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DOE OSTI2022

Microbial extracellular enzyme activity with simulated climate change

It is critical to understand the consequences of environmental change for the microbial regulation of carbon and nutrient cycling. Specifically, understanding microbial community traits, such as extracellular enzyme activity, can help inform nutrient cycling models and address knowledge gaps. We analyzed data on extracellular enzyme activities and litter decomposition from an 18-month experiment in which microbial communities were reciprocally transplanted along a climate gradient in Southern California. Communities were from desert, scrubland, grassland, pine–oak, and subalpine ecosystems. We aimed to test how enzyme activities responded to climate change following transplantation and how those responses related to decomposition rates. We hypothesized that microbial communities would specialize on their native climate conditions, resulting in higher enzyme activities when transplanted back into their native climate. We investigated the relationship between extracellular enzyme Vmax values, substrate mass loss, and microbial biomass as well as variation in these variables across the climate gradient. We found little evidence for climate specialization, and there was rarely a reduction in enzyme functioning after microbial communities were transplanted into new climate conditions. Moreover, observed differences in decomposition were not related to changes in extracellular enzyme potential, although there were significant differences in enzyme activities and decomposition rates across sites. These results suggest that direct, physiological impacts of climate are likely to be important for enzyme-mediated decomposition, but climate specialization will not constrain the microbial response to climate change in our system.

54 ENVIRONMENTAL SCIENCES↗

DOE OSTI2023

Inhibition of Extracellular Enzyme Activity by Reactive Oxygen Species upon Oxygenation of Reduced Iron-Bearing Minerals

The dual roles of minerals in inhibiting and prolonging extracellular enzyme activity in soils and sediments are governed by enzyme adsorption to mineral surface. Oxigenation of mineral-bound Fe(II) generates reactive oxygen species (ROS), yet it is unknown whether and how this process alters the activity and functional lifespan of extracellular enzymes. Here, the effect of mineral-bound Fe(II) oxidation on the hydrolytic activity of a cellulose-degrading enzyme ß-glucosidase (BG) was studied using two pre-reduced Fe-bearing clay minerals (nontronite and montmorillonite) and one pre-reduced iron oxide (magnetite) at pH 5 and 7. Under anoxic condition, BG adsorption to mineral surface decreased its activity but prolonged its lifespan. Under oxic condition, ROS was produced, with the amount of •OH, the most abundant ROS, being positively correlated with the extent of structural Fe(II) oxidation in reduced minerals. •OH decreased BG activity and shortened its lifespan via conformational change and structural decomposition of BG. These results suggest that under oxic condition the ROS-induced inhibitory role of Fe(II)-bearing minerals outweighed their adsorption-induced protective role in controlling enzyme activity. These results disclose a previously unknown mechanism of extracellular enzyme inactivation, which have pivotal implications for predicting the active enzyme pool in redox-oscillating environments.

58 GEOSCIENCES↗

DOE OSTI2020

Continental-scale patterns of extracellular enzyme activity in the subsoil: an overlooked reservoir of microbial activity

Abstract Chemical stabilization of microbial-derived products such as extracellular enzymes (EE) onto mineral surfaces has gained attention as a possibly important mechanism leading to the persistence of soil organic carbon (SOC). While the controls on EE activities and their stabilization in the surface soil are reasonably well-understood, how these activities change with soil depth and possibly diverge from those at the soil surface due to distinct physical, chemical, and biotic conditions remains unclear. We assessed EE activity to a depth of 1 m (10 cm increments) in 19 soil profiles across the Critical Zone Observatory Network, which represents a wide range of climates, soil orders, and vegetation types. For all EEs, activities per mass of soil correlated positively with microbial biomass (MB) and SOC, and all three of these variables decreased logarithmically with depth ( p < 0.05). Across all sites, over half of the potential EE activities per mass soil consistently occurred below 20 cm for all measured EEs. Activities per unit MB or SOC were substantially higher at depth (soils below 20 cm accounted for 80% of whole-profile EE activity), suggesting an accumulation of stabilized (i.e. mineral sorbed) EEs in subsoil horizons. The pronounced enzyme stabilization in subsurface horizons was corroborated by mixed-effects models that showed a significant, positive relationship between clay concentration and MB-normalized EE activities in the subsoil. Furthermore, the negative relationships between soil C, N, and P and C-, N-, and P-acquiring EEs found in the surface soil decoupled below 20 cm, which could have also been caused by EE stabilization. This finding suggests that EEs may not reflect soil nutrient availabilities deeper in the soil profile. Taken together, our results suggest that deeper soil horizons hold a significant reservoir of EEs, and that the controls of subsoil EEs differ from their surface soil counterparts.

37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CH↗

DOE OSTI2020

Patterns in extracellular enzyme activity and microbial diversity in deep-sea Mediterranean sediments

Deep-sea sediments are populated by diverse microbial communities that derive their nutritional requirements from the degradation of organic matter. Extracellular hydrolytic enzymes play a key role in the survival of microbes by enabling them to access and degrade complex organic compounds that are found in seafloor sediments. Despite their importance, extracellular enzymatic activity is poorly characterized at water depths greater than a few hundred meters where physical properties, such as pressure and temperature, create a unique environment for influencing enzyme behavior. In this work, we investigated microbial communities and enzyme activities in surface sediment collected at four sampling stations in the central Mediterranean Sea at water depths ranging from 800 to 2200 m. Fluorometric assays revealed that extracellular hydrolytic activity varied according to substrate type and water depth which suggests that the distributions of these enzymes within this basin are not homogenous. Furthermore, enzyme activities indicated substantial demand for phosphomonoesters and proteins, with measurable but much lower demand for polysaccharides. Barcoded amplicon sequencing of bacterial and archaeal SSU genes revealed that microbial communities varied across sampling stations and some groups displayed water-depth related trends. Our results demonstrate that heterotrophic capabilities of microbes in deep-sea Mediterranean sediments can differ substantially even within the same region.

16S rRNA↗

DOE OSTI2020

Soil microbial function and fungal community data along an ectomycorrhizal basal area gradient, Vermont, May 2019

Mycorrhizal fungi can affect soil organic matter cycling through several mechanisms including priming, nutrient competition, and direct enzyme production. Differences in nutrient foraging strategies between ectomycorrhizal (EcM) and arbuscular mycorrhizal (AM) fungi produce divergent belowground dynamics: where EcM can take up organic nitrogen and directly break down SOM by producing enzymes, AM fungi are limited to scavenging mineral N. EcM-associated tree species also have leaf litter with relatively higher ratios of carbon to nitrogen (C:N), and belowground saprotrophic communities more dominated by fungi. Consequently, free-living microbes in EcM-dominated soils should experience nitrogen limitation, with subsequent increases in enzyme production and decreased carbon use efficiency (CUE). However, the relative importance of the effects of substrate quality and fungal community composition on enzyme production and CUE are unclear. To assess this distinction, we sampled the organic horizon and 10 cm of the mineral horizon in northern temperate forest soils along a gradient of EcM dominance (see SCxTS_DBH.csv for full tree species information). We characterized fungal community composition by measuring EcM relative abundances from extracted fungal DNA (To run raw ASV data through R code, use SCxTS_ASV_taxonomy.csv, and R code ITS_processing.Rmd; to see processed data with EcM relative abundance, use file SCxTS_sum_afitch_Feb18.20.csv) and the fungal to bacterial ratios (see data file SCxTS_plfa.csv) from phospholipid fatty acid analysis. Soil microbial functions were measured as potential activities of five hydrolytic and two oxidative enzymes ( To run raw data through R code us SCxTS_metadata.csv, hydrolytic_oxidative_raw.csv, MUBraw.csv, Enzyme_soilweight.csv, and incubationtime.csv, and R code SCxTS_enzymes.Rmd; to use Enzyme data ready to run through statistics code, use file Enzyme.data.csv) and microbial carbon use efficiency (see file SCxTS_CUE.csv and for full calculations file 18O_CUEcalcs_SCxTS_2019.xlsx). We assessed soil substrate quality as the soil carbon:nitrogen ratio (See file Organic_CN.csv). Statistical analysis can be run using R code from file SCxTS_analysis.Rmd.

54 ENVIRONMENTAL SCIENCES↗

DOE OSTI2021

Phenotypic plasticity of fungal traits in response to moisture and temperature

Phenotypic plasticity of traits is commonly measured in plants to improve understanding of organismal and ecosystem responses to climate change but is far less studied for microbes. Specifically, decomposer fungi are thought to display high levels of phenotypic plasticity and their functions have important implications for ecosystem dynamics. Assessing the phenotypic plasticity of fungal traits may therefore be important for predicting fungal community response to climate change. Here, we assess the phenotypic plasticity of 15 fungal isolates (12 species) from a Southern California grassland. Fungi were incubated on litter at five moisture levels (ranging from 4–50% water holding capacity) and at five temperatures (ranging from 4–36 °C). After incubation, fungal biomass and activities of four extracellular enzymes (cellobiohydrolase (CBH), β -glucosidase (BG), β -xylosidase (BX), and N-acetyl- β - D -glucosaminidase (NAG)) were measured. We used response surface methodology to determine how fungal phenotypic plasticity differs across the moisture-temperature gradient. We hypothesized that fungal biomass and extracellular enzyme activities would vary with moisture and temperature and that the shape of the response surface would vary between fungal isolates. We further hypothesized that more closely related fungi would show more similar response surfaces across the moisture-temperature gradient. In support of our hypotheses, we found that plasticity differed between fungi along the temperature gradient for fungal biomass and for all the extracellular enzyme activities. Plasticity also differed between fungi along the moisture gradient for BG activity. These differences appear to be caused by variation mainly at the moisture and temperature extremes. We also found that more closely related fungi had more similar extracellular enzymes activities at the highest temperature. Altogether, this evidence suggests that with global warming, fungal biodiversity may become increasingly important as functional traits tend to diverge along phylogenetic lines at higher temperatures.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2022

On Single-Cell Enzyme Assays in Marine Microbial Ecology and Biogeochemistry

Extracellular enzyme activity is a well-established parameter for evaluating microbial biogeochemical roles in marine ecosystems. The presence and activity of extracellular enzymes in seawater provide insights into the quality and quantity of organic matter being processed by the present microorganisms. A key challenge in our understanding of these processes is to decode the extracellular enzyme repertoire and activities of natural communities at the single-cell level. Current measurements are carried out on bulk or size-fractionated samples capturing activities of mixed populations. This approach – even with size-fractionation – cannot be used to trace enzymes back to their producers, nor distinguish the active microbial members, leading to a disconnect between measured activities and the producer cells. By targeting extracellular enzymes and resolving their activities at the single-cell level, we can investigate underlying phenotypic heterogeneity among clonal or closely related organisms, characterize enzyme kinetics under varying environmental conditions, and resolve spatio-temporal distribution of individual enzyme producers within natural communities. In this perspective piece, we discuss state-of-the-art technologies in the fields of microfluidic droplets and functional screening of prokaryotic cells for measuring enzyme activity in marine seawater samples, one cell at a time. We further elaborate on how this single-cell approach can be used to address research questions that cannot be answered with current methods, as pertinent to the enzymatic degradation of organic matter by marine microorganisms.

54 ENVIRONMENTAL SCIENCES↗

DOE OSTI2021

Exploring Trait Trade-Offs for Fungal Decomposers in a Southern California Grassland

Fungi are important decomposers in terrestrial ecosystems, so their responses to climate change might influence carbon (C) and nitrogen (N) dynamics. We investigated whether growth and activity of fungi under drought conditions were structured by trade-offs among traits in 15 fungal isolates from a Mediterranean Southern California grassland. We inoculated fungi onto sterilized litter that was incubated at three moisture levels (4, 27, and 50% water holding capacity, WHC). For each isolate, we characterized traits that described three potential lifestyles within the newly proposed “YAS” framework: growth yield, resource acquisition, and stress tolerance. Specifically, we measured fungal hyphal length per unit litter decomposition for growth yield; the potential activities of the extracellular enzymes cellobiohydrolase (CBH), β -glucosidase (BG), β -xylosidase (BX), and N-acetyl- β - D -glucosaminidase (NAG) for resource acquisition; and ability to grow in drought vs. higher moisture levels for drought stress tolerance. Although, we had hypothesized that evolutionary and physiological trade-offs would elicit negative relationships among traits, we found no supporting evidence for this hypothesis. Across isolates, growth yield, drought stress tolerance, and extracellular enzyme activities were not significantly related to each other. Thus, it is possible that drought-induced shifts in fungal community composition may not necessarily lead to changes in fungal biomass or decomposer ability in this arid grassland.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2021

Differential Organic Carbon Mineralization Responses to Soil Moisture in Three Different Soil Orders Under Mixed Forested System

Soil microbial respiration is one of the largest sources of carbon (C) emissions to the atmosphere in terrestrial ecosystems, which is strongly dependent on multiple environmental variables including soil moisture. Soil moisture content is strongly dependent on soil texture, and the combined effects of texture and moisture on microbial respiration are complex and less explored. Therefore, this study examines the effects of soil moisture on the mineralization of soil organic C Soil organic carbon in three different soils, Ultisol, Alfisol and Vertisol, collected from mixed forests of Georgia, Missouri, and Texas, United States , respectively. A laboratory microcosm experiment was conducted for 90 days under different moisture regimes. Soil respiration was measured weekly, and destructive harvests were conducted at 1, 15, 60, and 90 days after incubation to determine extractable organic C (EOC), phospholipid fatty acid based microbial community, and C-acquiring hydrolytic extracellular enzyme activities (EEA). The highest cumulative respiration in Ultisol was observed at 50% water holding capacity (WHC), in Alfisol at 100% water holding capacity, and in Vertisol at 175% WHC. The trends in Extractable Organic Carbon were opposite to that of cumulative microbial respiration as the moisture levels showing the highest respiration showed the lowest EOC concentration in all soil types. Also, extracellular enzyme activities increased with increase in soil moisture in all soils, however, respiration and EEA showed a decoupled relationship in Ultisol and Alfisol soils. Soil moisture differences did not influence microbial community composition.

54 ENVIRONMENTAL SCIENCES↗

DOE OSTI2022

Trait relationships of fungal decomposers in response to drought using a dual field and laboratory approach

Abstract Decomposer fungi play a fundamental role in terrestrial ecosystem dynamics. In the southwestern United States, climate change is causing more frequent and severe droughts, which may alter fungal community composition and activity. Investigating relationships between fungal traits may improve the prediction of fungal responses to drought. In this dual field and laboratory experiment, we examine whether trade‐offs occur between traits associated with drought. Specifically, we test the hypothesis that fungi sort into lifestyles specializing in growth y ield, resource a cquisition, and drought s tress tolerance (“YAS” framework). For the field experiment, we constructed microbial “cages” containing sterilized litter and 1 of 10 fungal isolates. These cages were placed in long‐term drought and control plots in a southern Californian grassland for 6 and 12 months. We measured fungal hyphal length per unit litter mass loss for growth yield, the potential activities of four extracellular enzymes for resource acquisition, and the ability to grow in the drought versus control plots for drought stress tolerance. We compared these results with a laboratory microcosm experiment constructed with the same fungal isolates and that measured the same fungal traits. The field experiment corroborated our laboratory results, in that no trade‐offs were observed between growth yield and resource acquisition traits. However, in contrast to the laboratory experiment, drought tolerance was negatively related to extracellular enzyme activity and growth yield in the field, implying a trade‐off. Despite this observed trade‐off in the field, growth yield was not hindered by drought. We propose a modification to the YAS framework, by combining the growth yield and resource acquisition lifestyles, which may be more appropriate for this arid system. This joint laboratory and field approach contextualizes a theoretical framework in microbial ecology and improves understanding of fungal community response to climate change.

54 ENVIRONMENTAL SCIENCES↗

DOE OSTI2023

Dairy manure acidogenic fermentation at hyperthermophilic temperature enabled superior activity of thermostable hydrolytic enzymes linked to the genus Caldicoprobacter

In this study, fermentation experiments were conducted under mesophilic, thermophilic, and hyperthermophilic conditions to investigate adaptation of microbial communities and its effect on extracellular enzyme activities toward degradation of cellulose, hemicellulose and proteins in dairy manure. Here, hyperthermophilic conditions transformed the microbiome structure and stimulated activity of extracellular proteolytic, cellulolytic, and hemicellulolytic enzymes. Specifically, the activities of protease, cellulose 1,4-β-cellobiosidase, and β-glucosidase secreted by hyperthermophilic microbes were higher by 22%, 47% and 49% compared to those produced by mesophilic and thermophilic communities. Enhanced hydrolytic activity of hyperthermophilic microbes enabled improved feedstock solubilization and production of 39% and 22% more soluble COD than mesophilic and thermophilic microbes, respectively. Connections between hydrolytic function and microbial community structure at various temperatures were assessed using the PICRUSt2 computational tool. Genus Caldicoprobacter was identified as the primary candidate responsible for increased production of thermostable endo-1,4-β-glucanase, β-glucosidase and endo-1,4-β-xylanase, and enhanced hydrolytic performance of hyperthermophilic microbial community.

09 BIOMASS FUELS↗

DOE OSTI2024

Root exudation links root traits to soil functioning in agroecosystems

Root exudation is a key process for plant nutrient acquisition, but the controls on root exudation and its relationship to soil C and N processes in agroecosystems are unclear. We hypothesized that root exudation rates would be related to root morphological traits, N fertilization, and soil moisture. We also anticipated that root exudation would be correlated with bulk soil enzyme activity. Root exudation, root traits, and bulk soil extracellular enzyme activity were assessed in maize (Zea mays L.), soybean (Glycine max (L.) Merr.), biomass sorghum (Sorghum bicolor (L.) Moench), giant miscanthus (Miscanthus × giganteus), and switchgrass (Panicum virgatum L.). Measurements were taken in situ during two growing seasons with contrasting precipitation regimes, and N fertilization rate was varied in sorghum during one year. Specific root exudation (per unit root surface area) was negatively related to root diameter and was generally higher in annuals than perennials. Sorghum N fertilization did not affect root exudation rates, and soil moisture regime had no effect on annual root exudation rates within maize, sorghum, and miscanthus. Specific root exudation was negatively related to bulk soil C- and N-degrading soil enzyme activities. Intrinsic plant characteristics appeared more important than environmental variables in controlling in situ root exudation rates. The relationships between root diameter, root exudation, and soil C and N processes link root morphological traits to soil functions and demonstrate the potential tradeoffs among plant nutrient acquisition strategies in agroecosystems.

54 ENVIRONMENTAL SCIENCES↗

DOE OSTI2024

Data for Root Exudation Links Root Traits to Soil Functioning in Agroecosystems

Biomass Analytics↗

DOE OSTI2025

Direct root contact among neighboring plants influences activity of soil extracellular enzymes

Composition and diversity of vegetation systems can influence soil microbial activity and extracellular enzyme (EE) dynamics, which are crucial for soil carbon (C) accrual and nutrient cycling. Yet, the impact of plant interactions and competition on EE activities remains a notable knowledge gap. This study examines how direct root contact and neighboring plant identity affect the activity and spatial distribution of four key soil EEs: β-glucosidase (BGlu), chitinase, acid phosphatase (AcidP), and alkaline phosphatase (AlkP). Using three-compartment rhizoboxes with switchgrass (Panicum virgatum L.) grown alongside bush clover (Lespedeza capitata Michx.), and black-eyed Susan (Rudbeckia hirta L.), we assessed enzyme activities using zymography under conditions that either allowed or restricted direct root contact by root barriers. Results show that root proliferation and species interactions significantly influenced EE activity. While BGlu and AcidP activities were strongly correlated with root biomass, AlkP activity was consistently higher in the absence of root barriers, indicating a pronounced microbial response to plant interactions via direct/close root contacts. Additionally, soil phosphorus availability modulated enzyme activity, with higher phosphatase activities in low-P soils. Furthermore, these findings highlight the importance of root-root interactions and plant species composition in shaping soil biochemical processes.

enyzme activity↗

DOE OSTI2021

Depth dependence of climatic controls on soil microbial community activity and composition

Abstract Subsoil microbiomes play important roles in soil carbon and nutrient cycling, yet our understanding of the controls on subsoil microbial communities is limited. Here, we investigated the direct (mean annual temperature and precipitation) and indirect (soil chemistry) effects of climate on microbiome composition and extracellular enzyme activity throughout the soil profile across two elevation-bioclimatic gradients in central California, USA. We found that microbiome composition changes and activity decreases with depth. Across these sites, the direct influence of climate on microbiome composition and activity was relatively lower at depth. Furthermore, we found that certain microbial taxa change in relative abundance over large temperature and precipitation gradients only in specific soil horizons, highlighting the depth dependence of the climatic controls on microbiome composition. Our finding that the direct impacts of climate are muted at depth suggests that deep soil microbiomes may lag in their acclimation to new temperatures with a changing climate.

16S rRNA↗

DOE OSTI2020

Fungal Community, Not Substrate Quality, Drives Soil Microbial Function in Northeastern U.S. Temperate Forests

Mycorrhizal fungi can affect soil organic matter cycling through several mechanisms including priming, nutrient competition, and direct enzyme production. Differences in nutrient foraging strategies between ectomycorrhizal (EcM) and arbuscular mycorrhizal (AM) fungi produce divergent belowground dynamics: where EcM can take up organic nitrogen and directly break down soil organic matter (SOM) by producing enzymes, AM fungi are limited to scavenging mineral N. EcM-associated tree species also have leaf litter with relatively higher ratios of carbon to nitrogen (C:N), and belowground saprotrophic communities more dominated by fungi. Consequently, free-living microbes in EcM-dominated soils should experience nitrogen limitation, with subsequent increases in enzyme production and decreased carbon use efficiency (CUE). However, the relative importance of the effects of substrate quality and fungal community composition on enzyme production and CUE are unclear. To assess this distinction, we sampled the organic horizon and 10 cm of the mineral horizon in northern temperate forest soils along a gradient of EcM dominance. We characterized fungal community composition by measuring EcM relative abundances from extracted fungal DNA and the fungal to bacterial (F:B) ratios from phospholipid fatty acid (PLFA) analysis. We assessed soil substrate quality as the soil C:N ratio. Soil microbial functions were measured as potential activities of five hydrolytic and two oxidative enzymes, and microbial CUE. We found that the fungal community, represented by either the F:B ratio, EcM relative abundance, or both, affected CUE and six measured enzyme activities, while the C:N ratio affected only oxidative and chitin-targeting extracellular enzyme activities. Our results highlight the use of EcM relative dominance as a predictor of soil microbial community composition and function independent of substrate quality.

54 ENVIRONMENTAL SCIENCES↗

DOE OSTI2021

Variation in hyphal production rather than turnover regulates standing fungal biomass in temperate hardwood forests

Abstract Soil fungi link above‐ and belowground carbon (C) fluxes through their interactions with plants and contribute to C and nutrient dynamics through the production, turnover, and activity of fungal hyphae. Despite their importance to ecosystem processes, estimates of hyphal production and turnover rates are relatively uncommon, especially in temperate hardwood forests. We sequentially harvested hyphal ingrowth bags to quantify the rates of Dikarya (Ascomycota and Basidiomycota) hyphal production and turnover in three hardwood forests in the Midwestern United States, where plots differed in their abundance of arbuscular (AM)‐ vs. ectomycorrhizal (ECM)‐associated trees. Hyphal production rates increased linearly with the percentage of ECM trees and annual production rates were 66% higher in ECM‐ than AM‐dominated plots. Hyphal turnover rates did not differ across the mycorrhizal gradient (plots varying in their abundance of AM vs. ECM trees), suggesting that the greater fungal biomass in ECM‐dominated plots relates to greater fungal production rather than slower fungal turnover. Differences in hyphal production across the gradient aligned with distinctly different fungal communities and activities. As ECM trees increased in dominance, fungi inside ingrowth bags produced more extracellular enzymes involved in degrading nitrogen (N)‐bearing relative to C‐bearing compounds, suggesting greater fungal (and possibly plant) N demand in ECM‐dominated soils. Collectively, our results demonstrate that shifts in temperate tree species composition that result in changes in the dominant type of mycorrhizal association may have strong impacts on Dikarya hyphal production, fungal community composition and extracellular enzyme activity, with important consequences for soil C and N cycling.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2022

Substrate availability and not thermal acclimation controls microbial temperature sensitivity response to long-term warming

Microbes are responsible for cycling carbon (C) through soils, and predicted changes in soil C stocks under climate change are highly sensitive to shifts in the mechanisms assumed to control the microbial physiological response to warming. Two mechanisms have been suggested to explain the long-term warming impact on microbial physiology: microbial thermal acclimation and changes in the quantity and quality of substrates available for microbial metabolism. Yet studies disentangling these two mechanisms are lacking. To resolve the drivers of changes in microbial physiology in response to long-term warming, we sampled soils from 13- and 28-year-old soil warming experiments in different seasons. We performed short-term laboratory incubations across a range of temperatures to measure the relationships between temperature sensitivity of physiology (growth, respiration, carbon use efficiency, and extracellular enzyme activity) and the chemical composition of soil organic matter. We observed apparent thermal acclimation of microbial respiration, but only in summer, when warming had exacerbated the seasonally-induced, already small dissolved organic matter pools. Irrespective of warming, greater quantity and quality of soil carbon increased the extracellular enzymatic pool and its temperature sensitivity. We propose that fresh litter input into the system seasonally cancels apparent thermal acclimation of C-cycling processes to decadal warming. Our findings reveal that long-term warming has indirectly affected microbial physiology via reduced C availability in this system, implying that earth system models including these negative feedbacks may be best suited to describe long-term warming effects on these soils.

59 BASIC BIOLOGICAL SCIENCES↗