Publications

Publications in peer reviewed journals

33 Publications found
  • Soil CH4 and N2O response diminishes during decadal soil warming in a temperate mountain forest

    Heinzle J, Kitzler B, Zechmeister-Boltenstern S, Tian Y, Kengdo SW, Wanek W, Borken W, Schindlbacher A
    2023 - Agricultural and Forest Meteorology, 329: Article 109287

    Abstract: 

    Global warming is considered to impact the fluxes of methane (CH4) and nitrous oxide (N2O) between forest soils and the atmosphere, but it is unclear whether the responses change over time. In this study the response of soil CH4 and N2O fluxes to field soil warming (+4 °C) were determined during years 2–5 and 14–16 in a soil warming experiment in a temperate forest. In the second and sixteenth year of soil warming, temperature sensitivities of CH4 and N2O fluxes were assessed in-situ by gradually rising field soil temperatures to ∼10 °C above ambient within a short period of three to four days. Production of dinitrogen (N2) was measured ex-situ in the sixteenth year of warming. Soil warming significantly reduced CH4 uptake (-19.5%) and increased N2O emissions (+41.6%) during the first years of warming, whereas no warming effects on soil CH4 and N2O fluxes were observed during the later years. Dinitrogen production was up to ten times higher than N2O production, though the high spatiotemporal variability masked any significant effects of soil warming on soil N2 fluxes. Temperature sensitivities (Q10) for CH4 uptake and N2O emissions were 2.07 and 4.06, respectively, in the second year of warming and 1.52 and 1.79, respectively, in the sixteenth year of soil warming. The diminishing warming response of the soil N2O fluxes likely were caused by longer-term changes in soil N availability and/or simultaneous acclimation of the soil microbial community to soil warming. Soil moisture was largely unaffected by soil warming, and soil temperature alone was only a weak predictor of soil CH4 fluxes. Methane fluxes therefore can be expected to be generally less affected than N2O fluxes. Overall, our results suggest that soil warming has only limited and transient effects on soil CH4 and N2O fluxes in this type of temperate forest.

  • Climate change impacts on soil biology

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

    Abstract: 

    Abstract

    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.

  • Water availability is a stronger driver of soil microbial processing of organic nitrogen than tree species composition

    Maxwell TL, Augusto L, Tian Y, Wanek W, Fanin N
    2023 - European Journal of Soil Science, 74: Article e13350

    Abstract: 

    Soil organic nitrogen (N) cycling processes constitute a bottleneck of soil N cycling, yet little is known about how tree species composition may influence these rates, and even less under changes in soil water availability such as those that are being induced by climate change. In this study, we used a 12-year-old tree biodiversity experiment in southwestern France to assess the interactive effects of soil water availability (half of the blocks seasonally irrigated to double precipitation) and tree species composition (monocultural vs. mixed plots of coniferous Pinus pinaster, and of broadleaf Betula pendula). We measured gross protein depolymerisation rates using a novel high-throughput isotope pool dilution method, along with soil microbial biomass carbon and N to calculate microbial biomass-specific activities of soil organic N processes. Overall, high soil water availability led to a 42% increase in soil protein depolymerisation rates compared to the unirrigated plots, but we found no effect of species composition on these soil organic N cycling processes. When investigating the interactive effect of tree species mixing and soil water availability, the results suggest that mixing tree species had a negative effect on soil organic N cycling processes in the non-irrigated blocks subject to dry summers, but that this effect tended to become positive at higher soil water availability in irrigated plots. These results put forth that soil water availability could influence potential tree species mixing effects on soil organic N cycling processes in dry conditions.

  • 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

    Abstract: 

    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

    Abstract: 

    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.

  • Phosphorus limitation reduces microbial nitrogen use efficiency by increasing extracellular enzyme investments

    Sun L, Li J, Qu L, Wang X, Sang C, Wang J, Sun M, Wanek W, Moorhead DL, Bai E, Wang C
    2023 - Geoderma, 432: Article 116416

    Abstract: 

    Microbial nitrogen use efficiency (NUE), which reflects the proportion of nitrogen (N) taken up to be allocated to microbial biomass and growth, is central to our understanding of soil N cycling. However, the factors influencing microbial NUE remain unclear. Here, we explored the effects of climate factors, soil properties, and microbial variables on microbial NUE based on a survey of soils from 11 locations along a forest transect in eastern China. We found microbial NUE decreased with the ratio of acid phosphatase (AP) activity versus microbial growth rate. This suggested that increased microbial phosphorus acquisition decreased microbial NUE due to increasing investment in AP. However, microbial NUE increased with soil organic carbon content, because soil organic carbon is the source of material and energy for microbial growth and metabolism. Soil pH and mean annual temperature indirectly affected microbial NUE through their effects on the ratio of AP activity relative to microbial growth rate and soil organic carbon content, respectively. Our results improve our understanding and prediction of microbial NUE on a large spatial scale and emphasize the importance of phosphorus in affecting microbial metabolic efficiency.

  • 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

    Abstract: 

    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.

  • Modeling the carbon costs of plant phosphorus acquisition in Amazonian forests

    Reichert T, Rammig A, Papastefanou P, Lugli LF, Filho JPD, Gregor K, Fuchslueger L, Quesada CA, Fleischer K
    2023 - Ecological Modelling, 485: Article 110491

    Abstract: 

    Plants growing in low phosphorus (P) soils, such as in the predominant soils of Amazonia, are believed to devote more energy to acquiring P through absorptive root production, symbionts, and root exudates than plants in more fertile soils. Accounting for these energy costs in vegetation models is essential, as underestimating carbon (C) allocation to nutrient acquisition may lead to overestimating plant biomass growth. We developed a quantitative model to test a theoretical framework of C costs of P acquisition across soil P gradients. The model considers four strategies: P foraging via absorptive roots and arbuscular mycorrhizal fungi and P mining via root exudation of phosphatases and organic acids. We used field observations (i.e., soil data, plant biomass production, and stoichiometry of different organs) from ten sites across Amazonia to calibrate the model and explore different scenarios of (i) experimental soil P addition and (ii) elevated atmospheric 

    CO2 concentrations (

    eCO2). Our model reproduced expected trends in P-acquisition strategies, with plants increasingly investing in foraging strategies as soil soluble inorganic P (Pi) increases and increasingly investing in mining strategies as total P and less available P forms decrease. Relative investment in P acquisition was within observed ranges. Plants, on average and across all sites, invested the equivalent of 20.5% of their estimated total net primary production (NPP) in P acquisition. On average, plants allocated 15.3% of their NPP to P acquisition in the three most fertile sites, compared to 29.0% in the least fertile sites. C allocation to arbuscular mycorrhizas, phosphatases, and organic acids, which are not commonly measured components of total NPP, was up to 25.8% (16.9% on average) of the total NPP. We highlight the need for quantitative data on plant C allocation to P acquisition from the soil to strengthen further model development and future model projections.

  • Revisiting process-based simulations of soil nitrite dynamics: Tighter cycling between nitrite and nitrate than considered previously

    Zheng J, Fujii K, Koba K, Wanek W, Müller C, Jansen-Willems AB, Nakajima Y, Wagai R, Canarini A
    2023 - Soil Biology and Biochemistry, 178: Article 108958

    Abstract: 

    Nitrite is an important precursor of many environmentally hazardous compounds (e.g., nitrate, nitrous oxide, and nitrous acid). However, its dynamics in the soil environment are not yet fully understood. The NtraceNitrite tool has been successful in analyzing 15N tracing data. Here, based on a 15N tracing experiment (under aerobic condition) where either the nitrite, the nitrate, or the ammonium pool was labelled, we developed an extended model (NO2Trace), which was featured by the addition of coupled nitrate reduction and nitrite re-oxidation and the separation of the nitrate pool in two sub-pools. With 5 additional parameters optimized, NO2Trace was able to achieve a superior fit to the data, as compared to the NtraceNitrite tool. The additional features might offer a suitable explanation for the isotopic composition of nitrate produced via nitrification in terrestrial ecosystems. Our results carry two important implications: (i) a key assumption of the classical isotope pool dilution technique (i.e., no reflux of tracer) for estimating gross nitrate fluxes is violated, leading to considerable underestimations (22–99% in the datasets tested); (ii) re-oxidation can dominate the consumption (∼75%) of nitrite derived from nitrate reduction, indicating the potential of this process as a target for nitrogen retention mechanism against gaseous nitrogen losses (through nitrite reduction). The additional features of the extended model show a tighter cycle between soil nitrite and nitrate than considered previously and provide a more comprehensive description of soil nitrite transformations. This study also highlights that more work is needed to develop methods capable of separating process- and pathways-specific nitrate and nitrite pools.

  • 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

    Abstract: 

    Purpose

    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.

    Methods

    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).

    Results

    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.

    Conclusion

    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.

  • A rapid and sensitive assay to quantify amino sugars, neutral sugars and uronic acid necromass biomarkers using pre-column derivatization, ultra-high-performance liquid chromatography and high-resolution mass spectrometry

    Salas E, Gorfer M, Bandian D, Wang B, Kaiser C, Wanek W
    2023 - Soil Biology and Biochemistry, 177: Article 108927

    Abstract: 

    Microbial necromass comprises a large fraction of soil organic matter (SOM) due to the accumulation and stabilization of microbial residues from dead archaea, bacteria and fungi. Amino sugars, neutral sugars and uronic acids have been used as microbial necromass biomarkers to trace the origin and composition of microbial residues in the SOM pool. Due to the structural complexity of sugars, derivatization reactions and high-throughput analytical methods are required to separate and quantify these sugar-related compounds. Our aim was to develop a rapid and sensitive assay to measure amino sugar, neutral sugar and uronic acid compounds using pre-column 1-phenyl-3-methyl-5-pyrazolone (PMP) derivatization. PMP-derivatives were separated and quantified via reversed phase (RP) ultra-high-performance liquid chromatography (UPLC) coupled to high-resolution Orbitrap mass spectrometry (MS). The method was validated and applied on hydrolyzed peptidoglycans and the biomass of archaeal, bacterial, fungal and plant species, as well as with soils. This developed PMP method allowed the separation and quantification of 18 sugar-related compounds, including four amino sugars, three N-acetyl amino sugars, eight neutral sugars, and three uronic acids within 20 min. This PMP method showed a precision for isotope enrichment detection of 0.03–0.05 atom % 13C for D-glucose and D-glucosamine. This is the first time talosaminuronic acid (deriving from archaeal pseudopeptidoglycan) was identified and quantified using PMP derivatization. The application of this novel PMP method on pure hydrolyzed biomass and soils, showed the successful chromatographic and mass spectrometric separation and quantification of amino sugar, neutral sugar and uronic acid compounds. A multivariate analysis using these sugar-related PMP derivatives showed a clustering of the species according to their respective taxonomic group (archaea, gram-positive bacteria, gram-negative bacteria, fungi and plants). The modified PMP method can be applied to identify and quantify soil microbial necromass biomarkers, as well as their contribution to SOM. The sensitive isotope tracer detection allows tracing isotopically labeled materials into necromass biomarkers in SOM pools.

  • 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

    Abstract: 

    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.

  • 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

    Abstract: 

    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.

  • 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

    Abstract: 

    Abstract

    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.

  • Loss of nitrogen fixing capacity in a montane lichen is linked to increased nitrogen deposition

    Crittenden PD, Ellis CJ, Smith RI, Wanek W, Thornton B
    2023 - Journal of Ecology, 111: 288-299

    Abstract: 

    1. The circumboreal/circumpolar N2-fixing lichen Stereocaulon vesuvianum is among the most widespread and abundant fruticose species in montane Britain but has lost the capacity to fix N2 over large areas of the country.
    2. To investigate whether loss of N2-fixation in S. vesuvianum is linked to increased N deposition, we examined thallus morphology, physiology and chemistry at twelve locations representing an N deposition gradient of 3–40 kg ha−1 year−1. Measurements were made in parallel on a non-N2-fixing reference species (Parmelia saxatilis). The presence or absence of cephalodia (N2-fixing nodules containing the cyanobacterium Stigonema sp) was recorded in over 500 herbarium specimens of S. vesuvianum dating back to 1820.
    3. Cephalodium abundance in S. vesuvianum, and 15N concentration in S. vesuvianum and P. saxatilis, were strongly negatively correlated with N deposition and particularly with dry deposited N; cephalodia do not form at total N deposition rates ≥8–9 kg ha−1 year−1. Other morphological oddities in S. vesuvianum at N-polluted sites include increased apothecium (fungal reproductive structure) production and green algal biofilm development. Biofilm covered thalli without cephalodia lacked nitrogenase activity and cephalodia at sites where they rarely develop had nitrogenase activities typical for this species. The presence or absence of cephalodia in herbarium specimens of S. vesuvianum suggest that the present-day N-deposition linked gradient in N2-fixing capacity did not exist in the 19th century and largely developed between 1900–1940.
    4. Synthesis. We provide clear evidence that N2-fixing capacity in S. vesuvianum has been lost in regions subjected to many decades of enhanced atmospheric N deposition. This loss is consistent with established models of diazotrophy, which identify supply of combined N as an inhibitor of N2-fixation. Progressive depletion of thallus 15N with increasing N deposition is in line with available data indicating that much atmospheric N pollution is 15N-depleted. Rates of nitrogenase activity in S. vesuvianum are low compared to other symbiotic systems and perhaps more likely supplanted by elevated N deposition. We suggest that other ecosystem compartments with low rates of fixation (e.g. soils) might also be susceptible to N pollution and merit investigation.
    • The circumboreal/circumpolar N2-fixing lichen Stereocaulon vesuvianum is among the most widespread and abundant fruticose species in montane Britain but has lost the capacity to fix N2 over large areas of the country.
    • To investigate whether loss of N2-fixation in S. vesuvianum is linked to increased N deposition, we examined thallus morphology, physiology and chemistry at twelve locations representing an N deposition gradient of 3–40 kg ha−1 year−1. Measurements were made in parallel on a non-N2-fixing reference species (Parmelia saxatilis). The presence or absence of cephalodia (N2-fixing nodules containing the cyanobacterium Stigonema sp) was recorded in over 500 herbarium specimens of S. vesuvianum dating back to 1820.
    • Cephalodium abundance in S. vesuvianum, and 15N concentration in S. vesuvianum and P. saxatilis, were strongly negatively correlated with N deposition and particularly with dry deposited N; cephalodia do not form at total N deposition rates ≥8–9 kg ha−1 year−1. Other morphological oddities in S. vesuvianum at N-polluted sites include increased apothecium (fungal reproductive structure) production and green algal biofilm development. Biofilm covered thalli without cephalodia lacked nitrogenase activity and cephalodia at sites where they rarely develop had nitrogenase activities typical for this species. The presence or absence of cephalodia in herbarium specimens of S. vesuvianum suggest that the present-day N-deposition linked gradient in N2-fixing capacity did not exist in the 19th century and largely developed between 1900–1940.
    • Synthesis. We provide clear evidence that N2-fixing capacity in S. vesuvianum has been lost in regions subjected to many decades of enhanced atmospheric N deposition. This loss is consistent with established models of diazotrophy, which identify supply of combined N as an inhibitor of N2-fixation. Progressive depletion of thallus 15N with increasing N deposition is in line with available data indicating that much atmospheric N pollution is 15N-depleted. Rates of nitrogenase activity in S. vesuvianum are low compared to other symbiotic systems and perhaps more likely supplanted by elevated N deposition. We suggest that other ecosystem compartments with low rates of fixation (e.g. soils) might also be susceptible to N pollution and merit investigation.
  • Tracing 33P-labelled organic phosphorus compounds in two soils: New insights into decomposition dynamics and direct use by microbes

    Wasner D, Prommer J, Zezula D, Mooshammer M, Hu Y, Wanek W
    2023 - Frontiers in Soil Science, 3: Article 1097965

    Abstract: 

    Introduction: Organic phosphorus (Po) compounds constitute an important pool in soil P cycling, but their decomposition dynamics are poorly understood. Further, it has never been directly tested whether low molecular weight Po compounds are taken up by soil microbes in an intact form, which reduces the dependence of their P acquisition on extracellular phosphatases.

    Methods: We investigated the short-term fate (24 h) of five 33P-labelled Po compounds (teichoic acids, phospholipids, DNA, RNA and soluble organophosphates) and 33P-labelled inorganic P (Pi) in two soils.

    Results: We found indications that soil microbial breakdown of phosphodiesters was limited by the depolymerization step, and that direct microbial uptake of Po occurred to a substantial extent.

    Discussion: We postulate a trade-off between direct Po uptake and complete extracellular Po mineralization. These findings have profound consequences for our understanding of microbial P cycling in soils.

  • One-time freeze-thawing or carbon input events have long-term legacies in soil microbial communities

    Gorka S, Ranits C, zhang S, Imai B, Guseva K, Kaiser C
    2023 - Geoderma, 432: Article 116399

    Abstract: 

    Soil microbial communities are regularly exposed to sudden changes in environmental conditions, such as root exudation pulses or freeze-thaw events. As microbial communities have a high potential to adapt to changing conditions, they are expected to be resilient towards this kind of short-term perturbations and return to their pre-perturbed state quickly. Here, we conducted a lab incubation experiment to evaluate the resilience of soil microbial communities to single-pulse perturbations.

    We incubated temperate forest soil at constant temperature (20 °C) and water content, and exposed it to strong single-pulse perturbations, which nonetheless mimic common pulse-events in temperate soils (glucose addition at 4 mg g−1 soil, or freeze-thawing overnight at −20 °C). We subsequently measured microbial community composition and microbial storage compounds via phospho- and neutral lipid fatty acid (PLFA and NLFA) profiling, as well as C/N stoichiometry of microbial biomass and dissolved organic carbon and nitrogen in the soil solution shortly after (0.4, 1, 4, and 6 days) and after longer time periods (84 and 160 days) following the perturbations.

    Transferring the soils from their natural environment to the laboratory and incubating them under controlled conditions led to a continuous change of microbial community structure over time, along with an increase in microbial biomass and dissolved N in both perturbed and control soils over the time of the experiment. Against the background of this ‘press-disturbance’, caused by the permanently changed conditions, we see immediate and long-lasting effects of the single pulse events on microbial community composition, C storage and C/N stoichiometry. Both perturbations significantly influenced the microbial community structure (based on PLFA profiles), microbial biomass N and dissolved N up to 160 days, as well as fungal and bacterial biomass and storage (based on absolute PLFA and NLFA concentrations) up to 84 days. Both perturbations increased microbial N (+59.6 µg g−1 dw) and decreased dissolved N (−40.3 µg g−1 dw) after 160 days, and significantly altered C/N ratios in microbial and dissolved pools (particularly in the first 6 days of the experiment).

    Our results demonstrate that single-pulse perturbations can have long-term legacies in soil microbial ecosystems. In our experiment they led to alternative system states which differed from the unperturbed control in multiple parameters even after 160 days. This indicates that soil microbial communities exhibit a low resistance and resilience towards single-pulse perturbations, and may easily be pushed on alternative trajectories by short but strong environmental pulses.

     
  • Seasonal fluctuations of extracellular enzyme activities are related to the biogeochemical cycling of C, N and P in a tropical terra-firme forest

    Schaap KJ, Fuchslueger L, Quesada CA, Hofhansl F, Valverde-Barrantes O, Camargo PB, Hoosbeek MR
    2023 - Biogeochemistry, 163: 1-15

    Abstract: 

    Extracellular enzymes (EE) play a vital role in soil nutrient cycling and thus affect terrestrial ecosystem functioning. Yet the drivers that regulate microbial activity, and therefore EE activity, remain under debate. In this study we investigate the temporal variation of soil EE in a tropical terra-firme forest. We found that EE activity peaked during the drier season in association with increased leaf litterfall, which was also reflected in negative relationships between EE activities and precipitation. Soil nutrients were weakly related to EE activities, although extractable N was related to EE activities in the top 5 cm of the soil. These results suggest that soil EE activity is synchronized with precipitation-driven substrate inputs and depends on the availability of N. Our results further indicate high investments in P acquisition, with a higher microbial N demand in the month before the onset of the drier season, shifting to higher P demand towards the end of the drier season. These seasonal fluctuations in the potential acquisition of essential resources imply dynamic shifts in microbial activity in coordination with climate seasonality and resource limitation of central-eastern Amazon forests.

  • 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

    Abstract: 

    • 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.
  • Close coupling of plant functional types with soil microbial community composition drives soil carbon and nutrient cycling in tundra heath

    Koranda M, Rinnan R, Michelsen A
    2023 - Plant and soil, 488: 551-572

    Abstract: 

    Aims

    This study aimed at elucidating divergent effects of two dominant plant functional types (PFTs) in tundra heath, dwarf shrubs and mosses, on soil microbial processes and soil carbon (C) and nutrient availability, and thereby to enhance our understanding of the complex interactions between PFTs, soil microbes and soil functioning.

    Methods

    Samples of organic soil were collected under three dwarf shrub species (of distinct mycorrhizal association and life form) and three moss species in early and late growing season. We analysed soil C and nutrient pools, extracellular enzyme activities and phospholipid fatty acid profiles, together with a range of plant traits, soil and abiotic site characteristics.

    Results

    Shrub soils were characterised by high microbial biomass C and phosphorus and phosphatase activity, which was linked with a fungal-dominated microbial community, while moss soils were characterised by high soil nitrogen availability, peptidase and peroxidase activity associated with a bacterial-dominated microbial community. The variation in soil microbial community structure was explained by mycorrhizal association, root morphology, litter and soil organic matter quality and soil pH-value. Furthermore, we found that the seasonal variation in microbial biomass and enzyme activities over the growing season, likely driven by plant belowground C allocation, was most pronounced under the tallest shrub Betula nana.

    Conclusion

    Our study demonstrates a close coupling of PFTs with soil microbial communities, microbial decomposition processes and soil nutrient availability in tundra heath, which suggests potential strong impacts of global change-induced shifts in plant community composition on carbon and nutrient cycling in high-latitude ecosystems.

  • 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

    Abstract: 

    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.

  • Individual and interactive effects of warming and nitrogen supply on CO2 fluxes and carbon allocation in subarctic grassland

    Meeran K, Verbrigge N, Ingrisch J, Fuchslueger L, Müller L, Sigurðsson P, Sigurdsson BD, Wachter H, Watzka M, Soong JL, Vicca S, Janssens IA, Bahn M
    2023 - Global Change Biology, 29: 5276-5291

    Abstract: 

    Climate warming has been suggested to impact high latitude grasslands severely, potentially causing considerable carbon (C) losses from soil. Warming can also stimulate nitrogen (N) turnover, but it is largely unclear whether and how altered N availability impacts belowground C dynamics. Even less is known about the individual and interactive effects of warming and N availability on the fate of recently photosynthesized C in soil. On a 10-year geothermal warming gradient in Iceland, we studied the effects of soil warming and N addition on CO2 fluxes and the fate of recently photosynthesized C through CO2 flux measurements and a 13CO2 pulse-labeling experiment. Under warming, ecosystem respiration exceeded maximum gross primary productivity, causing increased net CO2 emissions. N addition treatments revealed that, surprisingly, the plants in the warmed soil were N limited, which constrained primary productivity and decreased recently assimilated C in shoots and roots. In soil, microbes were increasingly C limited under warming and increased microbial uptake of recent C. Soil respiration was increased by warming and was fueled by increased belowground inputs and turnover of recently photosynthesized C. Our findings suggest that a decade of warming seemed to have induced a N limitation in plants and a C limitation by soil microbes. This caused a decrease in net ecosystem CO2 uptake and accelerated the respiratory release of photosynthesized C, which decreased the C sequestration potential of the grassland. Our study highlights the importance of belowground C allocation and C-N interactions in the C dynamics of subarctic ecosystems in a warmer world.

  • RGS4 impacts carbohydrate and siderophore metabolism in Trichoderma reesei

    Schalamun M, Molin EM, Schmoll M
    2023 - BMC Genomics, 24: Article 372

    Abstract: 

    Background

    Adaptation to complex, rapidly changing environments is crucial for evolutionary success of fungi. The heterotrimeric G-protein pathway belongs to the most important signaling cascades applied for this task. In Trichoderma reesei, enzyme production, growth and secondary metabolism are among the physiological traits influenced by the G-protein pathway in a light dependent manner.

    Results

    Here, we investigated the function of the SNX/H-type regulator of G-protein signaling (RGS) protein RGS4 of T. reesei. We show that RGS4 is involved in regulation of cellulase production, growth, asexual development and oxidative stress response in darkness as well as in osmotic stress response in the presence of sodium chloride, particularly in light. Transcriptome analysis revealed regulation of several ribosomal genes, six genes mutated in RutC30 as well as several genes encoding transcription factors and transporters. Importantly, RGS4 positively regulates the siderophore cluster responsible for fusarinine C biosynthesis in light. The respective deletion mutant shows altered growth on nutrient sources related to siderophore production such as ornithine or proline in a BIOLOG phenotype microarray assay. Additionally, growth on storage carbohydrates as well as several intermediates of the D-galactose and D-arabinose catabolic pathway is decreased, predominantly in light.

    Conclusions

    We conclude that RGS4 mainly operates in light and targets plant cell wall degradation, siderophore production and storage compound metabolism in T. reesei.

  • Gold-FISH enables targeted NanoSIMS analysis of plant-associated bacteria

    Schmidt H, Gorka S, Seki D, Schintlmeister A, Woebken D
    2023 - New Phytologist, 240: 439-451

    Abstract: 

    Summary

     

    • Bacteria colonize plant roots and engage in reciprocal interactions with their hosts. However, the contribution of individual taxa or groups of bacteria to plant nutrition and fitness is not well characterized due to a lack of in situ evidence of bacterial activity.
    • To address this knowledge gap, we developed an analytical approach that combines the identification and localization of individual bacteria on root surfaces via gold-based in situ hybridization with correlative NanoSIMS imaging of incorporated stable isotopes, indicative of metabolic activity.
    • We incubated Kosakonia strain DS-1-associated, gnotobiotically grown rice plants with 15N–N2 gas to detect in situ N2 fixation activity. Bacterial cells along the rhizoplane showed heterogeneous patterns of 15N enrichment, ranging from the natural isotope abundance levels up to 12.07 at% 15N (average and median of 3.36 and 2.85 at% 15N, respectively, n = 697 cells).
    • The presented correlative optical and chemical imaging analysis is applicable to a broad range of studies investigating plant–microbe interactions. For example, it enables verification of the in situ metabolic activity of host-associated commercialized strains or plant growth-promoting bacteria, thereby disentangling their role in plant nutrition. Such data facilitate the design of plant–microbe combinations for improvement of crop management.
  • Phosphorus scarcity contributes to nitrogen limitation in lowland tropical rainforests

    Vallicrosa H, Lugli LF, Fuchslueger L, Sardans J, Ramírez-Rojas I, Verbruggen E, Grau O, Bréchet L, Peguero G, Van Langenhove L, Verryckt LT, Terrer C, Llusià J, Ogaya R, Márquez L, Roc-Fernández P, Janssens I, Peñuelas J
    2023 - Ecology, Article e4049

    Abstract: 

    There is increasing evidence to suggest that soil nutrient availability can limit the carbon sink capacity of forests, a particularly relevant issue considering today's changing climate. This question is especially important in the tropics, where most part of the Earth's plant biomass is stored. To assess whether tropical forest growth is limited by soil nutrients and to explore N and P limitations, we analyzed stem growth and foliar elemental composition of the 5 stem widest trees per plot at two sites in French Guiana after three years of nitrogen (N), phosphorus (P), and N+P addition. We also compared the results between potential N-fixer and non-N-fixer species. We found a positive effect of N fertilization on stem growth and foliar N, as well as a positive effect of P fertilization on stem growth, foliar N, and foliar P. Potential N-fixing species had greater stem growth, greater foliar N and greater foliar P concentrations than non-N-fixers. In terms of growth, there was a negative interaction between N-fixer status, N+P, and P fertilization, but no interaction with N fertilization. Since N-fixing plants does not show to be completely N saturated, we do not anticipate N providing from N-fixing plants would supply non-N-fixers. Although the soil age hypothesis only anticipates P limitation in highly weathered systems, our results for stem growth and foliar elemental composition indicate the existence of considerable N and P co-limitation, which is alleviated in N-fixing plants. The evidence suggests that certain mechanisms invest in N to obtain the scarce P through soil phosphatases, which potentially contributes to the N limitation detected by this study.

  • Long-term soil warming decreases microbial phosphorus utilization by increasing abiotic phosphorus sorption and phosphorus losses

    Tian Y, Shi C, Malo CU, Kendo SK, Heinzle J, Inselsbacher E, Ottner F, Borken W, Michel K, Schindlbacher A, Wanek W
    2023 - Nature Communications, 14: Article 864

    Abstract: 

    Phosphorus (P) is an essential and often limiting element that could play a crucial role in terrestrial ecosystem responses to climate warming. However, it has yet remained unclear how different P cycling processes are affected by warming. Here we investigate the response of soil P pools and P cycling processes in a mountain forest after 14 years of soil warming (+4 °C). Long-term warming decreased soil total P pools, likely due to higher outputs of P from soils by increasing net plant P uptake and downward transportation of colloidal and particulate P. Warming increased the sorption strength to more recalcitrant soil P fractions (absorbed to iron oxyhydroxides and clays), thereby further reducing bioavailable P in soil solution. As a response, soil microbes enhanced the production of acid phosphatase, though this was not sufficient to avoid decreases of soil bioavailable P and microbial biomass P (and biotic phosphate immobilization). This study therefore highlights how long-term soil warming triggers changes in biotic and abiotic soil P pools and processes, which can potentially aggravate the P constraints of the trees and soil microbes and thereby negatively affect the C sequestration potential of these forests.

  • MAPkinases regulate secondary metabolism, sexual development and light dependent cellulase regulation in Trichoderma reesei

    Schalamun M, Beier S, Hinterdobler W, Wanko N, Schinnerl J, Brecher L, Engl DE, Schmoll M
    2023 - Scientific Reports, 13: Article 1912

    Abstract: 

    The filamentous fungus Trichoderma reesei is a prolific producer of plant cell wall degrading enzymes, which are regulated in response to diverse environmental signals for optimal adaptation, but also produces a wide array of secondary metabolites. Available carbon source and light are the strongest cues currently known to impact secreted enzyme levels and an interplay with regulation of secondary metabolism became increasingly obvious in recent years. While cellulase regulation is already known to be modulated by different mitogen activated protein kinase (MAPK) pathways, the relevance of the light signal, which is transmitted by this pathway in other fungi as well, is still unknown in T. reesei as are interconnections to secondary metabolism and chemical communication under mating conditions. Here we show that MAPkinases differentially influence cellulase regulation in light and darkness and that the Hog1 homologue TMK3, but not TMK1 or TMK2 are required for the chemotropic response to glucose in T. reesei. Additionally, MAPkinases regulate production of specific secondary metabolites including trichodimerol and bisorbibutenolid, a bioactive compound with cytostatic effect on cancer cells and deterrent effect on larvae, under conditions facilitating mating, which reflects a defect in chemical communication. Strains lacking either of the MAPkinases become female sterile, indicating the conservation of the role of MAPkinases in sexual fertility also in T. reesei. In summary, our findings substantiate the previously detected interconnection of cellulase regulation with regulation of secondary metabolism as well as the involvement of MAPkinases in light dependent gene regulation of cellulase and secondary metabolite genes in fungi.

  • 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

    Abstract: 

    Summary

     

    • 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

    Abstract: 

    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.

  • Does long-term soil warming affect microbial element limitation? A test by short-term assays of microbial growth responses to labile C, N and P additions

    Shi C, Urbina-Malo C, Tian Y, Heinzle J, Kendo SK, Inselsbacher E, Borken W, Schindlbacher A, Wanek W
    2023 - Global Change Biology, 29: 2188-2202

    Abstract: 

    Increasing global temperatures have been reported to accelerate soil carbon (C) cycling, but also to promote nitrogen (N) and phosphorus (P) dynamics in terrestrial ecosystems. However, warming can differentially affect ecosystem C, N and P dynamics, potentially intensifying elemental imbalances between soil resources, plants and soil microorganisms. Here, we investigated the effect of long-term soil warming on microbial resource limitation, based on measurements of microbial growth (18O incorporation into DNA) and respiration after C, N and P amendments. Soil samples were taken from two soil depths (0–10, 10–20 cm) in control and warmed (>14 years warming, +4°C) plots in the Achenkirch soil warming experiment. Soils were amended with combinations of glucose-C, inorganic/organic N and inorganic/organic P in a full factorial design, followed by incubation at their respective mean field temperatures for 24 h. Soil microbes were generally C-limited, exhibiting 1.8-fold to 8.8-fold increases in microbial growth upon C addition. Warming consistently caused soil microorganisms to shift from being predominately C limited to become C-P co-limited. This P limitation possibly was due to increased abiotic P immobilization in warmed soils. Microbes further showed stronger growth stimulation under combined glucose and inorganic nutrient amendments compared to organic nutrient additions. This may be related to a prolonged lag phase in organic N (glucosamine) mineralization and utilization compared to glucose. Soil respiration strongly positively responded to all kinds of glucose-C amendments, while responses of microbial growth were less pronounced in many of these treatments. This highlights that respiration–though easy and cheap to measure—is not a good substitute of growth when assessing microbial element limitation. Overall, we demonstrate a significant shift in microbial element limitation in warmed soils, from C to C-P co-limitation, with strong repercussions on the linkage between soil C, N and P cycles under long-term warming.

  • Uptake, Metabolism, and Accumulation of Tire Wear Particle-Derived Compounds in Lettuce

    Castan S, Sherman A, Peng R, Zumstein MT, Wanek W, Hüffer T, Hofmann T
    2023 - Environmental Science & Technology, 57: 168-178

    Abstract: 

    Tire wear particle (TWP)-derived compounds may be of high concern to consumers when released in the root zone of edible plants. We exposed lettuce plants to the TWP-derived compounds diphenylguanidine (DPG), hexamethoxymethylmelamine (HMMM), benzothiazole (BTZ), N-phenyl-N′-(1,3-dimethylbutyl)-p-phenylenediamine (6PPD), and its quinone transformation product (6PPD-q) at concentrations of 1 mg L–1 in hydroponic solutions over 14 days to analyze if they are taken up and metabolized by the plants. Assuming that TWP may be a long-term source of TWP-derived compounds to plants, we further investigated the effect of leaching from TWP on the concentration of leachate compounds in lettuce leaves by adding constantly leaching TWP to the hydroponic solutions. Concentrations in leaves, roots, and nutrient solution were quantified by triple quadrupole mass spectrometry, and metabolites in the leaves were identified by Orbitrap high resolution mass spectrometry. This study demonstrates that TWP-derived compounds are readily taken up by lettuce with measured maximum leaf concentrations between ∼0.75 (6PPD) and 20 μg g–1 (HMMM). Although these compounds were metabolized in the plant, we identified several transformation products, most of which proved to be more stable in the lettuce leaves than the parent compounds. Furthermore, continuous leaching from TWP led to a resupply and replenishment of the metabolized compounds in the lettuce leaves. The stability of metabolized TWP-derived compounds with largely unknown toxicities is particularly concerning and is an important new aspect for the impact assessment of TWP in the environment.

  • Spectroscopic analysis of sequestered chloroplasts in Elphidium williamsoni (Foraminifera)

    Lintner M, Wildner M, Lintner B, Wanek W, Heinz P
    2023 - Journal of Photochemistry and Photobiology B: Biology, 238: Article 112623

    Abstract: 

    Foraminifera are unicellular, marine organisms that occur worldwide. A very common species in the German Wadden Sea is Elphidium williamsoni. Some foraminifera (such as elphidia) are able to use kleptoplastidy, which allows them to incorporate chloroplasts from their algal food source into their own cell body. The experiments reported here are based on the fact that chlorophyll (a and c) can be detected in the intact cells with spectroscopic methods in the visible spectral range, which allows an indirect investigation of the presence of sequestered chloroplasts. Starving experiments of E. williamsoni in the light (24 h continuous) showed that the greatest decrease in chlorophyll content was recorded within the first 20–30 days. From day 60 on, chlorophyll was hardly detectable. Through subsequent feeding on a renewed algal food source a significant increase in the chlorophyll content in foraminifera was noticed. The degradation of chlorophyll in the dark (24 h continuous darkness) during the starving period was much more complex. Chlorophyll was still detected in the cells after 113 days of starving time. Therefore, we hypotheses that the effect of photoinhibition applies to chloroplasts in foraminifera under continuous illumination.

  • Increase in carbon input by enhanced fine root turnover in a long-term warmed forest soil

    Kengdo SK, Ahrens B, Tian Y, Heinzle J, Wanek W, Schindlbacher A, Borken W
    2023 - Science of The Total Environment, 855: Article 15800

    Abstract: 

    Fine root litter represents an important carbon input to soils, but the effect of global warming on fine root turnover (FRT) is hardly explored in forest ecosystems. Understanding tree fine roots' response to warming is crucial for predicting soil carbon dynamics and the functioning of forests as a sink for atmospheric carbon dioxide (CO2). We studied fine root production (FRP) with ingrowth cores and used radiocarbon signatures of first-order, second- to third-order, and bulk fine roots to estimate fine root turnover times after 8 and 14 years of soil warming (+4 °C) in a temperate forest. Fine root turnover times of the individual root fractions were estimated with a one-pool model. Soil warming strongly increased fine root production by up to 128 % within one year, but after two years, the production was less pronounced (+35 %). The first-year production was likely very high due to the rapid exploitation of the root-free ingrowth cores. The radiocarbon signatures of fine roots were overall variable among treatments and plots. Soil warming tended to decrease fine root turnover times of all the measured root fractions after 8 and 14 years of warming, and there was a tendency for trees to use older carbon reserves for fine root production in warmed plots. Furthermore, soil warming increased fine root turnover from 50 to 106 g C m−2 yr−1 (based on two different approaches). Our findings suggest that future climate warming may increase carbon input into soils by enhancing fine root turnover. If this increase may partly offset carbon losses by increased mineralization of soil organic matter in temperate forest soils is still unclear and should guide future research.

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