market S, Turaev D, Becher D, Rattei T, Schweder T, Richter A, Watzka M, Nielsen PH, Wagner M
    2019 - Environmental Microbiology, 21: 3831-3854


    Marine sponges represent one of the few eukaryotic
    groups that frequently harbour symbiotic members of
    the Thaumarchaeota, which are important chemoautotrophic
    ammonia-oxidizers in many environments.
    However, in most studies, direct demonstration of
    ammonia-oxidation by these archaea within sponges
    is lacking, and little is known about sponge-specific
    adaptations of ammonia-oxidizing archaea (AOA). Here,
    we characterized the thaumarchaeal symbiont of the
    marine sponge Ianthella basta using metaproteogenomics,
    fluorescence in situ hybridization, qPCR
    and isotope-based functional assays. ‘Candidatus
    Nitrosospongia ianthellae’ is only distantly related
    to cultured AOA. It is an abundant symbiont that is
    solely responsible for nitrite formation from ammonia
    in I. basta that surprisingly does not harbour nitriteoxidizing
    microbes. Furthermore, this AOA is equipped
    with an expanded set of extracellular subtilisin-like proteases,
    a metalloprotease unique among archaea, as
    well as a putative branched-chain amino acid ABC
    transporter. This repertoire is strongly indicative of a
    mixotrophic lifestyle and is (with slight variations) also
    found in other sponge-associated, but not in free-living
    AOA. We predict that this feature as well as an expanded
    and unique set of secreted serpins (protease inhibitors),
    a unique array of eukaryotic-like proteins, and a DNAphosporothioation
    system, represent important adaptations
    of AOA to life within these ancient filter-feeding

  • Microbial carbon and nitrogen cycling responses to drought and temperature in differently managed mountain grasslands

    Fuchslueger L, Wild B, Mooshammer M, Takriti M, Kienzl S, Knoltsch A, Hofhansl F, Bahn M, Richter A
    2019 - Soil Biology and Biochemistry, 135: 144-153


    Grassland management can modify soil microbial carbon (C) and nitrogen (N) cycling, affecting the resistance to extreme weather events, which are predicted to increase in frequency and magnitude in the near future. However, effects of grassland management on microbial C and N cycling and their responses to extreme weather events, such as droughts and heatwaves, have rarely been tested in a combined approach. We therefore investigated whether grassland management affects microbial C and N cycling responses to drought and temperature manipulation. We collected soils from in situdrought experiments conducted in an extensively managed and an abandoned mountain grassland and incubated them at two temperature levels. We measured microbial respiration and substrate incorporation, as well as gross rates of organic and inorganic N cycling to estimate microbial C and N use efficiencies (CUE and NUE). The managed grassland was characterized by lower microbial biomass, lower fungi to bacteria ratio, and higher microbial CUE, but only slightly different microbial NUE. At both sites drought induced a shift in microbial community composition driven by an increase in Gram-positive bacterial abundance. Drought significantly reduced C substrate respiration and incorporation by microbes at both sites, while microbial CUE remained constant. In contrast, drought increased gross rates of N mineralization at both sites, whereas gross amino acid uptake rates only marginally changed. We observed a significant direct, as well as interactive effect between land management and drought on microbial NUE. Increased temperatures significantly stimulated microbial respiration and reduced microbial CUE independent of drought or land management. Although microbial N processing rates showed no clear response, microbial NUE significantly decreased at higher temperatures. In summary in our study, microbial CUE, in particular respiration, is more responsive to temperature changes. Although N processing rates were stronger responding to drought than to temperature microbial NUE was affected by both drought and temperature increase. We conclude that direct effects of drought and heatwaves can induce different responses in soil microbial C and N cycling similarly in the studied land management systems.

  • Coupled carbon and nitrogen losses in response to seven years of chronic warming in subarctic soils

    Marañon-Jimenez S, Peñuelas J, Richter A, Sigurdsson BD, Fuchslueger L, Leblans NIW, Janssens IA
    2019 - Soil Biology and Biochemistry, 134: 152-161


    Increasing temperatures may alter the stoichiometric demands of soil microbes and impair their capacity to stabilize carbon (C) and retain nitrogen (N), with critical consequences for the soil C and N storage at high latitude soils. Geothermally active areas in Iceland provided wide, continuous and stable gradients of soil temperatures to test this hypothesis. In order to characterize the stoichiometric demands of microbes from these subarctic soils, we incubated soils from ambient temperatures after the factorial addition of C, N and P substrates separately and in combination. In a second experiment, soils that had been exposed to different in situ warming intensities (+0, +0.5, +1.8, +3.4, +8.7, +15.9 °C above ambient) for seven years were incubated after the combined addition of C, N and P to evaluate the capacity of soil microbes to store and immobilize C and N at the different warming scenarios. The seven years of chronic soil warming triggered large and proportional soil C and N losses (4.1 ± 0.5% °C−1 of the stocks in unwarmed soils) from the upper 10 cm of soil, with a predominant depletion of the physically accessible organic substrates that were weakly sorbed in soil minerals up to 8.7 °C warming. Soil microbes met the increasing respiratory demands under conditions of low C accessibility at the expenses of a reduction of the standing biomass in warmer soils. This together with the strict microbial C:N stoichiometric demands also constrained their capacity of N retention, and increased the vulnerability of soil to N losses. Our findings suggest a strong control of microbial physiology and C:N stoichiometric needs on the retention of soil N and on the resilience of soil C stocks from high-latitudes to warming, particularly during periods of vegetation dormancy and low C inputs.

  • Growth explains microbial carbon use efficiency across soils differing in land use and geology

    Zheng Q, Hu Y, zhang S, Noll L, Boeckle T, Richter A, Wanek W
    2019 - Soil Biology and Biochemistry, 128: 45-55


    The ratio of carbon (C) that is invested into microbial growth to organic C taken up is known as microbial carbon use efficiency (CUE), which is influenced by environmental factors such as soil temperature and soil moisture. How microbes will physiologically react to short-term environmental changes is not well understood, primarily due to methodological restrictions. Here we report on two independent laboratory experiments to explore short-term temperature and soil moisture effects on soil microbial physiology(i.e. respiration, growth, CUE, and microbial biomass turnover): (i) a temperature experiment with 1-day pre-incubation at 5, 15 and 25 °C at 60% water holding capacity (WHC), and (ii) a soil moisture/oxygen (O2) experiment with 7-day pre-incubation at 20 °C at 30%, 60% WHC (both at 21% O2) and 90% WHC at 1% O2. Experiments were conducted with soils from arable, pasture and forest sites derived from both silicate and limestone bedrocks. We found that microbial CUE responded heterogeneously though overall positively to short-term temperature changes, and decreased significantly under high moisture level (90% WHC)/suboxic conditions due to strong decreases in microbial growth. Microbial biomass turnover time decreased dramatically with increasing temperature, and increased significantly at high moisture level (90% WHC)/suboxic conditions. Our findings reveal that the responses of microbial CUE and microbial biomass turnover to short-term temperature and moisture/O2 changes depended mainly on microbial growth responses and less on respiration responses to the environmental cues, which were consistent across soils differing in land use and geology.

  • Life at 0 °C: the biology of the alpine snowbed plant Soldanella pusilla

    Körner C, Riedl S, Keplinger T, Richter A, Wiesenbauer J, Schweingruber F, Hiltbrunner E
    2019 - Alpine Botany, 129: 63-80


    All plant species reach a low temperature range limit when either low temperature extremes exceed their freezing tolerance
    or when their metabolism becomes too restricted. In this study, we explore the ultimate thermal limit of plant tissue formation
    exemplified by a plant species that seemingly grows through snow. By a combination of studies in alpine snowbeds and
    under controlled environmental conditions, we demonstrate and quantify that the clonal herb Soldanella pusilla (Primulaceae)
    does indeed grow its entire flowering shoot at 0 °C. We show that plants resume growth under 2–3 m of snow in mid-winter,
    following an internal clock, with the remaining period under snow until snow melt (mostly in July) sufficient to produce a
    flowering shoot that is ready for pollination. When snow pack gets thin, the flowering shoot intercepts and re-radiates longwave
    solar radiation, so that snow and ice gently melt around the fragile shoot and the flowers emerge without any mechanical
    interaction. We evidence bud preformation in the previous season and enormous non-structural carbohydrate reserves
    in tissues (mainly below ground) in the form of soluble sugars (largely stachyose) that would support basic metabolism for
    more than 2 entire years under snow. However, cell-wall formation at 0 °C appears to lack unknown strengthening factors,
    including lignification (assessed by confocal Raman spectroscopy imaging) that require between a few hours or a day of
    warmth after snow melt to complete tissue strengthening. Complemented with a suite of anatomical data, the work opens a
    window towards understanding low temperature limits of plant growth in general, with potential relevance for winter crops
    and trees at the natural climatic treeline.

  • Soil multifunctionality is affected by the soil environment and by microbial community composition and diversity

    Zheng Q, Hu Y, zhang S, Noll L, Böckle T, Dietrich M, Herbold CW, Eichhorst SA, Woebken D, Richter A, Wanek W
    2019 - Soil Biology and Biochemistry, 136: Article 107521


    Microorganisms are critical in mediating carbon (C) and nitrogen (N) cycling processes in soils. Yet, it has long been debated whether the processes underlying biogeochemical cycles are affected by the composition and diversity of the soil microbial community or not. The composition and diversity of soil microbial communities can be influenced by various environmental factors, which in turn are known to impact biogeochemical processes. The objectives of this study were to test effects of multiple edaphic drivers individually and represented as the multivariate soil environment interacting with microbial community composition and diversity, and concomitantly on multiple soil functions (i.e. soil enzyme activities, soil C and N processes). We employed high-throughput sequencing (Illumina MiSeq) to analyze bacterial/archaeal and fungal community composition by targeting the 16S rRNA gene and the ITS1 region of soils collected from three land uses (cropland, grassland and forest) deriving from two bedrock forms (silicate and limestone). Based on this data set we explored single and combined effects of edaphic variables on soil microbial community structure and diversity, as well as on soil enzyme activities and several soil C and N processes. We found that both bacterial/archaeal and fungal communities were shaped by the same edaphic factors, with most single edaphic variables and the combined soil environment representation exerting stronger effects on bacterial/archaeal communities than on fungal communities, as demonstrated by (partial) Mantel tests. We also found similar edaphic controls on the bacterial/archaeal/fungal richness and diversity. Soil C processes were only directly affected by the soil environment but not affected by microbial community composition. In contrast, soil N processes were significantly related to bacterial/archaeal community composition and bacterial/archaeal/fungal richness/diversity but not directly affected by the soil environment. This indicates direct control of the soil environment on soil C processes and indirect control of the soil environment on soil N processes by structuring the microbial communities. The study further highlights the importance of edaphic drivers and microbial communities (i.e. composition and diversity) on important soil C and N processes.

  • Plant roots increase both decomposition and stable organic matter formation in boreal forest soil

    Adamczyk B, Sietiö OM, Straková P, Prommer J, Wild B, Hagner M, Pihlatie M, Fritze H, Richter A, Heinonsalo J
    2019 - Nature Communications, 10: Article 3982
  • Nutrient scarcity strengthens soil fauna control over leaf litter decomposition in tropical rainforests

    Peguero G, Sardans J, Asensio D, Fernández-Martínez M, Gargallo-Garriga A, Grau O, Llusià J, Margalef O, Márquez L, Ogaya R, Urbina I, Courtois EA, Stah C, Van Langenhove L, Verryckt LT, Richter A, anssens IA, Peñuelas J
    2019 - Proceedings of the Royal Society B: Biological Sciences, 286: Article 20191300


    Soil fauna is a key control of the decomposition rate of leaf litter, yet its
    interactions with litter quality and the soil environment remain elusive. We
    conducted a litter decomposition experiment across different topographic
    levels within the landscape replicated in two rainforest sites providing natural
    gradients in soil fertility to test the hypothesis that low nutrient availability in
    litter and soil increases the strength of fauna control over litter decomposition.
    We crossed these data with a large dataset of 44 variables characterizing
    the biotic and abiotic microenvironment of each sampling point and found
    that microbe-driven carbon (C) and nitrogen (N) losses from leaf litter were
    10.1 and 17.9% lower, respectively, in the nutrient-poorest site, but this
    among-site difference was equalized when meso- and macrofauna had
    access to the litterbags. Further, on average, soil fauna enhanced the rate of
    litter decomposition by 22.6%, and this contribution consistently increased
    as nutrient availability in the microenvironment declined. Our results indicate
    that nutrient scarcity increases the importance of soil fauna on C and N
    cycling in tropical rainforests. Further, soil fauna is able to equalize differences
    in microbial decomposition potential, thus buffering to a remarkable extent
    nutrient shortages at an ecosystem level.

  • Carbon isotopic tracing of sugars throughout whole-trees exposed to climate warming

    Furze M., Drake JE, Wiesenbauer J, Richter A, Pendall E
    2019 - Plant Cell and Environment, 42: 3253-3263


    Trees allocate C from sources to sinks by way of a series of processes involving carbohydrate transport and utilization. Yet these dynamics are not well characterized in trees, and it is unclear how these dynamics will respond to a warmer world. Here, we conducted a warming and pulse‐chase experiment on Eucalyptus parramattensis growing in a whole‐tree chamber system to test whether warming impacts carbon allocation by increasing the speed of carbohydrate dynamics. We pulse‐labelled large (6‐m tall) trees with 13C‐CO2 to follow recently fixed C through different organs by using compound‐specific isotope analysis of sugars. We then compared concentrations and mean residence times of individual sugars between ambient and warmed (+3°C) treatments. Trees dynamically allocated 13C‐labelled sugars throughout the aboveground‐belowground continuum. We did not, however, find a significant treatment effect on C dynamics, as sugar concentrations and mean residence times were not altered by warming. From the canopy to the root system, 13C enrichment of sugars decreased, and mean residence times increased, reflecting dilution and mixing of recent photoassimilates with older reserves along the transport pathway. Our results suggest that a locally endemic eucalypt was seemingly able to adjust its physiology to warming representative of future temperature predictions for Australia.

  • Low yield and abiotic origin of NO formed by the complete nitrifier Nitrospira inopinata

    Kits KD, Jung MY, Vierheilig J, Pjevac P, Sedlacek CJ, Liu S, Herbold C, Stein LY, Richter A, Wissel H, Brüggemann N, Wagner M, Daims H
    2019 - Nature Communications, 10: Article 1836


    Nitrous oxide (NO) and nitric oxide (NO) are atmospheric trace gases that contribute to climate change and affect stratospheric and ground-level ozone concentrations. Ammonia oxidizing bacteria (AOB) and archaea (AOA) are key players in the nitrogen cycle and major producers of NO and NO globally. However, nothing is known about NO and NO production by the recently discovered and widely distributed complete ammonia oxidizers (comammox). Here, we show that the comammox bacterium Nitrospira inopinata is sensitive to inhibition by an NO scavenger, cannot denitrify to NO, and emits NO at levels that are comparable to AOA but much lower than AOB. Furthermore, we demonstrate that NO formed by N. inopinata formed under varying oxygen regimes originates from abiotic conversion of hydroxylamine. Our findings indicate that comammox microbes may produce less NO during nitrification than AOB.

  • Widespread soil bacterium that oxidizes atmospheric methane

    Tveit AT, Hestnes AG, Robinson SL, Schintlmeister A, Dedysh SN, Jehmlich N, von Bergen M, Herbold CW, Wagner M, Richter A, Svenning MM
    2019 - Proceedings of the National Academy of Sciences of the United States of America (PNAS), 17: 8515-8524


    The global atmospheric level of methane (CH), the second most important greenhouse gas, is currently increasing by ∼10 million tons per year. Microbial oxidation in unsaturated soils is the only known biological process that removes CH from the atmosphere, but so far, bacteria that can grow on atmospheric CH have eluded all cultivation efforts. In this study, we have isolated a pure culture of a bacterium, strain MG08 that grows on air at atmospheric concentrations of CH [1.86 parts per million volume (p.p.m.v.)]. This organism, named , is globally distributed in soils and closely related to uncultured members of the upland soil cluster α. CH oxidation experiments and C-single cell isotope analyses demonstrated that it oxidizes atmospheric CH aerobically and assimilates carbon from both CH and CO Its estimated specific affinity for CH (a) is the highest for any cultivated methanotroph. However, growth on ambient air was also confirmed for and , close relatives with a lower specific affinity for CH, suggesting that the ability to utilize atmospheric CH for growth is more widespread than previously believed. The closed genome of MG08 encodes a single particulate methane monooxygenase, the serine cycle for assimilation of carbon from CH and CO, and CO fixation via the recently postulated reductive glycine pathway. It also fixes dinitrogen and expresses the genes for a high-affinity hydrogenase and carbon monoxide dehydrogenase, suggesting that atmospheric CH oxidizers harvest additional energy from oxidation of the atmospheric trace gases carbon monoxide (0.2 p.p.m.v.) and hydrogen (0.5 p.p.m.v.).

  • Root exudation of primary metabolites: mechanisms and their roles in plant responses to environmental stimuli

    2019 - Frontiers in Plant Science, 10: Article 157


    Root exudation is an important process determining plant interactions with the soil environment. Many studies have linked this process to soil nutrient mobilization. Yet, it remains unresolved how exudation is controlled and how exactly and under what circumstances plants benefit from exudation. The majority of root exudates include primary metabolites (sugars, amino acids and organic acids) believed to be passively lost from the root and used by rhizosphere-dwelling microbes. In this review, we synthetize recent advances in ecology and plant biology to explain and propose mechanisms by which root exudation of primary metabolites is controlled, and what role their exudation plays in plant nutrient acquisition strategies. Specifically, we propose a novel conceptual framework for root exudates. This framework is built upon two main concepts: (i) root exudation of primary metabolites is driven by diffusion, with plants and microbes both modulating concentration gradients and therefore diffusion rates to soil depending on their nutritional status; (ii) exuded metabolite concentrations can be sensed at the root tip and signals are translated to modify root architecture. The flux of primary metabolites through root exudation is mostly located at the root tip, where the lack of cell differentiation favors diffusion of metabolites to the soil. We show examples of how the root tip senses concentration changes of exuded metabolites and translate that into signals to modify root growth. Plants can modify the concentration of metabolites either by controlling source/sink processes or by expressing and regulating efflux carriers, therefore challenging the idea of root exudation as a purely unregulated passive process. Through root exudate flux, plants can locally enhance concentrations of many common metabolites which can serve as sensors and integrators of the plant nutritional status and of the nutrient availability in the surrounding environment. Plant-associated micro-organisms also constitute a strong sink for plant carbon thereby increasing concentration gradients of metabolites and affecting root exudation. Understanding the mechanisms of, and the effects that, environmental stimuli have on the magnitude and type of root exudation will ultimately improve our knowledge of processes determining soil CO2 emissions, ecosystem functioning and how to improve the sustainability of agricultural production.

  • Rapid transfer of plant photosynthates to soil bacteria via ectomycorrhizal hyphae and its interaction with nitrogen availability

    Gorka S, Dietrich M, Mayerhofer W, Gabriel R, Wiesenbauer J, Martin V, Zheng Q, Imai B, Prommer J, Weidinger M, Schweiger P, Eichorst SA, Wagner M, Richter A, Schintlmeister A, Woebken D, Kaiser C
    2019 - Frontiers Microbioly, 10: Article 168


    Plant roots release recent photosynthates into the rhizosphere, accelerating decomposition of organic matter by saprotrophic soil microbes (’rhizosphere priming effect’) which consequently increases nutrient availability for plants. However, about 90% of all higher plant species are mycorrhizal, transferring a significant fraction of their photosynthates directly to their fungal partners. Whether mycorrhizal fungi pass on plant-derived carbon (C) to bacteria in root-distant soil areas, i.e. incite a ‘hyphosphere priming effect’, is not known. Experimental evidence for C transfer from mycorrhizal hyphae to soil bacteria is limited, especially for ectomycorrhizal systems. As ectomycorrhizal fungi possess enzymatic capabilities to degrade organic matter themselves, it remains unclear whether they cooperate with soil bacteria by providing photosynthates, or compete for available nutrients.

    To investigate a possible C transfer from ectomycorrhizal hyphae to soil bacteria, and its response to changing nutrient availability, we planted young beech trees (Fagus sylvatica) into ‘split-root’ boxes, dividing their root systems into two disconnected soil compartments. Each of these compartments was separated from a litter compartment by a mesh penetrable for fungal hyphae, but not for roots. Plants were exposed to a 13C-CO2–labeled atmosphere, while 15N-labeled ammonium and amino acids were added to one side of the split-root system.

    We found a rapid transfer of recent photosynthates via ectomycorrhizal hyphae to bacteria in root-distant soil areas. Fungal and bacterial phospholipid fatty acid (PLFA) biomarkers were significantly enriched in hyphae-exclusive compartments 24 h after 13C-CO2–labeling. Isotope imaging with nanometer-scale secondary ion mass spectrometry (NanoSIMS) allowed for the first time in situ visualization of plant-derived C and N taken up by extraradical fungal hyphae, and in microbial cells thriving on hyphal surfaces. When N was added to the litter compartments, bacterial biomass and the amount of incorporated 13C strongly declined. Interestingly, this effect was also observed in adjacent soil compartments where added N was only available for bacteria through hyphal transport, indicating that ectomycorrhizal fungi were acting on soil bacteria. Together, our results demonstrate that (i) ectomycorrhizal hyphae rapidly transfer plant-derived C to bacterial communities in root-distant areas, and (ii) this transfer promptly responds to changing soil nutrient conditions.

  • Cyanate and urea are substrates for nitrification by Thaumarchaeota in the marine environment

    Kitzinger K, Padilla CC, Marchant HK, Hach PF, Herbold CW, Kidane AT, Könneke M, Littmann S, Mooshammer M, Niggemann J, Petriv S, Richter A, Stewart FJ, Wagner M, Kuypers MMM, Bristow LA
    2019 - Nature Microbiology, 4: 234-243


    Ammonia-oxidizing archaea of the phylum Thaumarchaeota are among the most abundant marine microorganisms1. These organisms thrive in the oceans despite ammonium being present at low nanomolar concentrations2,3. Some Thaumarchaeota isolates have been shown to utilize urea and cyanate as energy and N sources through intracellular conversion to ammonium4,5,6. Yet, it is unclear whether patterns observed in culture extend to marine Thaumarchaeota, and whether Thaumarchaeota in the ocean directly utilize urea and cyanate or rely on co-occurring microorganisms to break these substrates down to ammonium. Urea utilization has been reported for marine ammonia-oxidizing communities7,8,9,10, but no evidence of cyanate utilization exists for marine ammonia oxidizers. Here, we demonstrate that in the Gulf of Mexico, Thaumarchaeota use urea and cyanate both directly and indirectly as energy and N sources. We observed substantial and linear rates of nitrite production from urea and cyanate additions, which often persisted even when ammonium was added to micromolar concentrations. Furthermore, single-cell analysis revealed that the Thaumarchaeota incorporated ammonium-, urea- and cyanate-derived N at significantly higher rates than most other microorganisms. Yet, no cyanases were detected in thaumarchaeal genomic data from the Gulf of Mexico. Therefore, we tested cyanate utilization in Nitrosopumilus maritimus, which also lacks a canonical cyanase, and showed that cyanate was oxidized to nitrite. Our findings demonstrate that marine Thaumarchaeota can use urea and cyanate as both an energy and N source. On the basis of these results, we hypothesize that urea and cyanate are substrates for ammonia-oxidizing Thaumarchaeota throughout the ocean.

  • Amino acid production exceeds plant nitrogen demand in Siberian tundra

    Wild B, Alves RJE, Barta J, Capek P, Gentsch N, Guggenberger G, Hugelius G, Knoltsch A, Kuhry P, Lashchinskiy N, Mikutta R, Palmtag J, Prommer J, Schnecker J, Shibistova O, Takriti M, Urich T, Richter A
    2018 - Environmental Research Letters, 13: 11


    Arctic plant productivity is often limited by low soil N availability. This has been attributed to slow breakdown of N-containing polymers in litter and soil organic matter (SOM) into smaller, available units, and to shallow plant rooting constrained by permafrost and high soil moisture. Using 15N pool dilution assays, we here quantified gross amino acid and ammonium production rates in 97 active layer samples from four sites across the Siberian Arctic. We found that amino acid production in organic layers alone exceeded literature-based estimates of maximum plant N uptake 17-fold and therefore reject the hypothesis that arctic plant N limitation results from slow SOM breakdown. High microbial N use efficiency in organic layers rather suggests strong competition of microorganisms and plants in the dominant rooting zone. Deeper horizons showed lower amino acid production rates per volume, but also lower microbial N use efficiency. Permafrost thaw together with soil drainage might facilitate deeper plant rooting and uptake of previously inaccessible subsoil N, and thereby promote plant productivity in arctic ecosystems. We conclude that changes in microbial decomposer activity, microbial N utilization and plant root density with soil depth interactively control N availability for plants in the Arctic.

  • Full 15N tracer accounting to revisit major assumptions of 15N isotope pool dilution approaches for gross nitrogen mineralization

    Braun J, Mooshammer M, Wanek W, Prommer J, Walker TWN, Rütting T, Richter A
    2018 - Soil Biology and Biochemistry, 117: 16-26
  • Geothermally warmed soils reveal persistent increases in the respiratory costs of soil microbes contributing to substantial C losses

    Marañon-Jimenez S, Soong JL, Leblans NI, Sigurdsson B, Peñuelas J, Richter A, Asensio D, Fransen E, Janssens IA
    2018 - Biogeochemistry, 138: 245-260


    Increasing temperatures can accelerate soil organic matter decomposition and release large amounts of CO2 to the atmosphere, potentially inducing positive warming feedbacks. Alterations to the temperature sensitivity and physiological functioning of soil microorganisms may play a key role in these carbon (C) losses. Geothermally active areas in Iceland provide stable and continuous soil temperature gradients to test this hypothesis, encompassing the full range of warming scenarios projected by the Intergovernmental Panel on Climate Change for the northern region. We took soils from these geothermal sites 7 years after the onset of warming and incubated them at varying temperatures and substrate availability conditions to detect persistent alterations of microbial physiology to long-term warming. Seven years of continuous warming ranging from 1.8 to 15.9 °C triggered a 8.6–58.0% decrease on the C concentrations in the topsoil (0–10 cm) of these sub-arctic silt-loam Andosols. The sensitivity of microbial respiration to temperature (Q10) was not altered. However, soil microbes showed a persistent increase in their microbial metabolic quotients (microbial respiration per unit of microbial biomass) and a subsequent diminished C retention in biomass. After an initial depletion of labile soil C upon soil warming, increasing energy costs of metabolic maintenance and resource acquisition led to a weaker capacity of C stabilization in the microbial biomass of warmer soils. This mechanism contributes to our understanding of the acclimated response of soil respiration to in situ soil warming at the ecosystem level, despite a lack of acclimation at the physiological level. Persistent increases in the respiratory costs of soil microbes in response to warming constitute a fundamental process that should be incorporated into climate change-C cycling models.

  • Spatial variation of soil CO2, CH4 and N2O fluxes across topographical positions in the tropical forests of the Guiana Shield

    Courtois EA, Stahl C, Van den Berge J, Bréchet L, Van Langenhove L, Richter A, Urbina I, Soong JL, Peñuelas J, Janssens IA
    2018 - Ecosystems, 7: 1445-1458


    The spatial variation of soil greenhouse gas fluxes (GHG; carbon dioxide—CO2, methane—CH4and nitrous oxide—N2O) remains poorly understood in highly complex ecosystems such as tropical forests. We used 240 individual flux measurements of these three GHGs from different soil types, at three topographical positions and in two extreme hydric conditions in the tropical forests of the Guiana Shield (French Guiana, South America) to (1) test the effect of topographical positions on GHG fluxes and (2) identify the soil characteristics driving flux variation in these nutrient-poor tropical soils. Surprisingly, none of the three GHG flux rates differed with topographical position. CO2 effluxes covaried with soil pH, soil water content (SWC), available nitrogen and total phosphorus. The CH4 fluxes were best explained by variation in SWC, with soils acting as a sink under drier conditions and as a source under wetter conditions. Unexpectedly, our study areas were generally sinks for N2O and N2O fluxes were partly explained by total phosphorus and available nitrogen concentrations. This first study describing the spatial variation of soil fluxes of the three main GHGs measured simultaneously in forests of the Guiana Shield lays the foundation for specific studies of the processes underlying the observed patterns.

  • Significance of dark CO2 fixation in arctic soils

    Santruckova H, Kotas P, Barta J, Urich T, Capek P, Palmtag J, Alves RJE, Biasi C, Diakova K, Gentsch N, Gittel A, Guggenberger G, Hugelius G, Lashchinsky N, Martikainen PJ, Mikutta R, Schleper C, Schnecker J, Schwab C, Shibistova O, Wild B, Richter A
    2018 - Soil Biology and Biochemistry, 119: 11-21


    The occurrence of dark fixation of CO2 by heterotrophic microorganisms in soil is generally accepted, but its importance for microbial metabolism and soil organic carbon (C) sequestration is unknown, especially under Climiting conditions. To fill this knowledge gap, we measured dark 13CO2 incorporation into soil organic matter and conducted a 13C-labelling experiment to follow the 13C incorporation into phospholipid fatty acids as microbial biomass markers across soil profiles of four tundra ecosystems in the northern circumpolar region, where net primary productivity and thus soil C inputs are low. We further determined the abundance of various carboxylase genes and identified their microbial origin with metagenomics. The microbial capacity for heterotrophic CO2 fixation was determined by measuring the abundance of carboxylase genes and the incorporation of 13C into soil C following the augmentation of bioavailable C sources. We demonstrate that dark CO2 fixation occurred ubiquitously in arctic tundra soils, with increasing importance in deeper soil horizons, presumably due to increasing C limitation with soil depth. Dark CO2 fixation accounted on average for 0.4, 1.0, 1.1, and 16% of net respiration in the organic, cryoturbated organic, mineral and permafrost horizons, respectively. Genes encoding anaplerotic enzymes of heterotrophic microorganisms comprised the majority of identified carboxylase genes. The genetic potential for dark CO2 fixation was spread over a broad taxonomic range. The results suggest important regulatory function of CO2 fixation in C limited conditions. The measurements were corroborated by modeling the long-term impact of dark CO2 fixation on soil organic matter. Our results suggest that increasing relative CO2 fixation rates in deeper soil horizons play an important role for soil internal C cycling and can, at least in part, explain the isotopic enrichment with soil depth.

  • Resistance of soil protein depolymerization rates to eight years of elevated CO2, warming, and summer drought in a temperate heathland

    Wild B, Ambus P, Reinsch S, Richter A
    2018 - Biogeochemistry, 140: 255-267


    Soil N availability for plants and microorganisms depends on the breakdown of soil polymers such as proteins into smaller, assimilable units by microbial extracellular enzymes. Changing climatic conditions are expected to alter protein depolymerization rates over the next decades, and thereby affect the potential for plant productivity. We here tested the effect of increased CO2 concentration, temperature, and drought frequency on gross rates of protein depolymerization, N mineralization, microbial amino acid and ammonium uptake using 15N pool dilution assays. Soils were sampled in fall 2013 from the multifactorial climate change experiment CLIMAITE that simulates increased CO2 concentration, temperature, and drought frequency in a fully factorial design in a temperate heathland. Eight years after treatment initiation, we found no significant effect of any climate manipulation treatment, alone or in combination, on protein depolymerization rates. Nitrogen mineralization, amino acid and ammonium uptake showed no significant individual treatment effects, but significant interactive effects of warming and drought. Combined effects of all three treatments were not significant for any of the measured parameters. Our findings therefore do not suggest an accelerated release of amino acids from soil proteins in a future climate at this site that could sustain higher plant productivity.

  • Soil organic matter quality exerts a stronger control than stoichiometry on microbial substrate use efficiency along a latitudinal transect

    Takriti M, Wild B, Schnecker J, Mooshammera M, Knoltsch A, Lashchinskiy N, Alves RJE, Gentsch N, Gittel A, Mikutta R, Wanek W, Richter A
    2018 - Soil Biology and Biochemistry, 121: 212-220


    A substantial portion of soil organic matter (SOM) is of microbial origin. The efficiency with which soil microorganisms can convert their substrate carbon (C) into biomass, compared to how much is lost as respiration, thus co-determines the carbon storage potential of soils. Despite increasing insight into soil microbial C cycling, empirical measurements of microbial C processing across biomes and across soil horizons remain sparse. The theory of ecological stoichiometry predicts that microbial carbon use efficiency (CUE), i.e. growth over uptake of organic C, strongly depends on the relative availability of C and nutrients, particularly N, as microorganisms will either respire excess C or conserve C while mineralising excess nutrients. Microbial CUE is thus expected to increase from high to low latitudes and from topsoil to subsoil as the soil C:N and the stoichiometric imbalance between SOM and the microbial biomass decrease. To test these hypotheses, we collected soil samples from the organic topsoil, mineral topsoil, and mineral subsoil of seven sites along a 1500-km latitudinal transect in Western Siberia. As a proxy for CUE, we measured the microbial substrate use efficiency (SUE) of added substrates by incubating soil samples with a mixture of 13C labelled sugars, amino sugarsamino acids, and organic acids and tracing 13C into microbial biomass and released CO2. In addition to soil and microbial C:N stoichiometry, we also determined the potential extracellular enzyme activities of cellobiohydrolase (CBH) and phenoloxidase (POX) and used the CBH:POX ratio as an indicator of SOM substrate quality. We found an overall decrease of SUE with latitude, corresponding to a decrease in mean annual temperature, in mineral soil horizons. SUE decreased with decreasing stoichiometric imbalance in the organic and mineral topsoil, while a relationship of SUE with soil C:N was only found in the mineral topsoil. However, contrary to our hypothesis, SUE did not increase with soil depth and mineral subsoils displayed lower average SUE than mineral topsoils. Both within individual horizons and across all horizons SUE was strongly correlated with CBH:POX ratio as well as with climate variables. Since enzyme activities likely reflect the chemical properties of SOM, our results indicate that SOM quality exerts a stronger control on SUE than SOM stoichiometry, particularly in subsoils were SOM has been turned over repeatedly and there is little variation in SOM elemental ratios.

  • Fate of carbohydrates and lignin in north-east Siberian permafrost soils

    Dao TT, Gentsch N, Mikutta R, Sauheitl L, Shibistova O, Wild B, Schnecker J, Barta J, Capek P, Gittel A, Lashchinskiy N, Urich T, Santruckova H, Richter A, Guggenberger G
    2018 - Soil Biology and Biochemistry, 116: 311-322


    Permafrost soils preserve huge amounts of organic carbon (OC) prone to decomposition under changing climatic conditions. However, knowledge on the composition of soil organic matter (OM) and its transformation and vulnerability to decomposition in these soils is scarce. We determined neutral sugars and lignin-derived phenols, released by trifluoroacetic acid (TFA) and CuO oxidation, respectively, within plants and soil density fractions from the active layer and the upper permafrost layer at three different tundra types (shrubby grass, shrubby tussock, shrubby lichen) in the Northeast Siberian Arctic. The heavy fraction (HF; > 1.6 g mL−1 ) was characterized by a larger enrichment of microbial sugars (hexoses vs. pentoses) and more pronounced lignin degradation (acids vs. aldehydes) as compared to the light fraction (LF; < 1.6 g mL−1 ), showing the transformation from plant residue-dominated particulate OM to a largely microbial imprint in mineral-associated OM. In contrast to temperate and tropical soils, total neutral sugar contents and galactose plus mannose to arabinose plus xylose ratios (GM/AX) decreased in the HF with soil depth, which may indicate a process of effective recycling of microbial biomass rather than utilizing old plant materials. At the same time, lignin-derived phenols increased and the degree of oxidative decomposition of lignin decreased with soil depth, suggesting a selective preservation of lignin presumably due to anaerobiosis. As large parts of the plant-derived pentoses are incorporated in lignocelluloses and thereby protected against rapid decomposition, this might also explain the relative enrichment of pentoses with soil depth. Hence, our results show a relatively large contribution of plantderived OM, particularly in the buried topsoil and subsoil, which is stabilized by the current soil environmental conditions but may become available to decomposers if permafrost degradation promotes soil drainage and improves the soil oxygen supply.

  • Soil microbial CNP and respiration responses to organic matter and nutrient additions: Evidence from a tropical soil incubation

    Soong J, Marañon-Jimenez S, Cotrufo MF, Boeckx P, Bodé S, Guenet B, Peñuelas J, Richter A, Stahl C, Verbruggen E, Janssens IA
    2018 - Soil Biology and Biochemistry, 122: 141-149


    Soil nutrient availability has a strong influence on the fate of soil carbon (C) during microbial decomposition, contributing to Earth's C balance. While nutrient availability itself can impact microbial physiology and C partitioning between biomass and respiration during soil organic matter decomposition, the availability of labile C inputs may mediate the response of microorganisms to nutrient additions. As soil organic matter is decomposed, microorganisms retain or release C, nitrogen (N) or phosphorus (P) to maintain a stoichiometric balance. Although the concept of a microbial stoichiometric homeostasis has previously been proposed, microbial biomass CNP ratios are not static, and this may have very relevant implications for microbial physiological activities. Here, we tested the hypothesis that N, P and potassium (K) nutrient additions impact C cycling in a tropical soil due to microbial stoichiometric constraints to growth and respiration, and that the availability of energy-rich labile organic matter in the soil (i.e. leaf litter) mediates the response to nutrient addition. We incubated tropical soil from French Guiana with a 13C labeled leaf litter addition and with mineral nutrient additions of +K, +N, +NK, +PK and +NPK for 30 days. We found that litter additions led to a ten-fold increase in microbial respiration and a doubling of microbial biomass C, along with greater microbial N and P content. We found some evidence that P additions increased soil CO2 fluxes. Additionally, we found microbial biomass CP and NP ratios varied more widely than CN in response to nutrient and organic matter additions, with important implications for the role of microorganisms in C cycling. The addition of litter did not prime soil organic matter decomposition, except in combination with +NK fertilization, indicating possible P-mining of soil organic matter in this P-poor tropical soil. Together, these results point toward an ultimate labile organic substrate limitation of soil microorganisms in this tropical soil, but also indicate a complex interaction between C, N, P and K availability. This highlights the difference between microbial C cycling responses to N, P, or K additions in the tropics and explains why coupled C, N and P cycle modeling efforts cannot rely on strict microbial stoichiometric homeostasis as an underlying assumption.

  • pH-Dependent Bioavailability, Speciation, and Phytotoxicity of Tungsten (W) in Soil Affect Growth and Molybdoenzyme Activity of Nodulated Soybeans

    Oburger E, Cid CV, Preiner J, Hu J, Hann S, Wanek W, Richter A
    2018 - Environmental Science & Technology, 52: 6146-6156


    Increasing use of tungsten (W)-based products opened new pathways for W into environmental systems. Due to its chemical alikeness with molybdenum (Mo), W is expected to behave similarly to its “twin element”, Mo; however, our knowledge of the behavior of W in the plant−soil environment remains inadequate. The aim of this study was to investigate plant growth as well as W and nutrient uptake depending on soil chemical properties such as soil pH and texture. Soybean (Glycine max cv. Primus) was grown on two acidic soils differing in soil texture that were either kept at their natural soil pH (pH of 4.5−5) or limed (pH of ≥7) and amended with increasing concentrations of metallic W (control and 500 and 5000 mg kg−1 ). In addition, the activity of molybdoenzymes involved in N assimilation (nitrate reductase) and symbiotic N2 fixation (nitrogenase) was also investigated. Our results showed that the risk of W entering the food web was significantly greater in high-pH soils due to increased solubility of mainly monomeric W. The effect of soil texture on W solubility and phytoavailability was less pronounced compared to soil pH. Particularly at intermediate W additions (W 500 mg kg−1 ), symbiotic nitrogen fixation was able to compensate for reduced leaf nitrate reductase activity. When W soil solution concentrations became too toxic (W 5000 mg kg−1 ), nodulation was more strongly inhibited than nitrogenase activity in the few nodules formed, suggesting a more-efficient detoxification and compartmentalization mechanism in nodules than in soybean leaves. The increasing presence of polymeric W species observed in low-pH soils spiked with high W concentrations resulted in decreased W uptake. Simultaneously, polymeric W species had an overall negative effect on nutrient assimilation and plant growth, suggesting a greater phytotoxicity of W polymers. Our study demonstrates the importance of accounting for soil pH in risk assessment studies of W in the plant−soil environment, something that has been completely neglected in the past.

  • Standardized protocols and procedures can precisely and accurately quantify non-structural carbohydrates

    Landhäuser SM, Chow PS, Dickman LT, Furze ME, Kuhlman I, Schmid S, Wiesenbauer J, Wild B, Gleixner G, Hartmann H, Hoch G, McDowell NG, Richardson AD, Richter A, Adams HD
    2018 - Tree Physiology, e-publication, 1-15


    Non-structural carbohydrates (NSCs), the stored products of photosynthesis, building blocks for growth and fuel for respiration, are central to plant metabolism, but their measurement is challenging. Differences in methods and procedures among laboratories can cause results to vary widely, limiting our ability to integrate and generalize patterns in plant carbon balance among studies. A recent assessment found that NSC concentrations measured for a common set of samples can vary by an order of magnitude, but sources for this variability were unclear. We measured a common set of nine plant material types, and two synthetic samples with known NSC concentrations, using a common protocol for sugar extraction and starch digestion, and three different sugar quantification methods (ion chromatography, enzyme, acid) in six laboratories. We also tested how sample handling, extraction solvent and centralizing parts of the procedure in one laboratory affected results. Non-structural carbohydrate concentrations measured for synthetic samples were within about 11.5% of known values for all three methods. However, differences among quantification methods were the largest source of variation in NSC measurements for natural plant samples because the three methods quantify different NSCs. The enzyme method quantified only glucose, fructose and sucrose, with ion chromatography we additionally quantified galactose, while the acid method quantified a large range of mono- and oligosaccharides. For some natural samples, sugars quantified with the acid method were two to five times higher than with other methods, demonstrating that trees allocate carbon to a range of sugar molecules. Sample handling had little effect on measurements, while ethanol sugar extraction improved accuracy over water extraction. Our results demonstrate that reasonable accuracy of NSC measurements can be achieved when different methods are used, as long as protocols are robust and standardized. Thus, we provide detailed protocols for the extraction, digestion and quantification of NSCs in plant samples, which should improve the comparability of NSC measurements among laboratories.

  • Microbial temperature sensitivity and biomass change explain soil carbon loss with warming

    Walker TWN, Kaiser C, Strasser F, Herbold CW, Leblans NIW, Woebken D, Janssens IA, Sigurdsson BD, Richter A
    2018 - Nature Climate Change, 8: 885-889


    Soil microorganisms control carbon losses from soils to the atmosphere, yet their responses to climate warming are often short-lived and unpredictable. Two mechanisms, microbial acclimation and substrate depletion, have been proposed to explain temporary warming effects on soil microbial activity. However, empirical support for either mechanism is unconvincing. Here we used geothermal temperature gradients (>50 years of field warming) and a short-term experiment to show that microbial activity (gross rates of growth, turnover, respiration and carbon uptake) is intrinsically temperature sensitive and does not acclimate to warming (+6 °C) over weeks or decades. Permanently accelerated microbial activity caused carbon loss from soil. However, soil carbon loss was temporary because substrate depletion reduced microbial biomass and constrained the influence of microbes over the ecosystem. A microbial biogeochemical model showed that these observations are reproducible through a modest, but permanent, acceleration in microbial physiology. These findings reveal a mechanism by which intrinsic microbial temperature sensitivity and substrate depletion together dictate warming effects on soil carbon loss via their control over microbial biomass. We thus provide a framework for interpreting the links between temperature, microbial activity and soil carbon loss on timescales relevant to Earth’s climate system.

  • A plant–microbe interaction framework explaining nutrient effects on primary production

    Capek P, Manzoni S, Kaštovská E, Wild B, Diakova K, Barta J, Schnecker J, Biasi C, Martikainen P, Alves R, Guggenberger G, Gentsch N, Hugelius G, Palmtag J, Mikutta R, Shibistova O, Urich T, Schleper C, Richter A, Santruckova H
    2018 - Nature Ecology & Evolution, 2: 1588-1596


    In most terrestrial ecosystems, plant growth is limited by nitrogen (N) and phosphorus (P). Adding either nutrient to soil usually affects primary production, but their effects can be positive or negative. Here we provide a general stoichiometric framework for interpreting these contrasting effects. First, we identify N and P limitations on plants and soil microorganisms using their respective N to P critical ratios. Second, we use these ratios to show how soil microorganisms mediate the response of primary production to limiting and non-limiting nutrient addition along a wide gradient of soil nutrient availability. Using a meta-analysis of 51 factorial N-P fertilization experiments conducted across multiple ecosystems, we demonstrate that the response of primary production to N and P additions is accurately predicted by our stoichiometric framework. The only pattern that could not be predicted by our original framework suggests that N has not only a structural function in growing organisms, but also a key role in promoting plant and microbial nutrient acquisition. We conclude that this stoichiometric framework offers the most parsimonious way to interpret contrasting and until now unresolved responses of primary production to nutrient addition in terrestrial ecosystems.

  • Temperature response of permafrost soil carbon is attenuated by mineral protection

    Gentsch N, Wild B, Mikutta R, Capek P, Diakova K, Schrumpf M, Turner S, Minnich C, Schaarschmidt F, Shibistova O, Schnecker J, Urich T, Gittel A, Santruckova H, Barta J, Lashchinskiy N, Fuß R, Richter A, Guggenberger G
    2018 - Global Change Biology, 8: 3401-3415


    Climate change in Arctic ecosystems fosters permafrost thaw and makes massive amounts of ancient soil organic carbon (OC) available to microbial breakdown. However, fractions of the organic matter (OM) may be protected from rapid decomposition by their association with minerals. Little is known about the effects of mineral‐organic associations (MOA) on the microbial accessibility of OM in permafrost soils and it is not clear which factors control its temperature sensitivity. In order to investigate if and how permafrost soil OC turnover is affected by mineral controls, the heavy fraction (HF) representing mostly MOA was obtained by density fractionation from 27 permafrost soil profiles of the Siberian Arctic. In parallel laboratory incubations, the unfractionated soils (bulk) and their HF were comparatively incubated for 175 days at 5 and 15°C. The HF was equivalent to 70 ± 9% of the bulk CO2 respiration as compared to a share of 63 ± 1% of bulk OC that was stored in the HF. Significant reduction of OC mineralization was found in all treatments with increasing OC content of the HF (HF‐OC), clay‐size minerals and Fe or Al oxyhydroxides. Temperature sensitivity (Q10) decreased with increasing soil depth from 2.4 to 1.4 in the bulk soil and from 2.9 to 1.5 in the HF. A concurrent increase in the metal‐to‐HF‐OC ratios with soil depth suggests a stronger bonding of OM to minerals in the subsoil. There, the younger 14C signature in CO2 than that of the OC indicates a preferential decomposition of the more recent OM and the existence of a MOA fraction with limited access of OM to decomposers. These results indicate strong mineral controls on the decomposability of OM after permafrost thaw and on its temperature sensitivity. Thus, we here provide evidence that OM temperature sensitivity can be attenuated by MOA in permafrost soils.

  • Application of stable-isotope labelling techniques for the detection of active diazotrophs

    Angel R, Panhölzl C, Gabriel R, Herbold C, Wanek W, Richter A, Eichorst SA, Woebken D
    2018 - Environ Microbiol, 20: 44-61


    nvestigating active participants in the fixation of dinitrogen gas is vital as N is often a limiting factor for primary production. Biological nitrogen fixation is performed by a diverse guild of bacteria and archaea (diazotrophs), which can be free-living or symbionts. Free-living diazotrophs are widely distributed in the environment, yet our knowledge about their identity and ecophysiology is still limited. A major challenge in investigating this guild is inferring activity from genetic data as this process is highly regulated. To address this challenge, we evaluated and improved several 15 N-based methods for detecting N2 fixation activity (with a focus on soil samples) and studying active diazotrophs. We compared the acetylene reduction assay and the 15 N2 tracer method and demonstrated that the latter is more sensitive in samples with low activity. Additionally, tracing 15 N into microbial RNA provides much higher sensitivity compared to bulk soil analysis. Active soil diazotrophs were identified with a 15 N-RNA-SIP approach optimized for environmental samples and benchmarked to 15 N-DNA-SIP. Lastly, we investigated the feasibility of using SIP-Raman microspectroscopy for detecting 15 N-labelled cells. Taken together, these tools allow identifying and investigating active free-living diazotrophs in a highly sensitive manner in diverse environments, from bulk to the single-cell level.

  • Global patterns of phosphatase activity in natural soils

    Margalef O, Sardans J, Fernández-Martínez M, Molowny-Horas R, Janssens IA, Ciais P, Richter A, Obersteiner M, Asenio D, Peñuelas J
    2017 - Scientific Reports, 7: 13


    Soil phosphatase levels strongly control the biotic pathways of phosphorus (P), an essential element for
    life, which is often limiting in terrestrial ecosystems. We investigated the influence of climatic and soil
    traits on phosphatase activity in terrestrial systems using metadata analysis from published studies.
    This is the first analysis of global measurements of phosphatase in natural soils. Our results suggest
    that organic P (Porg), rather than available P, is the most important P fraction in predicting phosphatase
    activity. Structural equation modeling using soil total nitrogen (TN), mean annual precipitation, mean
    annual temperature, thermal amplitude and total soil carbon as most available predictor variables
    explained up to 50% of the spatial variance in phosphatase activity. In this analysis, Porg could not be
    tested and among the rest of available variables, TN was the most important factor explaining the
    observed spatial gradients in phosphatase activity. On the other hand, phosphatase activity was also
    found to be associated with climatic conditions and soil type across different biomes worldwide. The
    close association among different predictors like Porg, TN and precipitation suggest that P recycling is
    driven by a broad scale pattern of ecosystem productivity capacity.

  • Post photosynthetic carbon partitioning to sugar alcohols and consequences for plant growth

    Dumschott K, Richter A, Loescher W, Merchant A
    2017 - Phytochemistry, 144: 243-252


    The occurrence of sugar alcohols is ubiquitous among plants. Physiochemical properties of sugar alcohols suggest numerous primary and secondary functions in plant tissues and are often well documented. In addition to functions arising from physiochemical properties, the synthesis of sugar alcohols may have significant influence over photosynthetic, respiratory, and developmental processes owing to their function as a large sink for photosynthates. Sink strength is demonstrated by the high concentrations of sugar alcohols found in plant tissues and their ability to be readily transported. The plant scale distribution and physiochemical function of these compounds renders them strong candidates for functioning as stress metabolites. Despite this, several aspects of sugar alcohol biosynthesis and function are poorly characterised namely: 1) the quantitative characterisation of carbon flux into the sugar alcohol pool; 2) the molecular control governing sugar alcohol biosynthesis on a quantitative basis; 3) the role of sugar alcohols in plant growth and ecology; and 4) consequences of sugar alcohol synthesis for yield production and yield quality. We highlight the need to adopt new approaches to investigating sugar alcohol biosynthesis using modern technologies in gene expression, metabolic flux analysis and agronomy. Combined, these approaches will elucidate the impact of sugar alcohol biosynthesis on growth, stress tolerance, yield and yield quality.

  • Rhizospheric microbial community of Caesalpinia spinosa (Mol.) Kuntze in conserved and deforested zones of the Atiquipa fog forest in Peru

    Cordero I, Ruiz-Diez B, Balaguer L, Richter A, Pueyo JJ, Rincon A
    2017 - Applied Soil Ecology, 114: 132-141


    Caesalpinia spinosa, tara, is the predominant fog catcher tree in the fog forest of Atiquipa, a biodiversity hotspot ecosystem within the coastal Peruvian desert highly threatened by intense land use over time. We investigated the impact of deforestation, as well as potential effects of the tree age (juveniles vs adults) and the type of tree (recruited vs planted), on the rhizospheric microbial communities of tara growing in contrasting landscapes (conserved vs deforested) of the Atiquipa forest.

    We used a phospholipid fatty acids analysis approach to study the microbial community associated with tara. Additionally, we isolated and sought for native rhizospheric bacteria with plant growth promoting (PGPR) traits to be used as potential inoculants for restoration projects.

    Deforestation profoundly altered the chemical and biological fertility of soils. All rhizospheric microorganisms were clearly reduced in abundance by deforestation, while the age or the type of trees had no effects. Both, deforestation and tree age influenced the assemblage of microbial communities, which tightly correlated with soil pH and organic matter among other soil properties. Adult trees harboured similar microbial communities in conserved and deforested soils being potential reservoirs of native microorganisms in the degraded areas. Some selected bacterial strains showed high plant growth promoting abilities, and PGPR traits were related with the isolation source of bacteria. The knowledge about key factors structuring the rhizospheric microbiota of tara and the identification of high-performing PGPR strains, provide a solid framework to formulate inocula for their use in restoration programmes in the Atiquipa fog forest.

  • Microbial utilization of mineral-associated nitrogen in soils

    Turner S, Meyer-Stüve S, Schippers A, Guggenberger G, Schaarschmidt F, Wild B, Richter A, Dohrmann R, Mikutta R
    2017 - Soil Biology and Biochemistry, 104: 185-196


    In soils, a large portion of organic nitrogen (ON) is associated with minerals and thus, possibly stabilized against biological decay. We therefore tested if mineral-associated N is an important N source for soil microorganisms, and which soil parameters control its bioavailability. Microcosm experiments with mineral-associated organic matter, obtained as heavy fraction (HF) via density fractionation, and bulk soil from mineral topsoil of the Franz Josef chronosequence were conducted for 125 days. We examined the effects of O2 status, soil age (differences in mineralogical properties), as well as cellulose and phosphate additions on the turnover of mineral-associated N. Using a combination of activity measurements and quantitative PCR, microbial N transformation rates and abundances of N-related functional genes (amoAnarGchiA) were determined. Similar or higher values for microbial N cycling rates and N-related functional abundances in the HF compared to bulk soil indicated that mineral-associated N provides an important bioavailable N source for soil microorganism. The turnover of mineral-associated N was mainly controlled by the O2 status. Besides, soil mineralogical properties significantly affected microbial N cycling and related gene abundances with the effect depending on the N substrate type (ON, NH4+ or NO3). In contrast, cellulose or phosphate addition hardly enhanced microbial utilization of mineral-associated N. The results of our microcosm study indicate that mineral-associated N is highly bioavailable in mineral topsoils, but effects of the mineral phase differ between N cycling processes.

  • Optimal metabolic regulation along resource stoichiometry gradients

    Manzoni S, Capek P, Mooshammer M, Lindahl BD, Richter A, Santruckova H
    2017 - Ecology Letters, 20: 1182-1191


    Most heterotrophic organisms feed on substrates that are poor in nutrients compared to their
    demand, leading to elemental imbalances that may constrain their growth and function. Flexible
    carbon (C)-use efficiency (CUE, C used for growth over C taken up) can represent a strategy to
    reduce elemental imbalances. Here, we argue that metabolic regulation has evolved to maximise
    the organism growth rate along gradients of nutrient availability and translated this assumption
    into an optimality model that links CUE to substrate and organism stoichiometry. The optimal
    CUE is predicted to decrease with increasing substrate C-to-nutrient ratio, and increase with
    nutrient amendment. These predictions are generally confirmed by empirical evidence from a new
    database of c. 2200 CUE estimates, lending support to the hypothesis that CUE is optimised
    across levels of organisation (microorganisms and animals), in aquatic and terrestrial systems, and
    when considering nitrogen or phosphorus as limiting nutrients.

  • Decoupling of microbial carbon, nitrogen, and phosphorus cycling in response to extreme temperature events

    Mooshammer M, Hofhansl F, Frank AH, Wanek W, Hämmerle I, Leitner S, Schnecker J, Wild B, Watzka M, Keiblinger KM, Zechmeister­‐Boltenstern S, Richter A
    2017 - Science Advances, 3: 13


    Predicted changes in the intensity and frequency of climate extremes urge a better mechanistic understanding of the
    stress response of microbially mediated carbon (C) and nutrient cycling processes. We analyzed the resistance and
    resilience of microbial C, nitrogen (N), and phosphorus (P) cycling processes and microbial community composition
    in decomposing plant litter to transient, but severe, temperature disturbances, namely, freeze-thaw and heat. Disturbances
    led temporarily to a more rapid cycling of C and N but caused a down-regulation of P cycling. In contrast to the
    fast recovery of the initially stimulated C and N processes, we found a slow recovery of P mineralization rates, which
    was not accompanied by significant changes in community composition. The functional and structural responses to
    the two distinct temperature disturbances were markedly similar, suggesting that direct negative physical effects and
    costs associated with the stress response were comparable. Moreover, the stress response of extracellular enzyme
    activities, but not that of intracellular microbial processes (for example, respiration or N mineralization), was
    dependent on the nutrient content of the resource through its effect on microbial physiology and community
    composition. Our laboratory study provides novel insights into the mechanisms of microbial functional stress responses
    that can serve as a basis for field studies and, in particular, illustrates the need for a closer integration of
    microbial C-N-P interactions into climate extremes research.

  • Geothermal ecosystems as natural climate change experiments: The ForHot research site in Iceland as a case study

    Sigurdsson BD, Leblans NIW, Dauwe S, Guðmundsdóttir E, Gundersen P, Gunnarsdóttir GE, Holmstrup M, Ilieva-Makulec K, Kätterer T, Marteinsdóttir B, Maljanen M, Oddsdóttir ES, Ostonen I, Peñuelas J, Poeplau C, Richter A, Sigurðsson P, Van Bodegom P, Wallander H, Weedon J, Janssens I
    2016 - Icelandic Agricultural Sciences (IAS), 29: 53-71


    This article describes how natural geothermal soil temperature gradients in Iceland have been used to study terrestrial ecosystem responses to soil warming. The experimental approach was evaluated at three study sites in southern Iceland; one grassland site that has been warm for at least 50 years (GO), and another comparable grassland site (GN) and a Sitka spruce plantation (FN) site that have both been warmed since an earthquake took place in 2008. Within each site type, five ca. 50 m long transects, with six permanent study plots each, were established across the soil warming gradients, spanning from unwarmed control conditions to gradually warmer soils. It was attempted to select the plots so the annual warming levels would be ca. +1, +3, +5, +10 and +20 °C within each transect. Results of continuous measurements of soil temperature (Ts) from 2013-2015 revealed that the soil warming was relatively constant and followed the seasonal Ts cycle of the unwarmed control plots. Volumetric water content in the top 5 cm of soil was repeatedly surveyed during 2013-2016. The grassland soils were wetter than the FN soils, but they had sometimes some significant warming-induced drying in the surface layer of the warmest plots, in contrast to FN. Soil chemistry did not show any indications that geothermal water had reached the root zone, but soil pH did increase somewhat with warming, which was probably linked to vegetation changes. As expected, the potential decomposition rate of organic matter increased significantly with warming. It was concluded that the natural geothermal gradients at the ForHot sites in Iceland offered realistic conditions for studying terrestrial ecosystem responses to warming with minimal artefacts. 

  • Drought history affects grassland plant and microbial carbon turnover during and after a subsequent drought event

    Fuchslueger L, Bahn M, Hasibeder R, Kienzl S, Fritz K, Schmitt M, Watzka M, Richter A
    2016 - Journal of Ecology, 104: 1453-1465



    1. Drought periods are projected to become more severe and more frequent in many European regions. While effects of single strong droughts on plant and microbial carbon (C) dynamics have been studied in some detail, impacts of recurrent drought events are still little understood.
    2. We tested whether the legacy of extreme experimental drought affects responses of plant and microbial C and nitrogen (N) turnover to further drought and rewetting. In a mountain grassland, we conducted a 13C pulse-chase experiment during a naturally occurring drought and rewetting event in plots previously exposed to experimental droughts and in ambient controls (AC). After labelling, we traced 13C below-ground allocation and incorporation into soil microbes using phospholipid fatty acid biomarkers.
    3. Drought history (DH) had no effects on the standing shoot and fine root plant biomass. However, plants with experimental DH displayed decreased shoot N concentrations and increased fine root N concentrations relative to those in AC. During the natural drought, plants with DH assimilated and allocated less 13C below-ground; moreover, fine root respiration was reduced and not fuelled by fresh C compared to plants in AC.
    4. Regardless of DH, microbial biomass remained stable during natural drought and rewetting. Although microbial communities initially differed in their composition between soils with and without DH, they responded to the natural drought and rewetting in a similar way: gram-positive bacteria increased, while fungal and gram-negative bacteria remained stable. In soils with DH, a strongly reduced uptake of recent plant-derived 13C in microbial biomarkers was observed during the natural drought, pointing to a smaller fraction of active microbes or to a microbial community that is less dependent on plant C.
    5. Synthesis. Drought history can induce changes in above- vs. below-ground plant N concentrations and affect the response of plant C turnover to further droughts and rewetting by decreasing plant C uptake and below-ground allocation. DH does not affect the responses of the microbial community to further droughts and rewetting, but alters microbial functioning, particularly the turnover of recent plant-derived carbon, during and after further drought periods.
  • Exploring the metabolic potential of microbial communities in ultra-basic, reducing springs at The Cedars, CA, USA: Experimental evidence of microbial methanogenesis and heterotrophic acetogenesis

    Kohl L, Cumming E, Cox A, Rietze A, Morrissey L, Lang SQ, Richter A, Suzuki S, Nealson KH, Morrill PL
    2016 - Journal of Geophysical Research Biogeosciences, 4: 1203-1220


    Present-day serpentinization generates groundwaters with conditions (pH > 11, Eh < −550 mV) favorable for the microbial and abiotic production of organic compounds from inorganic precursors. Elevated concentrations of methane, C2-C6 alkanes, acetate, and formate have been detected at these sites, but the microbial or abiotic origin of these compounds remains unclear. While geochemical data indicate that methane at most sites of present-day serpentinization is abiogenic, the stable carbon, hydrogen, and clumped isotope data as well as the hydrocarbon gas composition from The Cedars, CA, USA, are consistent with a microbial origin for methane. However, there is no direct evidence of methanogenesis at this site of serpentinization. We report on laboratory experiments in which the microbial communities in fluids and sediments from The Cedars were incubated with 13C labeled substrates. Increasing methane concentrations and the incorporation of 13C into methane in live experiments, but not in killed controls, demonstrated that methanogens converted methanol, formate, acetate (methyl group), and bicarbonate to methane. The apparent fractionation between methane and potential substrates (α13CCH4-CO2(g) = 1.059 to 1.105, α13CCH4-acetate = 1.042 to 1.119) indicated that methanogenesis was dominated by the carbonate reduction pathway. Increasing concentrations of volatile organic acid anions indicated microbial acetogenesis. α13CCO2(g)-acetate values (0.999 to 1.000), however, were inconsistent with autotrophic acetogenesis, thus suggesting that acetate was produced through fermentation. This is the first study to show direct evidence of microbial methanogenesis and acetogenesis by the native microbial community at a site of present-day serpentinization.

  • Environmental and landscape controls of soil organic carbon storage in continuous permafrost terrain of the Taymyr Peninsula (N Siberia, Russia)

    Palmtag J, Ramage J, Hugelius G, Gentsch N, Lashchinskiy N, Richter A, Kuhry P
    2016 - European Journal of Soil Science, 67: 478-491



    This research examined soil organic carbon (SOC), total nitrogen (TN) and aboveground phytomass carbon (PhC) stocks in two areas of the Taymyr Peninsula, northern Siberia. We combined field sampling, chemical and 14C radiocarbon dating analyses with land cover classifications for landscape-level assessments. The estimated mean for the 0–100-cm depth SOC stocks was 14.8 and 20.8 kg C m−2 in Ary-Mas and Logata, respectively. The corresponding values for TN were 1.0 and 1.3 kg N m−2. On average, about 2% only (range 0–12%) of the total ecosystem C is stored in PhC. In both study areas about 34% of the SOC at 0–100 cm is stored in cryoturbated pockets, which have formed since at least the early Holocene. The larger carbon/nitrogen (C/N) ratio of this cryoturbated material indicates that it consists of relatively undecomposed soil organic matter (SOM). There are substantial differences in SOC stocks and SOM properties within and between the two study areas, which emphasizes the need to consider both geomorphology and soil texture in the assessment of landscape-level and regional SOC stocks.


    • This research addresses landscape-scale and regional variation in SOC stocks.
    • Landform and soil texture are taken into account in the analysis.
    • The contribution of phytomass to total ecosystem C stored is limited.
    • Large SOC stocks are susceptible to decomposition following permafrost thaw.

  • Soil microbial carbon use efficiency and biomass turnover in a long-term fertilization experiment in a temperate grassland

    Spohn M, Pötsch EM, Eichhorst SA, Woebken D, Wanek W, Richter A
    2016 - Soil Biology and Biochemistry, 97: 168-175


    Soil microbial carbon use efficiency (CUE), defined as the ratio of organic C allocated to growth over organic C taken up, strongly affects soil carbon (C) cycling. Despite the importance of the microbial CUE for the terrestrial C cycle, very little is known about how it is affected by nutrient availability. Therefore, we studied microbial CUE and microbial biomass turnover time in soils of a long-term fertilization experiment in a temperate grassland comprising five treatments (control, PK, NK, NP, NPK). Microbial CUE and the turnover of microbial biomass were determined using a novel substrate-independent method based on incorporation of 18O from labeled water into microbial DNA. Microbial respiration was 28–37% smaller in all three N treatments (NK, NP, and NPK) compared to the control, whereas the PK treatment did not affect microbial respiration. N-fertilization decreased microbial C uptake, while the microbial growth rate was not affected. Microbial CUE ranged between 0.31 and 0.45, and was 1.3- to 1.4-fold higher in the N-fertilized soils than in the control. The turnover time ranged between 80 and 113 days and was not significantly affected by fertilization. Net primary production (NPP) and the abundance of legumes differed strongly across the treatments, and the fungal:bacterial ratio was very low in all treatments. Structural equation modeling revealed that microbial CUE was exclusively controlled by N fertilization and that neither the abundance of legumes (as a proxy for the quality of the organic matter inputs) nor NPP (as a proxy for C inputs) had an effect on microbial CUE. Our results show that N fertilization did not only decrease microbial respiration, but also microbial C uptake, indicating that less C was intracellularly processed in the N fertilized soils. The reason for reduced C uptake and increased CUE in the N-fertilization treatments is likely an inhibition of oxidative enzymes involved in the degradation of aromatic compounds by N in combination with a reduced energy requirement for microbial N acquisition in the fertilized soils. In conclusion, the study shows that N availability can control soil C cycling by affecting microbial CUE, while plant community-mediated changes in organic matter inputs and P and K availability played no important role for C partitioning of the microbial community in this temperate grassland.

  • Microbial carbon use efficiency and biomass turnover times depending on soil depth - Implications for carbon cycling.

    Spohn M, Klaus K, Wanek W, Richter A
    2016 - Soil Biology and Biochemistry, 96: 74-81


    Processing of organic carbon (C) by soil microorganisms is a key process of terrestrial C cycling. For this reason we studied (i) microbial carbon use efficiency (CUE) defined as C allocated to growth over organic C taken up by the microbial community, and (ii) the turnover time of microbial biomass in a pasture and in two forest soils. We hypothesized that microbial CUE decreases in mineral soils with depth from the topsoil to the subsoil, while the turnover time of the microbial biomass increases due to energetic constrains. We determined microbial CUE and turnover of microbial biomass C using a novel substrate-independent method based on incorporation of 18O from labeled water into microbial DNA with concurrent measurements of basal respiration. Microorganisms showed decreasing C uptake rates with decreasing C contents in the deeper soil layers. In the forest soils, no adaptation of microbial CUE with soil depth took place, i.e., microbes in the forest topsoil used C at the same efficiency as microbes in the subsoil. However, in the pasture soil, microbial CUE decreased in the lower soil layers compared to the topsoil, indicating that microorganisms in the deeper soil layers allocated relatively more C to respiration. In the organic soil layer, microorganisms respired more per unit microbial biomass C than in the subsoil, but had a similar CUE despite the high C-to-nitrogen and C-to-phosphorus ratios of the litter layers. The turnover time of microbial biomass increased with soil depth in the two forest soils. Thus, in the forest soils, a lower microbial C uptake rate in the deeper soil layers was partially compensated by a longer turnover time of microbial biomass C. In conclusion, our findings emphasize that in addition to microbial CUE, the turnover time of the microbial biomass strongly affects soil C cycling.


    • Soil microbial carbon use efficiency
    • Growth efficiency
    • Organic matter decomposition;
    • Microbial metabolism
    • Stoichiometry
    • Microbial biomass carbon turnover
  • Stress-induced changes in carbon allocation among metabolite pools influence isotope-based predictions of water use efficiency in Phaseolus vulgaris

    Lockhart R, Wild B, Richter A, Simonin K, Merchant A
    2016 - Functional Plant Biology, 1149-1158


    Understanding how major food crops respond to environmental stress will expand our capacity to improve food production with growing populations and a changing climate. This study uses chemical and physiological adaptations to heat, water deficit and elevated light stresses in Phaseolus vulgaris L. to identify changes in carbon (C) allocation that, combined with post-photosynthetic fractionation of C isotopes, influences water use efficiency (WUE) predictions. The chemical stress response was explored through changes in C allocation to the carbohydrate and cyclitol pools using GC–triple quadrupole MS. Carbon allocation to the sucrose pool fluctuated significantly among treatments, and the putative osmolytes and osmoprotectants (myo-inositol and D-ononitol) accumulated under stress. Significant osmotic adjustment (P < 0.05), quantified via pressure–volume curve analysis, was detected between control and stress treatments, although this was not attributable to active accumulation of the metabolites. Compound-specific 13C isotope abundance was measured using liquid chromatography isotope ratio MS to predict intrinsic WUE. In contrast to other metabolites measured, the δ13C of the sucrose pool fluctuated according to treatment and was proportional to predicted values based upon modelled Δ13C from gas exchange data. The results suggest that the accuracy and precision of predicting WUE may be enhanced by compound-specific analysis of Δ13C and that changes in the allocation of C among metabolite pools may influence WUE predictions based upon analysis of total soluble C. Overall, the plants appeared to use a range of mechanisms to cope with adverse conditions that could be utilised to improve plant breeding and management strategies.

  • Carbon isotope composition of carbohydrates and polyols in leaf and phloem sap of Phaseolus vulgaris L. influences predictions of plant water use efficiency

    Smith M, Wild B, Richter A, Simonin K, Merchant A
    2016 - Plant and Cell Physiology, 57: 1756-1766


    The use of carbon isotope abundance (δ13C) to assess plant carbon acquisition and water use has significant potential for use in crop management and plant improvement programs. Utilising Phaseolus vulgaris L. as a model system, this study demonstrates the occurrence and sensitivity of carbon isotope fractionation during the onset of abiotic stresses between leaf and phloem carbon pools. In addition to gas exchange data; compound-specific measures of carbon isotope abundance and concentrations of soluble components of phloem sap were compared to major carbohydrate and sugar alcohol pools in leaf tissue. Differences in both δ13C and concentration of metabolites were found in leaf and phloem tissues, the magnitude of which responded to changing environmental conditions. These changes have inplications for the modelling of leaf level gas exchange based upon δ13C natural abundance. While estimates of δ13C of low molecular weight carbohydrates and polyols increased the precision of predictions of water use efficiency compared to those based on bulk soluble carbon. The use of this technique requires consideration of the dynamics of the δ13C pool under investigation. Understanding the dynamics of changes in δ13C during movement and incorporation into heterotrophic tissues is vital for the continued development of tools that provide information on plant physiological performance relating to water use.

  • Plant-derived compounds stimulate the decomposition of organic matter in arctic permafrost soils

    Wild B, Gentsch N, Capek P, Diakova K, Alves RJ, Barta J, Gittel A, Hugelius G, Knoltsch A, Kuhry P, Lashchinskiy N, Mikutta R, Palmtag J, Schleper C, Schnecker J, Shibistova O, Takriti M, Torsvik VL, Urich T, Watzka M, Santruckova H, Guggenberger G, Richter A
    2016 - Scientific Reports, 6: 11


    Arctic ecosystems are warming rapidly, which is expected to promote soil organic matter (SOM) decomposition. In addition to the direct warming effect, decomposition can also be indirectly stimulated via increased plant productivity and plant-soil C allocation, and this so called “priming effect” might significantly alter the ecosystem C balance. In this study, we provide first mechanistic insights into the susceptibility of SOM decomposition in arctic permafrost soils to priming. By comparing 119 soils from four locations across the Siberian Arctic that cover all horizons of active layer and upper permafrost, we found that an increased availability of plant-derived organic C particularly stimulated decomposition in subsoil horizons where most of the arctic soil carbon is located. Considering the 1,035 Pg of arctic soil carbon, such an additional stimulation of decomposition beyond the direct temperature effect can accelerate net ecosystem C losses, and amplify the positive feedback to global warming.

  • Microbes as engines of ecosystem function: when does community structure enhance predictions of ecosystem processes?

    Graham EB, Knelman JE, Schindlbacher A, Siciliano S, Breulmann M, Yannarell A, Beman JM, Abell G, Philippot L, Prosser J, Foulquier A, Yuste JC, Glanville HC, Jones DL, Angel R, Salminen J, Newton RJ, Bürgmann H, Ingram LJ, Hamer U, Siljanen HM, Peltoniemi K, Potthast K, Bañeras L, Hartmann M, Banerjee S, Yu RQ, Nogaro G, Richter A, Koranda M, Castle SC, Goberna M, Song B, Chatterjee A, Nunes OC, Lopes AR, Cao Y, Kaisermann A, Hallin S, Strickland MS, Garcia-Pausas J, Barba J, Kang H, Isobe K, Papaspyrou S, Pastorelli R, Lagomarsino A, Lindström ES, Basiliko N, Nemergut DR
    2016 - Frontiers in microbiology, 7: 214


    Microorganisms are vital in mediating the earth's biogeochemical cycles; yet, despite our rapidly increasing ability to explore complex environmental microbial communities, the relationship between microbial community structure and ecosystem processes remains poorly understood. Here, we address a fundamental and unanswered question in microbial ecology: 'When do we need to understand microbial community structure to accurately predict function?' We present a statistical analysis investigating the value of environmental data and microbial community structure independently and in combination for explaining rates of carbon and nitrogen cycling processes within 82 global datasets. Environmental variables were the strongest predictors of process rates but left 44% of variation unexplained on average, suggesting the potential for microbial data to increase model accuracy. Although only 29% of our datasets were significantly improved by adding information on microbial community structure, we observed improvement in models of processes mediated by narrow phylogenetic guilds via functional gene data, and conversely, improvement in models of facultative microbial processes via community diversity metrics. Our results also suggest that microbial diversity can strengthen predictions of respiration rates beyond microbial biomass parameters, as 53% of models were improved by incorporating both sets of predictors compared to 35% by microbial biomass alone. Our analysis represents the first comprehensive analysis of research examining links between microbial communitystructure and ecosystem function. Taken together, our results indicate that a greater understanding of microbial communities informed by ecological principles may enhance our ability to predict ecosystem process rates relative to assessments based on environmental variables and microbial physiology.

  • Properties and bioavailability of particulate and mineral-associated organic matter in Arctic permafrost soils, Lower Kolyma Region, Russia

    Gentsch N, Mikutta R, Shibistova O, Wild B, Schnecker J, Richter A, Urich T, Gittel A, Santruckova H, Barta J, Lashchinskiy N, Mueller CW, Fuß R, Guggenberger G
    2015 - European Journal of Soil Science, 66: 722-734


    Permafrost degradation may cause strong feedbacks of arctic ecosystems to global warming, but this will depend on if, and to what extent, organic matter (OM) is protected against biodegradation by mechanisms other than freezing and anoxia. Here, we report on the amount, chemical composition and bioavailability of particulate (POM) and mineral-associated OM (MOM) in permafrost soils of the East Siberian Arctic. The average total organic carbon (OC) stock across all soils was 24.0 +/- 6.7 kg m(-2) within 100 cm soil depth. Density fractionation (density cut-off 1.6 g cm(-3)) revealed that 54 +/- 16% of the total soil OC and 64 +/- 18% of OC in subsoil horizons was bound to minerals. As well as sorption of OM to clay-sized minerals (R-2 = 0.80; P < 0.01), co-precipitation of OM with hydrolyzable metals may also transfer carbon into the mineral-bound fraction. Carbon:nitrogen ratios, stable carbon and nitrogen isotopes, C-13-NMR and X-ray photoelectron spectroscopy showed that OM is transformed in permafrost soils, which is a prerequisite for the formation of mineral-organic associations. Mineral-associated OM in deeper soil was enriched in C-13 and N-15, and had narrow C:N and large alkyl C:(O-/N-alkyl C) ratios, indicating an advanced stage of decomposition. Despite being up to several thousands of years old, when incubated under favourable conditions (60% water-holding capacity, 15 degrees C, adequate nutrients, 90 days), only 1.5-5% of the mineral-associated OC was released as CO2. In the topsoils, POM had the largest mineralization but was even less bioavailable than the MOM in subsoil horizons. Our results suggest that the formation of mineral-organic associations acts as an important additional factor in the stabilization of OM in permafrost soils. Although the majority of MOM was not prone to decomposition under favourable conditions, mineral-organic associations host a readily accessible carbon fraction, which may actively participate in ecosystem carbon exchange.

  • Storage and transformation of organic matter fractions in cryoturbated permafrost soils across the Siberian Arctic

    Gentsch N, Mikutta R, Alves RJE, Barta J, Capek P, Gittel A, Hugelius G, Kuhry P, Lashchinskiy N, Palmtag J, Richter A, Santrukova H, Schnecker J, Shibistova O, Urich T, Wild B, Guggenberger G
    2015 - Biogeosciences, 12: 4525-4542


    In permafrost soils, the temperature regime and the resulting cryogenic processes are important determinants of the storage of organic carbon (OC) and its small-scale spatial variability. For cryoturbated soils, there is a lack of research assessing pedon-scale heterogeneity in OC stocks and the transformation of functionally different organic matter (OM) fractions, such as particulate and mineral-associated OM. Therefore, pedons of 28 Turbels were sampled in 5m wide soil trenches across the Siberian Arctic to calculate OC and total nitrogen (TN) stocks based on digital profile mapping. Density fractionation of soil samples was performed to distinguish between particulate OM (light fraction, LF, < 1.6 g cm(-3)), mineral associated OM (heavy fraction, HF, > 1.6 g cm(-3)), and a mobilizable dissolved pool (mobilizable fraction, MoF). Across all investigated soil profiles, the total OC storage was 20.2 +/- 8.0 kgm(-2) (mean +/- SD) to 100 cm soil depth. Fifty-four percent of this OC was located in the horizons of the active layer (annual summer thawing layer), showing evidence of cryoturbation, and another 35% was present in the upper permafrost. The HF-OC dominated the overall OC stocks (55 %), followed by LF-OC (19% in mineral and 13% in organic horizons). During fractionation, approximately 13% of the OC was released as MoF, which likely represents a readily bioavailable OM pool. Cryogenic activity in combination with cold and wet conditions was the principle mechanism through which large OC stocks were sequestered in the subsoil (16.4 +/- 8.1 kgm(-2); all mineral B, C, and permafrost horizons). Approximately 22% of the subsoil OC stock can be attributed to LF material subducted by cryoturbation, whereas migration of soluble OM along freezing gradients appeared to be the principle source of the dominant HF (63 %) in the subsoil. Despite the unfavourable abiotic conditions, low C/N ratios and high delta C-13 values indicated substantial microbial OM transformation in the subsoil, but this was not reflected in altered LF and HF pool sizes. Partial least-squares regression analyses suggest that OC accumulates in the HF fraction due to co-precipitation with multivalent cations (Al, Fe) and association with poorly crystalline iron oxides and clay minerals. Our data show that, across all permafrost pedons, the mineral-associated OM represents the dominant OM fraction, suggesting that the HF-OC is the OM pool in permafrost soils on which changing soil conditions will have the largest impact.

  • The application of ecological stoichiometry to plant-microbial-soil organic matter transformations

    Zechmeister-Boltenstern S, Keiblinger KM, Mooshammer M, Peñuelas J, Richter A, Sardans J, Wanek W
    2015 - Ecological Monographs, 85: 135-155


    Elemental stoichiometry constitutes an inherent link between biogeochemistry and the structure and processes within food webs, and thus is at the core of ecosystem functioning. Stoichiometry allows for spanning different levels of biological organization, from cellular metabolism to ecosystem structure and nutrient cycling, and is therefore particularly useful for establishing links between different ecosystem compartments. We review elemental carbon : nitrogen : phosphorus (C:N:P) ratios in terrestrial ecosystems (from vegetation, leaf litter, woody debris, and dead roots, to soil microbes and organic matter). While the stoichiometry of the plant, litter, and soil compartments of ecosystems is well understood, heterotrophic microbial communities, which dominate the soil food web and drive nutrient cycling, have received increasing interest in recent years. This review highlights the effects of resource stoichiometry on soil microorganisms and decomposition, specifically on the structure and function of heterotrophic microbial communities and suggests several general patterns. First, latitudinal gradients of soil and litter stoichiometry are reflected in microbial community structure and function. Second, resource stoichiometry may cause changes in microbial interactions and community dynamics that lead to feedbacks in nutrient availability. Third, global change alters the C:N, C:P, and N:P ratios of primary producers, with repercussions for microbial decomposer communities and critical ecosystem services such as soil fertility. We argue that ecological stoichiometry provides a framework to analyze and predict such global change effects at various scales.

  • Social dynamics within decomposer communities lead to nitrogen retention and organic matter build-up in soils

    Kaiser C, Franklin O, Richter A, Dieckmann U
    2015 - Nature Communication, 6: 8960


    The chemical structure of organic matter has been shown to be only marginally important for its decomposability by microorganisms. The question of why organic matter does accumulate in the face of powerful microbial degraders is thus key for understanding terrestrial carbon and nitrogen cycling. Here we demonstrate, based on an individual-based microbial community model, that social dynamics among microbes producing extracellular enzymes (‘decomposers’) and microbes exploiting the catalytic activities of others (‘cheaters’) regulate organic matter turnover. We show that the presence of cheaters increases nitrogen retention and organic matter build-up by downregulating the ratio of extracellular enzymes to total microbial biomass, allowing nitrogen-rich microbial necromass to accumulate. Moreover, increasing catalytic efficiencies of enzymes are outbalanced by a strong negative feedback on enzyme producers, leading to less enzymes being produced at the community level. Our results thus reveal a possible control mechanism that may buffer soil CO2 emissions in a future climate.

  • Microbial nitrogen dynamics in organic and mineral soil horizons along a latitudinal transect in western Siberia

    Wild B, Schnecker J, Knoltsch A, Takriti M, Mooshammer M, Gentsch N, Mikutta R, Eloy Alves RJ, Gittel A, Lashchinskiy N, Richter A
    2015 - Global Biogeochemical Cycles, 29: 567-582


    Soil N availability is constrained by the breakdown of N-containing polymers such as proteins to oligopeptides and amino acids that can be taken up by plants and microorganisms. Excess N is released from microbial cells as ammonium (N mineralization), which in turn can serve as substrate for nitrification. According to stoichiometric theory, N mineralization and nitrification are expected to increase in relation to protein depolymerization with decreasing N limitation, and thus from higher to lower latitudes and from topsoils to subsoils. To test these hypotheses, we compared gross rates of protein depolymerization, N mineralization and nitrification (determined using N-15 pool dilution assays) in organic topsoil, mineral topsoil, and mineral subsoil of seven ecosystems along a latitudinal transect in western Siberia, from tundra (67 degrees N) to steppe (54 degrees N). The investigated ecosystems differed strongly in N transformation rates, with highest protein depolymerization and N mineralization rates in middle and southern taiga. All N transformation rates decreased with soil depth following the decrease in organic matter content. Related to protein depolymerization, N mineralization and nitrification were significantly higher in mineral than in organic horizons, supporting a decrease in microbial N limitation with depth. In contrast, we did not find indications for a decrease in microbial N limitation from arctic to temperate ecosystems along the transect. Our findings thus challenge the perception of ubiquitous N limitation at high latitudes, but suggest a transition from N to C limitation of microorganisms with soil depth, even in high-latitude systems such as tundra and boreal forest.

  • Storage, landscape distribution, and burial history of soil organic matter in contrasting areas of continuous permafrost

    Palmtag J, Hugelius G, Lashchinskiy N, Tamstorf MP, Richter A, Elberling B, Kuhry P
    2015 - Arctic Antarctic and Alpine Research, 47: 71-88


    This study describes and compares soil organic matter (SOM) quantity and characteristics in two areas of continuous permafrost, a mountainous region in NE Greenland (Zackenberg study site) and a lowland region in NE Siberia (Cherskiy and Shalaurovo study sites). Our assessments are based on stratified-random landscape-level inventories of soil profiles down to 1 m depth, with physico-chemical, elemental, and radiocarbon-dating analyses. The estimated mean soil organic carbon (SOC) storage in the upper meter of soils in the NE Greenland site is 8.3 +/- 1.8 kg C m(-2) compared to 20.3 +/- 2.2 kg C m(-2) and 30.0 +/- 2.0 kg C m(-2) in the NE Siberian sites (95% confidence intervals). The lower SOC storage in the High Arctic site in NE Greenland can be largely explained by the fact that 59% of the study area is located at higher elevation with mostly barren ground and thus very low SOC contents. In addition, SOC-rich fens and bogs occupy a much smaller proportion of the landscape in NE Greenland (similar to 3%) than in NE Siberia (similar to 20%). The contribution of deeper buried C-enriched material in the mineral soil horizons to the total SOC storage is lower in the NE Greenland site (similar to 13%) compared to the NE Siberian sites (similar to 24%-30%). Buried SOM seems generally more decomposed in NE Greenland than in NE Siberia, which we relate to different burial mechanisms prevailing in these regions.

  • The effect of warming on the vulnerability of subducted organic carbon in arctic soils

    Capek P, Diakova K, Dickopp JE, Barta J, Wild B, Schnecker J, Alves RJE, Aiglsdorfer S, Guggenberger G, Gentsch N, Hugelius G, Kuhry P, Lashchinsky N, Gittel A, Schleper C, Mikutta R, Palmtag J, Shibistova O, Urich T, Richter A, Santruckova H
    2015 - Soil Biology and Biochemistry, 90: 19-29


    Arctic permafrost soils contain large stocks of organic carbon (OC). Extensive cryogenic processes in these soils cause subduction of a significant part of OC-rich topsoil down into mineral soil through the process of cryoturbation. Currently, one-fourth of total permafrost OC is stored in subducted organic horizons. Predicted climate change is believed to reduce the amount of OC in permafrost soils as rising temperatures will increase decomposition of OC by soil microorganisms. To estimate the sensitivity of OC decomposition to soil temperature and oxygen levels we performed a 4-month incubation experiment in which we manipulated temperature (4-20 degrees C) and oxygen level of topsoil organic, subducted organic and mineral soil horizons. Carbon loss (C-LOSS) was monitored and its potential biotic and abiotic drivers, including concentrations of available nutrients, microbial activity, biomass and stoichiometry, and extracellular oxidative and hydrolytic enzyme pools, were measured. We found that independently of the incubation temperature, C-LOSS from subducted organic and mineral soil horizons was one to two orders of magnitude lower than in the organic topsoil horizon, both under aerobic and anaerobic conditions. This corresponds to the microbial biomass being lower by one to two orders of magnitude. We argue that enzymatic degradation of autochthonous subducted OC does not provide sufficient amounts of carbon and nutrients to sustain greater microbial biomass. The resident microbial biomass relies on allochthonous fluxes of nutrients, enzymes and carbon from the OC-rich topsoil. This results in a "negative priming effect", which protects autochthonous subducted OC from decomposition at present. The vulnerability of subducted organic carbon in cryoturbated arctic soils under future climate conditions will largely depend on the amount of allochthonous carbon and nutrient fluxes from the topsoil. (C) 2015 Elsevier Ltd. All rights reserved.

  • Non-structural carbohydrates in woody plants compared among laboratories

    Quentin AG, Pinkard EA, Ryan MG, Tissue DT, Baggett LS, Adams HD, Maillard P, Marchand J, Landhäusser SM, Lacointe A, Gibon Y, Anderegg WR, Asao S, Atkin OK, Bonhomme M, Claye C, Chow PS, Clément-Vidal A, Davies ND, Dickman LT, Dumbur R, Ellsworth DS, Falk K, Galiano L, Grünzweig JM, Hartmann H, Hoch G, Jones JE, Koike T, Kuhlmann I, Lloret F, Maestro M, Mansfield SD, Martínez-Vilalta J, Maucourt M, McDowell NG, Moing A, Muller B, Nebauer SG, Niinemets U, Palacio S, Piper F, Raveh E, Richter A, Rolland G, Rosas T, Saint Joanis B, Sala A, Smith RA, Sterck F, Stinziano JR, Tobias M, Unda F, Watanabe M, Way DA, Weerasinghe LK, Wild B, Wiley E, Woodruff DR
    2015 - Tree Physiology, 35: 1146-1165


    Non-structural carbohydrates (NSC) in plant tissue are frequently quantified to make inferences about plant responses to environmental conditions. Laboratories publishing estimates of NSC of woody plants use many different methods to evaluate NSC. We asked whether NSC estimates in the recent literature could be quantitatively compared among studies. We also asked whether any differences among laboratories were related to the extraction and quantification methods used to determine starch and sugar concentrations. These questions were addressed by sending sub-samples collected from five woody plant tissues, which varied in NSC content and chemical composition, to 29 laboratories. Each laboratory analyzed the samples with their laboratory-specific protocols, based on recent publications, to determine concentrations of soluble sugars, starch and their sum, total NSC. Laboratory estimates differed substantially for all samples. For example, estimates for Eucalyptus globulus leaves (EGL) varied from 23 to 116 (mean = 56) mg g(-1) for soluble sugars, 6-533 (mean = 94) mg g(-1) for starch and 53-649 (mean = 153) mg g(-1) for total NSC. Mixed model analysis of variance showed that much of the variability among laboratories was unrelated to the categories we used for extraction and quantification methods (method category R(2) = 0.05-0.12 for soluble sugars, 0.10-0.33 for starch and 0.01-0.09 for total NSC). For EGL, the difference between the highest and lowest least squares means for categories in the mixed model analysis was 33 mg g(-1) for total NSC, compared with the range of laboratory estimates of 596 mg g(-1). Laboratories were reasonably consistent in their ranks of estimates among tissues for starch (r = 0.41-0.91), but less so for total NSC (r = 0.45-0.84) and soluble sugars (r = 0.11-0.83). Our results show that NSC estimates for woody plant tissues cannot be compared among laboratories. The relative changes in NSC between treatments measured within a laboratory may be comparable within and between laboratories, especially for starch. To obtain comparable NSC estimates, we suggest that users can either adopt the reference method given in this publication, or report estimates for a portion of samples using the reference method, and report estimates for a standard reference material. Researchers interested in NSC estimates should work to identify and adopt standard methods. © The Author 2015. Published by Oxford University Press. All rights reserved. For Permissions, please email:

  • Microbial community composition shapes enzyme patterns in topsoil and subsoil horizons along a latitudinal transect in Western Siberia

    Schnecker J, Wild B, Takriti M, Eloy Alves RJ, Gentsch N, Gittel A, Hofer A, Klaus K, Knoltsch A, Lashchinskiy N, Mikutta R, Richter A
    2015 - Soil Biology and Biochemistry, 83: 106-115


    Soil horizons below 30 cm depth contain about 60% of the organic carbon stored in soils. Although insight into the physical and chemical stabilization of soil organic matter (SOM) and into microbial community composition in these horizons is being gained, information on microbial functions of subsoil microbial communities and on associated microbially-mediated processes remains sparse. To identify possible controls on enzyme patterns, we correlated enzyme patterns with biotic and abiotic soil parameters, as well as with microbial community composition, estimated using phospholipid fatty acid profiles. Enzyme patterns (i.e. distance-matrixes calculated from these enzyme activities) were calculated from the activities of six extracellular enzymes (cellobiohydrolase, leucine-amino-peptidase, N-acetylglucosaminidase, chitotriosidase, phosphatase and phenoloxidase), which had been measured in soil samples from organic topsoil horizons, mineral topsoil horizons, and mineral subsoil horizons from seven ecosystems along a 1500 km latitudinal transect in Western Siberia. We found that hydrolytic enzyme activities decreased rapidly with depth, whereas oxidative enzyme activities in mineral horizons were as high as, or higher than in organic topsoil horizons. Enzyme patterns varied more strongly between ecosystems in mineral subsoil horizons than in organic topsoils. The enzyme patterns in topsoil horizons were correlated with SOM content (i.e., C and N content) and microbial community composition. In contrast, the enzyme patterns in mineral subsoil horizons were related to water content, soil pH and microbial community composition. The lack of correlation between enzyme patterns and SOM quantity in the mineral subsoils suggests that SOM chemistry, spatial separation or physical stabilization of SOM rather than SOM content might determine substrate availability for enzymatic breakdown. The correlation of microbial community composition and enzyme patterns in all horizons, suggests that microbial community composition shapes enzyme patterns and might act as a modifier for the usual dependency of decomposition rates on SOM content or C/N ratios.

  • Metatranscriptomic census of active protists in soils

    Geisen S, Tveit AT, Clark IM, Richter A, Svenning MM, Bonkowski M, Urich T
    2015 - The ISME Journal, 9: 2178-2190


    The high numbers and diversity of protists in soil systems have long been presumed, but their true diversity and community composition have remained largely concealed. Traditional cultivation-based methods miss a majority of taxa, whereas molecular barcoding approaches employing PCR introduce significant biases in reported community composition of soil protists. Here, we applied a metatranscriptomic approach to assess the protist community in 12 mineral and organic soil samples from different vegetation types and climatic zones using small subunit ribosomal RNA transcripts as marker. We detected a broad diversity of soil protists spanning across all known eukaryotic supergroups and revealed a strikingly different community composition than shown before. Protist communities differed strongly between sites, with Rhizaria and Amoebozoa dominating in forest and grassland soils, while Alveolata were most abundant in peat soils. The Amoebozoa were comprised of Tubulinea, followed with decreasing abundance by Discosea, Variosea and Mycetozoa. Transcripts of Oomycetes, Apicomplexa and Ichthyosporea suggest soil as reservoir of parasitic protist taxa. Further, Foraminifera and Choanoflagellida were ubiquitously detected, showing that these typically marine and freshwater protists are autochthonous members of the soil microbiota. To the best of our knowledge, this metatranscriptomic study provides the most comprehensive picture of active protist communities in soils to date, which is essential to target the ecological roles of protists in the complex soil system.

  • Convergence of soil nitrogen isotopes across global climate gradients

    Craine JM, Elmore AJ, Wang L, Augusto L, Baisden WT, Brookshire EN, Cramer MD, Hasselquist NJ, Hobbie EA, Kahmen A; Koba K, Kranabetter JM, Mack MC, Marin-Spiotta E, Mayor JR, McLauchlan KK, Michelsen A, Nardoto GB, Oliveira RS, Perakis SS, Peri PL, Quesada CA, Richter A, Schipper LA, Stevenson BA, Turner BL, Viani RA, Wanek W, Zeller B
    2015 - Scientific Reports, 5: 8


    Quantifying global patterns of terrestrial nitrogen (N) cycling is central to predicting future patterns of primary productivity, carbon sequestration, nutrient fluxes to aquatic systems, and climate forcing. With limited direct measures of soil N cycling at the global scale, syntheses of the (15)N:(14)N ratio of soil organic matter across climate gradients provide key insights into understanding global patterns of N cycling. In synthesizing data from over 6000 soil samples, we show strong global relationships among soil N isotopes, mean annual temperature (MAT), mean annual precipitation (MAP), and the concentrations of organic carbon and clay in soil. In both hot ecosystems and dry ecosystems, soil organic matter was more enriched in (15)N than in corresponding cold ecosystems or wet ecosystems. Below a MAT of 9.8°C, soil δ(15)N was invariant with MAT. At the global scale, soil organic C concentrations also declined with increasing MAT and decreasing MAP. After standardizing for variation among mineral soils in soil C and clay concentrations, soil δ(15)N showed no consistent trends across global climate and latitudinal gradients. Our analyses could place new constraints on interpretations of patterns of ecosystem N cycling and global budgets of gaseous N loss.

  • A pan-Arctic synthesis of CH4 and CO2 production from anoxic soil incubations

    Treat C, Natali S, Ernakovich J, Iversen CM, Lupascu M, McGuire AD, Norby RJ, Roy Chowdhury T, Richter A, Santruckova H, Schädel C, Schuur EA, Sloan VL, Turetsky MR, Waldrop MP
    2015 - Global Change Biology, 21: 2787-2803


    Permafrost thaw can alter the soil environment through changes in soil moisture, frequently resulting in soil saturation, a shift to anaerobic decomposition, and changes in the plant community. These changes, along with thawing of previously frozen organic material, can alter the form and magnitude of greenhouse gas production from permafrost ecosystems. We synthesized existing methane (CH4 ) and carbon dioxide (CO2 ) production measurements from anaerobic incubations of boreal and tundra soils from the geographic permafrost region to evaluate large-scale controls of anaerobic CO2 and CH4 production and compare the relative importance of landscape-level factors (e.g., vegetation type and landscape position), soil properties (e.g., pH, depth, and soil type), and soil environmental conditions (e.g., temperature and relative water table position). We found fivefold higher maximum CH4 production per gram soil carbon from organic soils than mineral soils. Maximum CH4 production from soils in the active layer (ground that thaws and refreezes annually) was nearly four times that of permafrost per gram soil carbon, and CH4 production per gram soil carbon was two times greater from sites without permafrost than sites with permafrost. Maximum CH4 and median anaerobic CO2 production decreased with depth, while CO2 :CH4 production increased with depth. Maximum CH4 production was highest in soils with herbaceous vegetation and soils that were either consistently or periodically inundated. This synthesis identifies the need to consider biome, landscape position, and vascular/moss vegetation types when modeling CH4 production in permafrost ecosystems and suggests the need for longer-term anaerobic incubations to fully capture CH4 dynamics. Our results demonstrate that as climate warms in arctic and boreal regions, rates of anaerobic CO2 and CH4 production will increase, not only as a result of increased temperature, but also from shifts in vegetation and increased ground saturation that will accompany permafrost thaw. © 2015 John Wiley & Sons Ltd.

  • Summer drought alters carbon allocation to roots and root respiration in mountain grassland

    Hasibeder R, Fuchslueger L, Richter A, Bahn M
    2015 - New Phytologist, 3: 1117-1127


    Drought affects the carbon (C) source and sink activities of plant organs, with potential consequences for belowground C allocation, a key process of the terrestrial C cycle. The responses of belowground C allocation dynamics to drought are so far poorly understood. We combined experimental rain exclusion with (13)C pulse labelling in a mountain meadow to analyse the effects of summer drought on the dynamics of belowground allocation of recently assimilated C and how it is partitioned among different carbohydrate pools and root respiration. Severe soil moisture deficit decreased the ecosystem C uptake and the amounts and velocity of C allocated from shoots to roots. However, the proportion of recently assimilated C translocated belowground remained unaffected by drought. Reduced root respiration, reflecting reduced C demand under drought, was increasingly sustained by C reserves, whilst recent assimilates were preferentially allocated to root storage and an enlarged pool of osmotically active compounds. Our results indicate that under drought conditions the usage of recent photosynthates is shifted from metabolic activity to osmotic adjustment and storage compounds. © 2014 The Authors. New Phytologist © 2014 New Phytologist Trust.

  • Effects of drought on nitrogen turnover and abundances of ammonia-oxidizers in mountain grassland

    Fuchslueger L, Kastl EM, Bauer F, Kienzl S, Hasibeder R, Ladreiter-Knauss T, Schmitt M, Bahn M, Schloter M, Richter A, Szukics UFM
    2014 - Biogeosciences, 11: 6003-6015


    Future climate scenarios suggest an increased frequency of summer drought periods in the European Alpine Region. Drought can affect soil nitrogen (N) cycling, by altering N transformation rates, as well as the abundances of ammonia-oxidizing bacteria and archaea. However, the extent to which drought affects N cycling under in situ conditions is still controversial. The goal of this study was to analyse effects of drought on soil N turnover and ammonia-oxidizer abundances in soil without drought history. To this end we conducted rain-exclusion experiments at two differently managed mountain grassland sites, an annually mown and occasionally fertilized meadow and an abandoned grassland. Soils were sampled before, during and after drought and were analysed for potential gross rates of N mineralization, microbial uptake of inorganic N, nitrification, and the abundances of bacterial and archaeal ammonia-oxidizers based on gene copy numbers of the amoA gene (AOB and AOA, respectively). Drought induced different responses at the two studied sites. At the managed meadow drought increased NH4+ immobilization rates and NH4+ concentrations in the soil water solution, but led to a reduction of AOA abundance compared to controls. At the abandoned site gross nitrification and NO3- immobilization rates decreased during drought, while AOB and AOA abundances remained stable. Rewetting had only minor, short-term effects on the parameters that had been affected by drought. Seven weeks after the end of drought no differences to control plots could be detected. Thus, our findings demonstrated that in mountain grasslands drought had distinct transient effects on soil nitrogen cycling and ammonia-oxidizers, which could have been related to a niche differentiation of AOB and AOA with increasing NH4+ levels. However, the effect strength of drought was modulated by grassland management.

  • Nutrient limitation of alpine plants: Implications from leaf N : P stoichiometry and leaf delta N-15

    Xu X, Wanek W, Zhou C, Richter A, Song M, Cao G, Ouyang H, Kuzyakov Y
    2014 - Journal of Plant Nutrition and Soil Science, 177: 178-387


    Nitrogen (N) deposition can affect grassland ecosystems by altering biomass production, plant species composition and abundance. Therefore, a better understanding of the response of dominant plant species to N input is a prerequisite for accurate prediction of future changes and interactions within plant communities. We evaluated the response of seven dominant plant species on the Tibetan Plateau to N input at two levels: individual species and plant functional group. This was achieved by assessing leaf N : P stoichiometry, leaf delta N-15 and biomass production for the plant functional groups. Seven dominant plant species-three legumes, two forbs, one grass, one sedge-were analyzed for N, P, and delta N-15 2 years after fertilization with one of the three N forms: NO3-, NH4+, or NH4NO3 at four application rates (0, 7.5, 30, and 150 kg N ha(-1) y(-1)). On the basis of biomass production and leaf N : P ratios, we concluded that grasses were limited by available N or co-limited by available P. Unlike for grasses, leaf N : P and biomass production were not suitable indicators of N limitation for legumes and forbs in alpine meadows. The poor performance of legumes under high N fertilization was mainly due to strong competition with grasses. The total above-ground biomass was not increased by N fertilization. However, species composition shifted to more productive grasses. A significant negative correlation between leaf N : P and leaf delta N-15 indicated that the two forbs Gentiana straminea and Saussurea superba switched from N deficiency to P limitation (e. g., N excess) due to N fertilization. These findings imply that alpine meadows will be more dominated by grasses under increased atmospheric N deposition.

  • Site- and horizon-specific patterns of microbial community structure and enzyme activities in permafrost-affected soils of Greenland

    Gittel A, Barta J, Kohoutová I, Schnecker J, Wild B, Capek P, Kaiser C, Torsvik VL, Richter A, Schleper C, Urich T
    2014 - Frontiers in microbiology, 14


    Permafrost-affected soils in the Northern latitudes store huge amounts of organic carbon (OC) that is prone to microbial degradation and subsequent release of greenhouse gasses to the atmosphere. In Greenland, the consequences of permafrost thaw have only recently been addressed, and predictions on its impact on the carbon budget are thus still highly uncertain. However, the fate of OC is not only determined by abiotic factors, but closely tied to microbial activity. We investigated eight soil profiles in northeast Greenland comprising two sites with typical tundra vegetation and one wet fen site. We assessed microbial community structure and diversity (SSU rRNA gene tag sequencing, quantification of bacteria, archaea and fungi), and measured hydrolytic and oxidative enzyme activities. Sampling site and thus abiotic factors had a significant impact on microbial community structure, diversity and activity, the wet fen site exhibiting higher potential enzyme activities and presumably being a hot spot for anaerobic degradation processes such as fermentation and methanogenesis. Lowest fungal to bacterial ratios were found in topsoils that had been relocated by cryoturbation ("buried topsoils"), resulting from a decrease in fungal abundance compared to recent ("unburied") topsoils. Actinobacteria (in particular Intrasporangiaceae) accounted for a major fraction of the microbial community in buried topsoils, but were only of minor abundance in all other soil horizons. It was indicated that the distribution pattern of Actinobacteria and a variety of other bacterial classes was related to the activity of phenol oxidases and peroxidases supporting the hypothesis that bacteria might resume the role of fungi in oxidative enzyme production and degradation of phenolic and other complex substrates in these soils. Our study sheds light on the highly diverse, but poorly-studied communities in permafrost-affected soils in Greenland and their role in OC degradation.

  • Growth of nitrite-oxidizing bacteria by aerobic hydrogen oxidation

    Koch H, Galushko A, Albertsen M, Schintlmeister A, Gruber-Dorninger C, Lücker S, Pelletier E, Le Paslier D, Spieck E, Richter A, Nielsen PH, Wagner M, Daims H
    2014 - Science, 345: 1052-1054


    The bacterial oxidation of nitrite to nitrate is a key process of the biogeochemical nitrogen cycle. Nitrite-oxidizing bacteria are considered a highly specialized functional group, which depends on the supply of nitrite from other microorganisms and whose distribution strictly correlates with nitrification in the environment and in wastewater treatment plants. On the basis of genomics, physiological experiments, and single-cell analyses, we show that Nitrospira moscoviensis, which represents a widely distributed lineage of nitrite-oxidizing bacteria, has the genetic inventory to utilize hydrogen (H2) as an alternative energy source for aerobic respiration and grows on H2 without nitrite. CO2 fixation occurred with H2 as the sole electron donor. Our results demonstrate a chemolithoautotrophic lifestyle of nitrite-oxidizing bacteria outside the nitrogen cycle, suggesting greater ecological flexibility than previously assumed. Copyright © 2014, American Association for the Advancement of Science.

  • Input of easily available organic C and N stimulates microbial decomposition of soil organic matter in arctic permafrost soil

    Wild B, Schnecker J, Knoltsch A, Takriti M, Mooshammer M, Gentsch N, Mikutta R, Alves ERJ Gittel A, Lashchinskiy N, Richter A
    2014 - Soil Biology and Biochemistry, 75: 143-151


    Rising temperatures in the Arctic can affect soil organic matter (SOM) decomposition directly and indirectly, by increasing plant primary production and thus the allocation of plant-derived organic compounds into the soil. Such compounds, for example root exudates or decaying fine roots, are easily available for microorganisms, and can alter the decomposition of older SUM ("priming effect"). We here report on a SUM priming experiment in the active layer of a permafrost soil from the central Siberian Arctic, comparing responses of organic topsoil, mineral subsoil, and cryoturbated subsoil material (i.e., poorly decomposed topsoil material subducted into the subsoil by freeze-thaw processes) to additions of C-13-labeled glucose, cellulose, a mixture of amino acids, and protein (added at levels corresponding to approximately 1% of soil organic carbon). SUM decomposition in the topsoil was barely affected by higher availability of organic compounds, whereas SUM decomposition in both subsoil horizons responded strongly. In the mineral subsoil, SUM decomposition increased by a factor of two to three after any substrate addition (glucose, cellulose, amino acids, protein), suggesting that the microbial decomposer community was limited in energy to break down more complex components of SOM. In the cryoturbated horizon, SUM decomposition increased by a factor of two after addition of amino acids or protein, but was not significantly affected by glucose or cellulose, indicating nitrogen rather than energy limitation. Since the stimulation of SUM decomposition in cryoturbated material was not connected to microbial growth or to a change in microbial community composition, the additional nitrogen was likely invested in the production of extracellular enzymes required for SUM decomposition. Our findings provide a first mechanistic understanding of priming in permafrost soils and suggest that an increase in the availability of organic carbon or nitrogen, e.g., by increased plant productivity, can change the decomposition of SUM stored in deeper layers of permafrost soils, with possible repercussions on the global climate. (C) 2014 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY license (

  • Adjustment of microbial nitrogen use efficiency to carbon:nitrogen imbalances regulates soil nitrogen cycling

    Mooshammer M, Wanek W, Hämmerle I, Fuchslueger L, Hofhansl F, Knoltsch A, Schnecker J, Takriti M, Watzka M, Wild B, Keiblinger KM, Zechmeister-Boltenstern S, Richter A
    2014 - Nature Communications, 5: 3694


    Microbial nitrogen use efficiency (NUE) describes the partitioning of organic N taken up between growth and the release of inorganic N to the environment (that is, N mineralization), and is thus central to our understanding of N cycling. Here we report empirical evidence that microbial decomposer communities in soil and plant litter regulate their NUE. We find that microbes retain most immobilized organic N (high NUE), when they are N limited, resulting in low N mineralization. However, when the metabolic control of microbial decomposers switches from N to C limitation, they release an increasing fraction of organic N as ammonium (low NUE). We conclude that the regulation of NUE is an essential strategy of microbial communities to cope with resource imbalances, independent of the regulation of microbial carbon use efficiency, with significant effects on terrestrial N cycling.

  • Effects of soil organic matter properties and microbial community composition on enzyme activities in cryoturbated arctic soils

    Schnecker J, Wild B, Hofhansl F, Alves ERJ, Barta J, Capek P, Fuchslueger L, Gentsch N, Gittel A, Guggenberger G, Hofer A, Kienzl S, Knoltsch A, Lashchinskiy N, Mikutta R, Santruckova H, Shibistova O, Takriti M, Urich T, Weltin G, Richter A
    2014 - PLoS One, 9: e94076


    Enzyme-mediated decomposition of soil organic matter (SOM) is controlled, amongst other factors, by organic matter properties and by the microbial decomposer community present. Since microbial community composition and SOM properties are often interrelated and both change with soil depth, the drivers of enzymatic decomposition are hard to dissect. We investigated soils from three regions in the Siberian Arctic, where carbon rich topsoil material has been incorporated into the subsoil (cryoturbation). We took advantage of this subduction to test if SOM properties shape microbial community composition, and to identify controls of both on enzyme activities. We found that microbial community composition (estimated by phospholipid fatty acid analysis), was similar in cryoturbated material and in surrounding subsoil, although carbon and nitrogen contents were similar in cryoturbated material and topsoils. This suggests that the microbial community in cryoturbated material was not well adapted to SOM properties. We also measured three potential enzyme activities (cellobiohydrolase, leucine-amino-peptidase and phenoloxidase) and used structural equation models (SEMs) to identify direct and indirect drivers of the three enzyme activities. The models included microbial community composition, carbon and nitrogen contents, clay content, water content, and pH. Models for regular horizons, excluding cryoturbated material, showed that all enzyme activities were mainly controlled by carbon or nitrogen. Microbial community composition had no effect. In contrast, models for cryoturbated material showed that enzyme activities were also related to microbial community composition. The additional control of microbial community composition could have restrained enzyme activities and furthermore decomposition in general. The functional decoupling of SOM properties and microbial community composition might thus be one of the reasons for low decomposition rates and the persistence of 400 Gt carbon stored in cryoturbated material.

  • Microbial community dynamics alleviate stoichiometric constraints during litter decay

    Kaiser C, Franklin O, Dieckmann U, Richter A
    2014 - Ecology Letters, 17: 680-690


    Under the current paradigm, organic matter decomposition and nutrient cycling rates are a function of the imbalance between substrate and microbial biomass stoichiometry. Challenging this view, we demonstrate that in an individual-based model, microbial community dynamics alter relative C and N limitation during litter decomposition, leading to a system behaviour not predictable from stoichiometric theory alone. Rather, the dynamics of interacting functional groups lead to an adaptation at the community level, which accelerates nitrogen recycling in litter with high initial C : N ratios and thus alleviates microbial N limitation. This mechanism allows microbial decomposers to overcome large imbalances between resource and biomass stoichiometry without the need to decrease carbon use efficiency (CUE), which is in contrast to predictions of traditional stoichiometric mass balance equations. We conclude that identifying and implementing microbial community-driven mechanisms in biogeochemical models are necessary for accurately predicting terrestrial C fluxes in response to changing environmental conditions. © 2014 The Authors. Ecology Letters published by John Wiley & Sons Ltd and CNRS.

  • Stoichiometric imbalances between terrestrial decomposer communities and their resources: mechanisms and implications of microbial adaptations to their resources

    Mooshammer M, Wanek W, Zechmeister-Boltenstern S, Richter A
    2014 - Frontiers in microbiology, 5: 1-10


    Terrestrial microbial decomposer communities thrive on a wide range of organic matter types that rarely ever meet their elemental demands. In this review we synthesize the current state-of-the-art of microbial adaptations to resource stoichiometry, in order to gain a deeper understanding of the interactions between heterotrophic microbial communities and their chemical environment. The stoichiometric imbalance between microbial communities and their organic substrates generally decreases from wood to leaf litter and further to topsoil and subsoil organic matter. Microbial communities can respond to these imbalances in four ways: first, they adapt their biomass composition toward their resource in a non-homeostatic behavior. Such changes are, however, only moderate, and occur mainly because of changes in microbial community structure and less so due to cellular storage of elements in excess. Second, microbial communities can mobilize resources that meet their elemental demand by producing specific extracellular enzymes, which, in turn, is restricted by the C and N requirement for enzyme production itself. Third, microbes can regulate their element use efficiencies (ratio of element invested in growth over total element uptake), such that they release elements in excess depending on their demand (e.g., respiration and N mineralization). Fourth, diazotrophic bacteria and saprotrophic fungi may trigger the input of external N and P to decomposer communities. Theoretical considerations show that adjustments in element use efficiencies may be the most important mechanism by which microbes regulate their biomass stoichiometry. This review summarizes different views on how microbes cope with imbalanced supply of C, N and P, thereby providing a framework for integrating and linking microbial adaptation to resource imbalances to ecosystem scale fluxes across scales and ecosystems.

  • Aerobic nitrous oxide production through N-nitrosating hybrid formation in ammonia-oxidizing archaea

    Stieglmeier M, Mooshammer M, Kitzler B, Wanek W, Zechmeister-Boltenstern S, Richter A, Schleper C
    2014 - ISME Journal, 8: 1135-1146


    Soil emissions are largely responsible for the increase of the potent greenhouse gas nitrous oxide (N2O) in the atmosphere and are generally attributed to the activity of nitrifying and denitrifying bacteria. However, the contribution of the recently discovered ammonia-oxidizing archaea (AOA) to N2O production from soil is unclear as is the mechanism by which they produce it. Here we investigate the potential of Nitrososphaera viennensis, the first pure culture of AOA from soil, to produce N2O and compare its activity with that of a marine AOA and an ammonia-oxidizing bacterium (AOB) from soil. N. viennensis produced N2O at a maximum yield of 0.09% N2O per molecule of nitrite under oxic growth conditions. N2O production rates of 4.6±0.6 amol N2O cell(-1) h(-1) and nitrification rates of 2.6±0.5 fmol NO2(-) cell(-1) h(-1) were in the same range as those of the AOB Nitrosospira multiformis and the marine AOA Nitrosopumilus maritimus grown under comparable conditions. In contrast to AOB, however, N2O production of the two archaeal strains did not increase when the oxygen concentration was reduced, suggesting that they are not capable of denitrification. In (15)N-labeling experiments we provide evidence that both ammonium and nitrite contribute equally via hybrid N2O formation to the N2O produced by N. viennensis under all conditions tested. Our results suggest that archaea may contribute to N2O production in terrestrial ecosystems, however, they are not capable of nitrifier-denitrification and thus do not produce increasing amounts of the greenhouse gas when oxygen becomes limiting.

  • Distinct microbial communities associated with buried soils in the Siberian tundra

    Gittel A, Barta J, Kohoutovác I, Mikutta R, Owens S, Gilbert J, Schnecker J, Wild B, Hannisdal B, Maerz J, Lashchinskiyk N, Capek P, Santruckova H, Gentsch N, Shibistova O, Guggenberger G, Richter A, Torsvik V, Schleper C, Urich T
    2014 - ISME Journal, 8: 841-853


    Cryoturbation, the burial of topsoil material into deeper soil horizons by repeated freeze-thaw events, is an important storage mechanism for soil organic matter (SOM) in permafrost-affected soils. Besides abiotic conditions, microbial community structure and the accessibility of SOM to the decomposer community are hypothesized to control SOM decomposition and thus have a crucial role in SOM accumulation in buried soils. We surveyed the microbial community structure in cryoturbated soils from nine soil profiles in the northeastern Siberian tundra using high-throughput sequencing and quantification of bacterial, archaeal and fungal marker genes. We found that bacterial abundances in buried topsoils were as high as in unburied topsoils. In contrast, fungal abundances decreased with depth and were significantly lower in buried than in unburied topsoils resulting in remarkably low fungal to bacterial ratios in buried topsoils. Fungal community profiling revealed an associated decrease in presumably ectomycorrhizal (ECM) fungi. The abiotic conditions (low to subzero temperatures, anoxia) and the reduced abundance of fungi likely provide a niche for bacterial, facultative anaerobic decomposers of SOM such as members of the Actinobacteria, which were found in significantly higher relative abundances in buried than in unburied topsoils. Our study expands the knowledge on the microbial community structure in soils of Northern latitude permafrost regions, and attributes the delayed decomposition of SOM in buried soils to specific microbial taxa, and particularly to a decrease in abundance and activity of ECM fungi, and to the extent to which bacterial decomposers are able to act as their functional substitutes.

  • Experimental drought reduces the transfer of recently fixed plant carbon to soil microbes and alters the bacterial community composition in a mountain meadow

    Fuchslueger L, Bahn M, Fritz K, Hasibeder R, Richter A
    2014 - New Phytologist, 201: 916-927


    Drought affects plants and soil microorganisms, but it is still not clear how it alters the carbon (C) transfer at the plant-microbial interface. Here, we tested direct and indirect effects of drought on soil microbes and microbial turnover of recent plant-derived C in a mountain meadow. Microbial community composition was assessed using phospholipid fatty acids (PLFAs); the allocation of recent plant-derived C to microbial groups was analysed by pulse-labelling of canopy sections with (13) CO2 and the subsequent tracing of the label into microbial PLFAs. Microbial biomass was significantly higher in plots exposed to a severe experimental drought. In addition, drought induced a shift of the microbial community composition, mainly driven by an increase of Gram-positive bacteria. Drought reduced belowground C allocation, but not the transfer of recently plant-assimilated C to fungi, and in particular reduced tracer uptake by bacteria. This was accompanied by an increase of (13) C in the extractable organic C pool during drought, which was even more pronounced after plots were mown. We conclude that drought weakened the link between plant and bacterial, but not fungal, C turnover, and facilitated the growth of potentially slow-growing, drought-adapted soil microbes, such as Gram-positive bacteria. © 2013 The Authors. New Phytologist © 2013 New Phytologist Trust.

  • NxrB encoding the beta subunit of nitrite oxidoreductase as functional and phylogenetic marker for nitrite-oxidizing Nitrospira

    Pester M, Maixner F, Berry D, Rattei T, Koch H, Lücker S, Nowka B, Richter A, Spieck E, Lebedeva E, Loy A, Wagner M, Daims H
    2014 - Environmental Microbiology, 16: 3055-3071


    Nitrospira are the most widespread and diverse known nitrite-oxidizing bacteria and key nitrifiers in natural and engineered ecosystems. Nevertheless, their ecophysiology and environmental distribution are understudied because of the recalcitrance of Nitrospira to cultivation and the lack of a molecular functional marker, which would allow the detection of Nitrospira in the environment. Here we introduce nxrB, the gene encoding subunit beta of nitrite oxidoreductase, as a functional and phylogenetic marker for Nitrospira. Phylogenetic trees based on nxrB of Nitrospira were largely congruent to 16S ribosomal RNA-based phylogenies. By using new nxrB-selective polymerase chain reaction primers, we obtained almost full-length nxrB sequences from Nitrospira cultures, two activated sludge samples, and several geographically and climatically distinct soils. Amplicon pyrosequencing of nxrB fragments from 16 soils revealed a previously unrecognized diversity of terrestrial Nitrospira with 1801 detected species-level operational taxonomic units (OTUs) (using an inferred species threshold of 95% nxrB identity). Richness estimates ranged from 10 to 946 coexisting Nitrospira species per soil. Comparison with an archaeal amoA dataset obtained from the same soils [Environ. Microbiol. 14: 525-539 (2012)] uncovered that ammonia-oxidizing archaea and Nitrospira communities were highly correlated across the soil samples, possibly indicating shared habitat preferences or specific biological interactions among members of these nitrifier groups. © 2013 The Authors. Environmental Microbiology published by Society for Applied Microbiology and John Wiley & Sons Ltd.

  • Soil warming alters microbial substrate use in alpine soils

    Streit K, Hagedorn F, Hiltbrunner D, Portmann M, Saurer M, Buchmann N, Wild B, Richter A, Wipf S, Siegwolf R
    2014 - Global Change Biology, 20: 1327-1338


    Will warming lead to an increased use of older soil organic carbon (SOC) by microbial communities, thereby inducing C losses from C-rich alpine soils? We studied soil microbial community composition, activity, and substrate use after 3 and 4 years of soil warming (+4 °C, 2007-2010) at the alpine treeline in Switzerland. The warming experiment was nested in a free air CO2 enrichment experiment using depleted (13)CO2 (δ(13)C = -30‰, 2001-2009). We traced this depleted (13)C label in phospholipid fatty acids (PLFA) of the organic layer (0-5 cm soil depth) and in C mineralized from root-free soils to distinguish substrate ages used by soil microorganisms: fixed before 2001 ('old'), from 2001 to 2009 ('new') or in 2010 ('recent'). Warming induced a sustained stimulation of soil respiration (+38%) without decline in mineralizable SOC. PLFA concentrations did not reveal changes in microbial community composition due to soil warming, but soil microbial metabolic activity was stimulated (+66%). Warming decreased the amount of new and recent C in the fungal biomarker 18:2ω6,9 and the amount of new C mineralized from root-free soils, implying a shift in microbial substrate use toward a greater use of old SOC. This shift in substrate use could indicate an imbalance between C inputs and outputs, which could eventually decrease SOC storage in this alpine ecosystem. © 2013 John Wiley & Sons Ltd.

  • Fungal and bacterial utilization of organic substrates depends on substrate complexity and N availability

    Koranda M, Kaiser C, Fuchslueger L, Kitzler B, Sessitsch A, Zechmeister-Boltenstern S, Richter A
    2014 - FEMS Microbiology Ecology, 87: 142-152


    There is growing evidence of a direct relationship between microbial community composition and function, which implies that distinct microbial communities vary in their functional properties. The aim of this study was to determine whether differences in initial substrate utilization between distinct microbial communities are due to the activities of certain microbial groups. We performed a short-term experiment with beech forest soils characterized by three different microbial communities (winter and summer community, and a community from a tree-girdling plot). We incubated these soils with different (13) C-labelled substrates with or without inorganic N addition and analyzed microbial substrate utilization by (13) C-phospholipid fatty acid (PLFA) analysis. Our results revealed that the fate of labile C (glucose) was similar in the three microbial communities, despite differences in absolute substrate incorporation between the summer and winter community. The active microbial community involved in degradation of complex C substrates (cellulose, plant cell walls), however, differed between girdling and control plots and was strongly affected by inorganic N addition. Enhanced N availability strongly increased fungal degradation of cellulose and plant cell walls. Our results indicate that fungi, at least in the presence of a high N supply, are the main decomposers of polymeric C substrates. © 2013 Federation of European Microbiological Societies. Published by John Wiley & Sons Ltd. All rights reserved.

  • Linking microbial community structure and allocation of plant-derived carbon in an organic agricultural soil using (CO2)-C-13 pulse-chase labelling combined with C-13-PLFA profiling

    Tavi NM, Martikainen PJ, Lokko K, Kontro M, Wild B, Richter A, Biasi C
    2013 - Soil Biology and Biochemistry, 58: 207-2015


    We conducted a (CO2)-C-13 pulse-chase labelling experiment in a drained boreal organic (peat) soil cultivated with perennial crop, reed canary grass (RCG; Phalaris arundinacea) to study the flow of carbon from plants to soil microbes. Both limed and unlimed soils were studied, since liming is a common agricultural practice for acidic organic soils. Soil samples taken within three months after the labelling and three times in the following year were used for the delta C-13 analysis of microbial phospholipid fatty acids (PLFAs), root sugars and root lipids. We estimated the contribution of carbon from root exudates to microbial PLFA synthesis. The flow of carbon from plants to microbes was fast as the label allocation in PLFAs had a peak 1-3 days after labelling. The results showed that fungi were important in the incorporation of fresh, plant-derived carbon, including root sugars. None of the main microbial PLFA biomarker groups (fungi, Gram-positive bacteria, Gram-negative bacteria, arbuscular mycorrhizal fungi) was completely lacking label over the measurement period. One year after the labelling, when the labelled carbon was widely distributed into plant biomass and soil, bacterial biomarkers increased their share of the label allocation. Liming had a minor effect on the label allocation rate into PLFAs. The mixing model approach used to calculate the root exudate contribution to microbial biomass resulted in a highly conservative estimate of utilization of this important C-source (0-6.5%, with highest incorporation into fungi). In summary, the results of this study provide new information about the role of various microbial groups in the turnover of plant-derived, fresh carbon in boreal organic soil. (C) 2012 Elsevier Ltd. All rights reserved.

  • Microbial N immobilization is of great importance in acidified mountain spruce forest soils

    Tahovska K, Kana J, Barta J, Oulehle F, Richter A, Santruckova H
    2013 - Soil Biology and Biochemistry, 59: 58-71


    he prevailing N saturation paradigm still considers microbial N immobilization as a less important process of ecosystem N retention. On the contrary, we hypothesize that it can even be a primary process affecting N leaching from N saturated soils. We studied N transformations in soils of acidified near-natural and primeval forests in the Bohemian Forest (watersheds of Plegne and Certovo Lakes, Czech Republic) and Pop Ivan Massif (Ukraine). Organic soils were sampled from similar conditions (1100-1500 m a.s.I., precipitation 1400-1800 mm, acidic bedrock, forest dominated by Picea abies) and had similar chemical properties (pH(KCI) 2.5-3.2, BS similar to 45%, Al-ex similar to 40 meq kg(-1)). However, the Ukrainian soil had lower soil C/N ratio (24 vs. 30) and C availability (water soluble C and C/N ratio of 65 vs. similar to 114-163 mu mol g(-1) and 6 vs. 21-24, respectively) than the other soils. We ran laboratory experiments in which mixtures of different N sources (N-NH4, N-NO3 and glycine) were added to the soil with only one source N-15-labelled. We followed N-15 partitioning within soil N pools and analysed the composition of the microbial community (16SrDNA-DGGE fingerprint of bacteria, ergosterol analyses, qPCR of fungal 18S rDNA gene). The microbial N pool was always three to five times higher than the total soluble N pool. We found rapid (15 min) and simultaneous immobilization of all added N forms into the microbial biomass with clear preferences for organic N over inorganic sources. The total N flux to the microbial pool always exceeded N flux into mineral N pools. The pattern of N transformation in the C limited soil was different from the other soils. The microbial pool and N flux into it were smaller compared to the mineral N pools and fluxes. The contribution of N-NO3 to microbial immobilization was negligible, while nitrification was almost equal to N mineralization. Total N flux through soluble N pools was greater than total N flux to insoluble pools (residual and microbial N); this was accompanied by lower microbial N uptake efficiency and shorter residence time of N in microbial pool than in soils with higher C availability. The composition of bacterial community was related to DOC content and C and N in microbial biomass. In soils with higher fungal abundance, more glycine was immobilized regardless of soil C availability, but with higher deamination (similar to 50 vs. 20%) and subsequent release of N-NH4 back to the soil. Our study emphasized the role of microbial N immobilization in preventing N-NO3 loss from N saturated ecosystems as a function of C availability. Nitrification was favoured when enough N-NH4 was available in the C limited soil. The discharged N-NO3 was not immobilized by the microbes and could be, if not immobilized by plants, leached out. C limitation plays an important role in the susceptibility of ecosystems to N leaching and could partially explain the observed differences in some Nsaturated ecosystems. (C) 2013 Elsevier Ltd. All rights reserved.

  • Nitrogen dynamics in Turbic Cryosols from Siberia and Greenland.

    Wild B, Schnecker J, Barta J, Capek P, Guggenberger G, Hofhansl F, Kaiser C, Lashchinsky N, Mikutta R, Mooshammer M, Santruckova H, Shibistova O, Urich T, Zimov SA, Richter A
    2013 - Soil Biology and Biochemistry, 67: 85-93


    Turbic Cryosols (permafrost soils characterized by cryoturbation, i.e., by mixing of soil layers due to freezing and thawing) are widespread across the Arctic, and contain large amounts of poorly decomposed organic material buried in the subsoil. This cryoturbated organic matter exhibits retarded decomposition compared to organic material in the topsoil. Since soil organic matter (SOM) decomposition is known to be tightly linked to N availability, we investigated N transformation rates in different soil horizons of three tundra sites in north-eastern Siberia and Greenland. We measured gross rates of protein depolymerization, N mineralization (ammonification) and nitrification, as well as microbial uptake of amino acids and NH4 + using an array of 15N pool dilution approaches. We found that all sites and horizons were characterized by low N availability, as indicated by low N mineralization compared to protein depolymerization rates (with gross N mineralization accounting on average for 14% of gross protein depolymerization). The proportion of organic N mineralized was significantly higher at the Greenland than at the Siberian sites, suggesting differences in N limitation. The proportion of organic N mineralized, however, did not differ significantly between soil horizons, pointing to a similar N demand of the microbial community of each horizon. In contrast, absolute N transformation rates were significantly lower in cryoturbated than in organic horizons, with cryoturbated horizons reaching not more than 32% of the transformation rates in organic horizons. Our results thus indicate a deceleration of the entire N cycle in cryoturbated soil horizons, especially strongly reduced rates of protein depolymerization (16% of organic horizons) which is considered the rate-limiting step in soil N cycling.

  • Metabolic features of Protochlamydia amoebophila elementary bodies--a link between activity and infectivity in Chlamydiae

    Sixt BS, Siegl A, Mueller C, Watzka M, Wultsch A, Tziotis D, Montanaro J, Richter A, Schmitt-Kopplin P, Horn M
    2013 - PLoS Pathogens, 9: in press


    The Chlamydiae are a highly successful group of obligate intracellular bacteria, whose members are remarkably diverse, ranging from major pathogens of humans and animals to symbionts of ubiquitous protozoa. While their infective developmental stage, the elementary body (EB), has long been accepted to be completely metabolically inert, it has recently been shown to sustain some activities, including uptake of amino acids and protein biosynthesis. In the current study, we performed an in-depth characterization of the metabolic capabilities of EBs of the amoeba symbiont Protochlamydia amoebophila. A combined metabolomics approach, including fluorescence microscopy-based assays, isotope-ratio mass spectrometry (IRMS), ion cyclotron resonance Fourier transform mass spectrometry (ICR/FT-MS), and ultra-performance liquid chromatography mass spectrometry (UPLC-MS) was conducted, with a particular focus on the central carbon metabolism. In addition, the effect of nutrient deprivation on chlamydial infectivity was analyzed. Our investigations revealed that host-free P. amoebophila EBs maintain respiratory activity and metabolize D-glucose, including substrate uptake as well as host-free synthesis of labeled metabolites and release of labeled CO2 from 13C-labeled D-glucose. The pentose phosphate pathway was identified as major route of D-glucose catabolism and host-independent activity of the tricarboxylic acid (TCA) cycle was observed. Our data strongly suggest anabolic reactions in P. amoebophila EBs and demonstrate that under the applied conditions D-glucose availability is essential to sustain metabolic activity. Replacement of this substrate by L-glucose, a non-metabolizable sugar, led to a rapid decline in the number of infectious particles. Likewise, infectivity of Chlamydia trachomatis, a major human pathogen, also declined more rapidly in the absence of nutrients. Collectively, these findings demonstrate that D-glucose is utilized by P. amoebophila EBs and provide evidence that metabolic activity in the extracellular stage of chlamydiae is of major biological relevance as it is a critical factor affecting maintenance of infectivity.

  • Seasonal variation in functional properties of microbial communities in beech forest soil

    Koranda M, Kaiser C, Fuchslueger L, Kitzler B, Sessitsch A, Zechmeister-Boltenstern S, Richter A
    2013 - Soil Biology and Biochemistry, 60: 95-104


    Substrate quality and the availability of nutrients are major factors controlling microbial decomposition processes in soils. Seasonal alteration in resource availability, which is driven by plants via belowground C allocation, nutrient uptake and litter fall, also exerts effects on soil microbial community composition. Here we investigate if seasonal and experimentally induced changes in microbial community composition lead to alterations in functional properties of microbial communities and thus microbial processes. Beech forest soils characterized by three distinct microbial communities (winter and summer community, and summer community from a tree girdling plot, in which belowground carbon allocation was interrupted) were incubated with different 13C-labeled substrates with or without inorganic N supply and analyzed for substrate use and various microbial processes. Our results clearly demonstrate that the three investigated microbial communities differed in their functional response to addition of various substrates. The winter communities revealed a higher capacity for degradation of complex C substrates (cellulose, plant cell walls) than the summer communities, indicated by enhanced cellulase activities and reduced mineralization of soil organic matter. In contrast, utilization of labile C sources (glucose) was lower in winter than in summer, demonstrating that summer and winter community were adapted to the availability of different substrates. The saprotrophic community established in girdled plots exhibited a significantly higher utilization of complex C substrates than the more plant root associated community in control plots if additional nitrogen was provided. In this study we were able to demonstrate experimentally that variation in resource availability as well as seasonality in temperate forest soils cause a seasonal variation in functional properties of soil microorganisms, which is due to shifts in community structure and physiological adaptations of microbial communities to altered resource supply.

  • Carbon use efficiency of microbial communities: stoichiometry, methodology and modelling

    Sinsabaugh RL, Manzoni S, Moorhead DL, Richter A
    2013 - Ecology Letters, 16: 930-939


    Carbon use efficiency (CUE) is a fundamental parameter for ecological models based on the physiology of microorganisms. CUE determines energy and material flows to higher trophic levels, conversion of plant-produced carbon into microbial products and rates of ecosystem carbon storage. Thermodynamic calculations support a maximum CUE value of ~ 0.60 (CUE max). Kinetic and stoichiometric constraints on microbial growth suggest that CUE in multi-resource limited natural systems should approach ~ 0.3 (CUE max /2). However, the mean CUE values reported for aquatic and terrestrial ecosystems differ by twofold (~ 0.26 vs. ~ 0.55) because the methods used to estimate CUE in aquatic and terrestrial systems generally differ and soil estimates are less likely to capture the full maintenance costs of community metabolism given the difficulty of measurements in water-limited environments. Moreover, many simulation models lack adequate representation of energy spilling pathways and stoichiometric constraints on metabolism, which can also lead to overestimates of CUE. We recommend that broad-scale models use a CUE value of 0.30, unless there is evidence for lower values as a result of pervasive nutrient limitations. Ecosystem models operating at finer scales should consider resource composition, stoichiometric constraints and biomass composition, as well as environmental drivers, to predict the CUE of microbial communities. © 2013 John Wiley & Sons Ltd/CNRS.

  • Host-compound foraging by intestinal microbiota revealed by single-cell stable isotope probing

    Berry D, Stecher B, Schintlmeister A, Reichert J, Brugiroux S, Wild B, Wanek W, Richter A, Rauch I, Decker T, Loy A, Wagner M
    2013 - Proceedings of the National Academy of Sciences of the United States of America (PNAS), 110: 4720-4725


    The animal and human intestinal mucosa secretes an assortment of compounds to establish a physical barrier between the host tissue and intestinal contents, a separation that is vital for health. Some pathogenic microorganisms as well as members of the commensal intestinal microbiota have been shown to be able to break down these secreted compounds. Our understanding of host-compound degradation by the commensal microbiota has been limited to knowledge about simplified model systems because of the difficulty in studying the complex intestinal ecosystem in vivo. In this study, we introduce an approach that overcomes previous technical limitations and allows us to observe which microbial cells in the intestine use host-derived compounds. We added stable isotope-labeled threonine i.v. to mice and combined fluorescence in situ hybridization with high-resolution secondary ion mass spectrometry imaging to characterize utilization of host proteins by individual bacterial cells. We show that two bacterial species, Bacteroides acidifaciens and Akkermansia muciniphila, are important host-protein foragers in vivo. Using gnotobiotic mice we show that microbiota composition determines the magnitude and pattern of foraging by these organisms, demonstrating that a complex microbiota is necessary in order for this niche to be fully exploited. These results underscore the importance of in vivo studies of intestinal microbiota, and the approach presented in this study will be a powerful tool to address many other key questions in animal and human microbiome research.

  • Nitrification rates in Arctic soils are associated with functionally distinct populations of ammonia-­‐oxidizing archaea

    Alves, RJE, Wanek W, Zappe A, Richter A, Svenning MM, Schleper C, Urich T
    2013 - The ISME Journal: multidisciplinary journal of microbial ecology, 7: 1620-1631


    The functioning of Arctic soil ecosystems is crucially important for global climate, and basic knowledge regarding their biogeochemical processes is lacking. Nitrogen (N) is the major limiting nutrient in these environments, and its availability is strongly dependent on nitrification. However, microbial communities driving this process remain largely uncharacterized in Arctic soils, namely those catalyzing the rate-limiting step of ammonia (NH3) oxidation. Eleven Arctic soils were analyzed through a polyphasic approach, integrating determination of gross nitrification rates, qualitative and quantitative marker gene analyses of ammonia-oxidizing archaea (AOA) and bacteria (AOB) and enrichment of AOA in laboratory cultures. AOA were the only NH3 oxidizers detected in five out of 11 soils and outnumbered AOB in four of the remaining six soils. The AOA identified showed great phylogenetic diversity and a multifactorial association with the soil properties, reflecting an overall distribution associated with tundra type and with several physico-chemical parameters combined. Remarkably, the different gross nitrification rates between soils were associated with five distinct AOA clades, representing the great majority of known AOA diversity in soils, which suggests differences in their nitrifying potential. This was supported by selective enrichment of two of these clades in cultures with different NH3 oxidation rates. In addition, the enrichments provided the first direct evidence for NH3 oxidation by an AOA from an uncharacterized Thaumarchaeota-AOA lineage. Our results indicate that AOA are functionally heterogeneous and that the selection of distinct AOA populations by the environment can be a determinant for nitrification activity and N availability in soils.

  • Responses of belowground carbon allocation dynamics to extended shading in mountain grassland

    Bahn M, Lattanzi FA, Hasibeder R, Wild B, Koranda M, Danese V, Brüggemann N, Schmitt M, Siegwolf R, Richter A
    2013 - New Phytologist, 198: 116-126


    Carbon (C) allocation strongly influences plant and soil processes. Short-term C allocation dynamics in ecosystems and their responses to environmental changes are still poorly understood. Using in situ (13) CO(2) pulse labeling, we studied the effects of 1 wk of shading on the transfer of recent photoassimilates between sugars and starch of above- and belowground plant organs and to soil microbial communities of a mountain meadow. C allocation to roots and microbial communities was rapid. Shading strongly reduced sucrose and starch concentrations in shoots, but not roots, and affected tracer dynamics in sucrose and starch of shoots, but not roots: recent C was slowly incorporated into root starch irrespective of the shading treatment. Shading reduced leaf respiration more strongly than root respiration. It caused no reduction in the amount of (13) C incorporated into fungi and Gram-negative bacteria, but increased its residence time. These findings suggest that, under interrupted C supply, belowground C allocation (as reflected by the amount of tracer allocated to root starch, soil microbial communities and belowground respiration) was maintained at the expense of aboveground C status, and that C source strength may affect the turnover of recent plant-derived C in soil microbial communities. © 2013 The Authors. New Phytologist © 2013 New Phytologist Trust.

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