Fungal community structure and function shifts with atmospheric nitrogen deposition.

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.

Unimodal productivity-diversity relationships among bacterial communities in a simple polar soil ecosystem.

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.

Limiting Resources Define the Global Pattern of Soil Microbial Carbon Use Efficiency.

Microbial carbon (C) use efficiency (CUE) delineates the proportion of organic C used by microorganisms for anabolism and ultimately influences the amount of C sequestered in soils. However, the key factors controlling CUE remain enigmatic, leading to considerable uncertainty in understanding soil C retention and predicting its responses to global change factors. Here, we investigate the global patterns of CUE estimate by stoichiometric modeling in surface soils of natural ecosystems, and examine its associations with temperature, precipitation, plant-derived C and soil nutrient availability. We found that CUE is determined by the most limiting resource among these four basic environmental resources within specific climate zones (i.e., tropical, temperate, arid, and cold zones). Higher CUE is common in arid and cold zones and corresponds to limitations in temperature, water, and plant-derived C input, while lower CUE is observed in tropical and temperate zones with widespread limitation of nutrients (e.g., nitrogen or phosphorus) in soil. The contrasting resource limitations among climate zones led to an apparent increase in CUE with increasing latitude. The resource-specific dependence of CUE implies that soils in high latitudes with arid and cold environments may retain less organic C in the future, as warming and increased precipitation can reduce CUE. In contrast, oligotrophic soils in low latitudes may increase organic C retention, as CUE could be increased with concurrent anthropogenic nutrient inputs. The findings underscore the importance of resource limitations for CUE and suggest asymmetric responses of organic C retention in soils across latitudes to global change factors.

Fast-decaying plant litter enhances soil carbon in temperate forests but not through microbial physiological traits.

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.

Primary productivity as a control over soil microbial diversity along environmental gradients in a polar desert ecosystem.

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.

Bacterial community composition of divergent soil habitats in a polar desert.

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.

Factors Controlling Soil Microbial Biomass and Bacterial Diversity and Community Composition in a Cold Desert Ecosystem: Role of Geographic Scale.

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.