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Fungal decomposition of soil organic matter depends on soil nitrogen (N) availability. This ecosystem process is being jeopardized by changes in N inputs that have resulted from a tripling of atmospheric N deposition in the last century. Soil fungi are impacted by atmospheric N deposition due to higher N availability, as soils are acidified, or as micronutrients become increasingly limiting. Fungal communities that persist with chronic N deposition may be enriched with traits that enable them to tolerate environmental stress, which may trade-off with traits enabling organic matter decomposition. We hypothesized that fungal communities would respond to N deposition by shifting community composition and functional gene abundances toward those that tolerate stress but are weak decomposers. We sampled soils at seven eastern US hardwood forests where ambient N deposition varied from 3.2 to 12.6 kg N ha-1 year-1 , five of which also have experimental plots where atmospheric N deposition was simulated through fertilizer application treatments (25-50 kg N ha-1 year-1 ). Fungal community and functional responses to fertilizer varied across the ambient N deposition gradient. Fungal biomass and richness increased with simulated N deposition at sites with low ambient deposition and decreased at sites with high ambient deposition. Fungal functional genes involved in hydrolysis of organic matter increased with ambient N deposition while genes involved in oxidation of organic matter decreased. One of four genes involved in generalized abiotic stress tolerance increased with ambient N deposition. In summary, we found that the divergent response to simulated N deposition depended on ambient N deposition levels. Fungal biomass, richness, and oxidative enzyme potential were reduced by N deposition where ambient N deposition was high suggesting fungal communities were pushed beyond an environmental stress threshold. Fungal community structure and function responses to N enrichment depended on ambient N deposition at a regional scale.

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

The physicochemical environment within aggregates controls the distribution of carbon and microbial communities in soils. Agricultural management, such as tillage, can disrupt aggregates and the microscale habitat provided to microorganisms, thus altering microbial community dynamics. Categorizing microbial communities into life history strategies with shared functional traits—as has been done to understand plant community structure for decades—can illuminate how the soil physicochemical environment constrains the membership and activity of microbial communities. We conducted an aggregate scale survey of microbial community composition and function through the lens of the yield–acquisition–stress (Y–A–S) tolerator life history framework. Soils collected from a 7-year tillage experiment were separated into 4 aggregate size classes and enzyme activity, multiple-substrate-induced respiration, and carbon use efficiency were measured to reveal trade-offs in microbial resource allocation. Microbial community structure was interrogated with bacterial and fungal marker gene sequencing, and metagenomic features such as community weighted genome size and traits conferring stress tolerance were predicted using PICRUSt2. Consistent with our hypothesis, aggregates of different size classes harbored distinct microbial communities manifesting distinct life history strategies. Large macroaggregate communities >2 mm were classified as acquisition strategists based on increased enzyme activity relative to other aggregate size classes. Small and medium microaggregate (0.25–2 mm) communities did not show a strong tendency toward any particular life history strategy. Genes conferring stress tolerance were significantly enriched in microaggregates

Unlike other macroecological principles, relationships between productivity and diversity have not been effectively tested for microbial communities. Here we describe an experiment in which the availability of resources to soil bacterial communities was manipulated in a model system, the McMurdo Dry Valleys of Antarctica. Mannitol additions were used to simulate a productivity gradient such that a response in bacterial biomass production, taxonomic diversity and functioning (e.g., enzyme activity) were induced. Resource amendment induced a positive linear response in microbial productivity (P < 0.001) but a unimodal (hump-shaped) response in microbial diversity at multiple taxonomic scales (P = 0.035). Putative oligotrophic (e.g., phyla Nitrospirae and Cyanobacteria) and copiotrophic (e.g., phylum Proteobacteria) taxa were apparent through substantial community turnover along the resource gradient. Soil enzyme activity was inversely related to bacterial biomass but positively related to diversity, suggesting the latter may be a stronger control over enzyme-mediated decomposition. The mechanisms behind this pattern are consistent with macroecological theory of a shift from environmental (e.g., stress tolerance) to biotic (e.g., competition) drivers with increasing resource availability. This evidence is among the first of its kind to document a significant unimodal productivity-diversity relationship for soil bacteria.

Conceptual and empirical advances in soil biogeochemistry have challenged long-held assumptions about the role of soil micro-organisms in soil organic carbon (SOC) dynamics; yet, rigorous tests of emerging concepts remain sparse. Recent hypotheses suggest that microbial necromass production links plant inputs to SOC accumulation, with high-quality (i.e., rapidly decomposing) plant litter promoting microbial carbon use efficiency, growth, and turnover leading to more mineral stabilization of necromass. We test this hypothesis experimentally and with observations across six eastern US forests, using stable isotopes to measure microbial traits and SOC dynamics. Here we show, in both studies, that microbial growth, efficiency, and turnover are negatively (not positively) related to mineral-associated SOC. In the experiment, stimulation of microbial growth by high-quality litter enhances SOC decomposition, offsetting the positive effect of litter quality on SOC stabilization. We suggest that microbial necromass production is not the primary driver of SOC persistence in temperate forests. Factors such as microbial necromass origin, alternative SOC formation pathways, priming effects, and soil abiotic properties can strongly decouple microbial growth, efficiency, and turnover from mineral-associated SOC.

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.

Accurate estimates of microbial carbon use efficiency (CUE) are required to predict how global change will impact microbially-mediated ecosystem functions such as organic matter decomposition. Multiple approaches are currently used to quantify CUE but the extent to which estimates reflect methodological variability is unknown. This limits our ability to apply or cross-compare published CUE values. Here we evaluated the performance of five methods in a single soil under standard conditions. The microbial response to three substrate amendment rates (0.0, 0.05, and 2.0 mg glucose-C g−1 soil) was examined using: 13C and 18O isotope tracing approaches which estimate CUE based on substrate uptake and growth dynamics; calorespirometry which infers growth and CUE from metabolic heat and respiration rates; metabolic flux analysis where CUE is determined as the balance between biosynthesis and respiration using position-specific 13CO2 production of labeled glucose; and stoichiometric modeling which derives CUE from elemental ratios of microbial biomass, substrate, and exoenzyme activity. The CUE estimates we obtained differed by method and substrate concentration, ranging under in situ conditions from 0.6 for the substrate-specific methods that trace glucose use (13C method, calorespirometry, metabolic flux analysis). We explore the different aspects of microbial metabolism that each method captures and how this affects the interpretation of CUE estimates. We recommend that users consider the strengths and weaknesses of each method when choosing the technique that will best address their research needs.

Forest soil organic matter (SOM) is derived from both above- and belowground plant inputs, with a significant portion of this plant-derived organic carbon being processed by fungal communities prior to becoming SOM. Despite the central role of fungi in the processing of litter and root inputs, little is known about the relationship between fungal community composition and the relative conversion of aboveground litter versus root inputs into SOM. The Detrital Input and Removal Treatment (DIRT) experiments offer a system in which to test such questions, wherein aboveground litter and root inputs to forest soils are chronically excluded independently and in combination. In this study, we characterized fungal biomass (ergosterol), community composition (ITS2 metabarcoding), and community assembly (via null modeling) under root and litter exclusion treatments in a northern temperate forest DIRT experiment, and we related fungal community parameters to soil carbon. Root, but not litter, presence significantly differentiated fungal community composition and drove a more stochastic community assembly. Roots were associated with higher fungal biomass, particularly that of ectomycorrhizal and saprotrophic fungi, and with higher soil carbon stocks. The resulting strong positive correlation between fungal biomass and soil carbon appeared to be driven by saprotroph biomass in particular. We suggest that fungal communities are important mediators of the conversion of above- and belowground plant inputs into SOM, and that characterizing their composition may aid in understanding the relative importance of these plant input sources to SOM.

We analyzed historical data from 1961-1965 for species occurrences of branchiobdellidans and their crayfish hosts throughout the Mountain Lake Region of southwestern Virginia, USA to quantify geographic variability in species composition and identify patterns in host and symbiont diversity. We collected contemporary census data of branchiobdellidan assemblages from the same region in 2011-2014 for intra-annual variation in symbiont abundance and species composition. We compared historical and contemporary records to assess the stability of geographic patterns in symbiont diversity over decadal timescales. Branchiobdellidan assemblages followed a hump-shaped relationship with Strahler stream order. Much of the geographic variation in symbiont species composition was explained by host species composition, despite low host fidelity in branchiobdellidans. There were strong seasonal cycles in branchiobdellidan abundance and species composition. A comparison of historical and contemporary records revealed little change in species distributions over 50 years. Thus, branchiobdellidan species composition changes predictably along habitat gradients, tracks variation in host composition, is repeatable across decadal timescales, and follow strong cyclic seasonal changes in total and relative abundances. These results suggest that complex but deterministic ecological processes drive symbiont population dynamics at multiple spatial and temporal scales.

Soil microbial carbon use efficiency (CUE) is a combination of growth and respiration, which may respond differently to climate change depending on physical protection of soil carbon (C) and its availability to microbes. In a mid-latitude hardwood forest in central Massachusetts, 27 years of soil warming (+5 °C) has resulted in C loss and altered soil organic matter (SOM) quality, yet the underlying mechanisms remain unclear. Here, we hypothesized that long-term warming reduces physical aggregate protection of SOM, microbial CUE, and its temperature sensitivity. Soil was separated into macroaggregate (250–2000 μm) and microaggregate (

Primary production is the fundamental source of energy to foodwebs and ecosystems, and is thus an important constraint on soil communities. This coupling is particularly evident in polar terrestrial ecosystems where biological diversity and activity is tightly constrained by edaphic gradients of productivity (e.g., soil moisture, organic carbon availability) and geochemical severity (e.g., pH, electrical conductivity). In the McMurdo Dry Valleys of Antarctica, environmental gradients determine numerous properties of soil communities and yet relatively few estimates of gross or net primary productivity (GPP, NPP) exist for this region. Here we describe a survey utilizing pulse amplitude modulation (PAM) fluorometry to estimate rates of GPP across a broad environmental gradient along with belowground microbial diversity and decomposition. PAM estimates of GPP ranged from an average of 0.27 μmol O2/m2/s in the most arid soils to an average of 6.97 μmol O2/m2/s in the most productive soils, the latter equivalent to 217 g C/m2/y in annual NPP assuming a 60 day growing season. A diversity index of four carbon-acquiring enzyme activities also increased with soil productivity, suggesting that the diversity of organic substrates in mesic environments may be an additional driver of microbial diversity. Overall, soil productivity was a stronger predictor of microbial diversity and enzymatic activity than any estimate of geochemical severity. These results highlight the fundamental role of environmental gradients to control community diversity and the dynamics of ecosystem-scale carbon pools in arid systems.

Communities of symbiotic microbes obtained from the environment are an integral component of animal fitness and ecology. Thus a general and practical understanding of the processes that drive microbiome assembly and structure are paramount to understanding animal ecology, health, and evolution. We conceptualized a series of ecological filters that operate at the environment, host, and host tissue levels during microbiome assembly and discuss key ecological processes that structure animal microbiomes at each level. We conducted a survey of crayfish across four sites within the contiguous range of the of stream-inhabiting crayfish Cambarus sciotensis in western Virginia, USA, to characterize multiscale variation in the crayfish microbiome. We also conducted an in situ experiment to assess local drivers of microbial diversity on the closely related Cambarus chasmodactylus. We used a combination of DNA fingerprinting and next-generation sequencing to characterize microbiome diversity and composition from crayfish carapaces and gills to identify key filters affecting microbiome structure. Field survey showed that local environment and host tissues interact to create patterns of microbial diversity and composition, but the strongest effects on microbial community structure were observed at the level of host tissue. Our field experiment confirmed strong effects of host tissue, and also showed that a metazoan ectosymbiont which feeds on biofilms (Annelida; Branchiobdellida) had significant effects on microbial composition of the host carapace. Crayfish carapaces were colonized by diverse and taxonomically even microbial communities that were similar to, and correlated with, microbial communities of the ambient environment. Conversely, crayfish gills were colonized by less diverse communities and dominated by two families of bacteria with potentially significant functional roles: Comamonadaceae and Chitinophagaceae. Our results suggest that microbial assembly of the carapace is driven by external biotic and abiotic processes, whereas assembly on the gills appears to be coupled to host biology that favors interactions with few specific taxa. Our work shows how multi-scale studies of symbiont community assembly provide valuable insights into how the animal microbiome is structured under conditions of natural complexity and help identify other symbiont taxa, i.e., the branchiobdellidans, that may further influence microbiome assembly and structure.

Edaphic factors such as pH, organic matter, and salinity are often the most significant drivers of diversity patterns in soil bacterial communities. Desert ecosystems in particular are model locations for examining such relationships as food web complexity is low and the soil environment is biogeochemically heterogeneous. Here, we present the findings from a 16S rRNA gene sequencing approach used to observe the differences in diversity and community composition among three divergent soil habitats of the McMurdo Dry Valleys, Antarctica. Results show that alpha diversity is significantly lowered in high pH soils, which contain higher proportions of the phyla Acidobacteria and Actinobacteria, while mesic soils with higher soil organic carbon (and ammonium) content contain high proportions of Nitrospira, a nitrite-oxidizing bacteria. Taxonomic community resolution also had a significant impact on our conclusions, as pH was the primary predictor of phylum-level diversity, while moisture was the most significant predictor of diversity at the genus level. Predictive power also increased with increasing taxonomic resolution, suggesting a potential increase in niche-based drivers of bacterial community composition at such levels.

Understanding controls over the distribution of soil bacteria is a fundamental step toward describing soil ecosystems, understanding their functional capabilities, and predicting their responses to environmental change. This study investigated the controls on the biomass, species richness, and community structure and composition of soil bacterial communities in the McMurdo Dry Valleys, Antarctica, at local and regional scales. The goals of the study were to describe the relationships between abiotic characteristics and soil bacteria in this unique, microbially dominated environment, and to test the scale dependence of these relationships in a low complexity ecosystem. Samples were collected from dry mineral soils associated with snow patches, which are a significant source of water in this desert environment, at six sites located in the major basins of the Taylor and Wright Valleys. Samples were analyzed for a suite of characteristics including soil moisture, pH, electrical conductivity, soil organic matter, major nutrients and ions, microbial biomass, 16 S rRNA gene richness, and bacterial community structure and composition. Snow patches created local biogeochemical gradients while inter-basin comparisons encompassed landscape scale gradients enabling comparisons of microbial controls at two distinct spatial scales. At the organic carbon rich, mesic, low elevation sites Acidobacteria and Actinobacteria were prevalent, while Firmicutes and Proteobacteria were dominant at the high elevation, low moisture and biomass sites. Microbial parameters were significantly related with soil water content and edaphic characteristics including soil pH, organic matter, and sulfate. However, the magnitude and even the direction of these relationships varied across basins and the application of mixed effects models revealed evidence of significant contextual effects at local and regional scales. The results highlight the importance of the geographic scale of sampling when determining the controls on soil microbial community characteristics.

Productivity-diversity theory has proven informative to many investigations seeking to understand drivers of spatial patterns in biotic communities and relationships between resource availability and community structure documented for a wide variety of taxa. For soil bacteria, availability of organic matter is one such resource known to influence diversity and community structure. Here we describe the influence of environmental gradients on soil bacterial communities of the McMurdo Dry Valleys, Antarctica, a model ecosystem that hosts simple, microbially-dominated foodwebs believed to be primarily structured by abiotic drivers such as water, organic matter, pH, and electrical conductivity. We sampled 48 locations exhibiting orders of magnitude ranges in primary production and soil geochemistry (pH and electrical conductivity) over local and regional scales. Our findings show that environmental gradients imposed by cryptogam productivity and regional variation in geochemistry influence the diversity and structure of soil bacterial communities. Responses of soil bacterial richness to carbon content illustrate a productivity-diversity relationship, while bacterial community structure primarily responds to soil pH and electrical conductivity. This diversity response to resource availability and a community structure response to environmental severity suggests a need for careful consideration of how microbial communities and associated functions may respond to shifting environmental conditions resulting from human activity and climate variability.

Microbial carbon use efficiency (CUE) is a critical regulator of soil organic matter dynamics and terrestrial carbon fluxes, with strong implications for soil biogeochemistry models. While ecologists increasingly appreciate the importance of CUE, its core concepts remain ambiguous: terminology is inconsistent and confusing, methods capture variable temporal and spatial scales, and the significance of many fundamental drivers remains inconclusive. Here we outline the processes underlying microbial efficiency and propose a conceptual framework that structures the definition of CUE according to increasingly broad temporal and spatial drivers where (1) CUE P reflects population-scale carbon use efficiency of microbes governed by species-specific metabolic and thermodynamic constraints, (2) CUE C defines community-scale microbial efficiency as gross biomass production per unit substrate taken up over short time scales, largely excluding recycling of microbial necromass and exudates, and (3) CUE E reflects the ecosystem-scale efficiency of net microbial biomass production (growth) per unit substrate taken up as iterative breakdown and recycling of microbial products occurs. CUEE integrates all internal and extracellular constraints on CUE and hence embodies an ecosystem perspective that fully captures all drivers of microbial biomass synthesis and decay. These three definitions are distinct yet complementary, capturing the capacity for carbon storage in microbial biomass across different ecological scales. By unifying the existing concepts and terminology underlying microbial efficiency, our framework enhances data interpretation and theoretical advances.