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Interactions between soil nitrogen (N) availability, fungal community composition, and soil organic matter (SOM) regulate soil carbon (C) dynamics in many forest ecosystems, but context dependency in these relationships has precluded general predictive theory. We found that ectomycorrhizal (ECM) fungi with peroxidases decreased with increasing inorganic N availability across a natural inorganic N gradient in northern temperate forests, whereas ligninolytic fungal saprotrophs exhibited no response. Lignin-derived SOM and soil C were negatively correlated with ECM fungi with peroxidases and were positively correlated with inorganic N availability, suggesting decay of lignin-derived SOM by these ECM fungi reduced soil C storage. The correlations we observed link SOM decay in temperate forests to tradeoffs in tree N nutrition and ECM composition, and we propose SOM varies along a single continuum across temperate and boreal ecosystems depending upon how tree allocation to functionally distinct ECM taxa and environmental stress covary with soil N availability.

Plants associating with mutualistic ectomycorrhizal (ECM) fungi may directly obtain nitrogen (N) bound in soil organic matter (N-SOM). However, the contribution of N-SOM to plant growth under field conditions remains poorly constrained. We tested the hypothesis that turnover in ECM communities along soil inorganic N gradients mediates a functional transition from plant reliance on N-SOM in low inorganic N soils, to primarily inorganic N uptake in inorganic N-rich condition soils. We quantified the δ 15 N of Q. rubra foliage and roots, organic and inorganic soil N pools, and used molecular sequencing to characterize ECM communities, morpho-traits associated with N-foraging, and a community aggregated sporocarp δ 15 N. In support of our hypothesis, we document the progressive enrichment of root and foliar δ 15 N with increasing soil inorganic N supply; green leaves ranged from − 5.95 to 0.16‰ as the supply of inorganic N increased. ECM communities inhabiting low inorganic N soils were dominated by the genus Cortinarius, and other fungi forming hyphal morphologies putatively involved in N-SOM acquisition; sporocarp estimates from these communities were enriched (+ 4‰), further supporting fungal N-SOM acquisition. In contrast, trees occurring in high inorganic N soils hosted distinct communities with morpho-traits associated with inorganic N acquisition and depleted sporocarps (+ 0.5‰). Together, our results are consistent with apparent tradeoffs in the foraging cost and contribution of N-SOM to plant growth and demonstrate linkages between ECM community composition, fungal N-foraging potential and foliar δ 15 N. The functional characteristics of ECM communities represent a mechanistic basis for flexibility in plant nutrient foraging strategies. We conclude that the contribution of N-SOM to plant growth is likely contingent on ECM community composition and local soil nutrient availability.

Fine root litter is a primary source of soil organic matter (SOM), which is a globally important pool of C that is responsive to climate change. We previously established that ~20 years of experimental nitrogen (N) deposition has slowed fine root decay and increased the storage of soil carbon (C; +18%) across a widespread northern hardwood forest ecosystem. However, the microbial mechanisms that have directly slowed fine root decay are unknown. Here, we show that experimental N deposition has decreased the relative abundance of Agaricales fungi (-31%) and increased that of partially ligninolytic Actinobacteria (+24%) on decaying fine roots. Moreover, experimental N deposition has increased the relative abundance of lignin-derived compounds residing in SOM (+53%), and this biochemical response is significantly related to shifts in both fungal and bacterial community composition. Specifically, the accumulation of lignin-derived compounds in SOM is negatively related to the relative abundance of ligninolytic Mycena and Kuehneromyces fungi, and positively related to Microbacteriaceae. Our findings suggest that by altering the composition of microbial communities on decaying fine roots such that their capacity for lignin degradation is reduced, experimental N deposition has slowed fine root litter decay, and increased the contribution of lignin-derived compounds from fine roots to SOM. The microbial responses we observed may explain widespread findings that anthropogenic N deposition increases soil C storage in terrestrial ecosystems. More broadly, our findings directly link composition to function in soil microbial communities, and implicate compositional shifts in mediating biogeochemical processes of global significance.

Atmospheric nitrogen (N) deposition has increased dramatically since preindustrial times and continues to increase across many regions of the Earth. In temperate forests, this agent of global change has increased soil carbon (C) storage, but the mechanisms underlying this response are not understood. One long‐standing hypothesis proposed to explain the accumulation of soil C proposes that higher inorganic N availability may suppress both the activity and abundance of fungi that decay lignin and other polyphenols in soil. In field studies, elevated rates of N deposition have reduced the activity of enzymes mediating lignin decay, but a decline in the abundance of lignolytic fungi has not been definitively documented to date. Here, we tested the hypothesis that elevated rates of anthropogenic N deposition reduce the abundance of lignolytic fungi. We conducted a field experiment in which we compared fungal communities colonizing low‐lignin, high‐lignin, and wood substrates in a northern hardwood forest that is part of a long‐term N deposition experiment. We reasoned that if lignolytic fungi decline under experimental N deposition, this effect should be most evident among fungi colonizing high‐lignin and wood substrates. Using molecular approaches, we provide evidence that anthropogenic N deposition reduces the relative abundance of lignolytic fungi on both wood and a high‐lignin substrate. Furthermore, experimental N deposition increased total fungal abundance on a low‐lignin substrate, reduced fungal abundance on wood, and had no significant effect on fungal abundance on a high‐lignin substrate. We simultaneously examined these responses in the surrounding soil and forest floor, in which we did not observe significant reductions in the relative abundance of lignolytic fungi or in the size of the fungal community; however, we did detect a change in community composition in the forest floor that appears to be driven by a shift away from lignolytic fungi and towards cellulolytic fungi. Our results provide direct evidence that reductions in the abundance of lignolytic fungi are part of the mechanism by which anthropogenic N deposition increases soil C storage.

Terrestrial ecosystems in the Northern Hemisphere are a globally important sink for anthropogenic CO2 in the Earth's atmosphere, slowing its accumulation as well as the pace of climate warming. With the use of a long-term field experiment (ca. 20 yr), we show that the expression of fungal class II peroxidase genes, which encode enzymes mediating the rate-limiting step of organic matter decay, are significantly downregulated (-60 to -80%) because of increases in anthropogenic N deposition; this response was consistent with a decline in extracellular peroxidase enzyme activity in soil, the slowing of organic-matter decay, and greater soil C storage. The reduction in peroxidase expression we document here occurred in the absence of a compositional shift in metabolically active fungi, indicating that an overall reduction in peroxidase expression underlies the slowing of decay and increases in soil C storage. This molecular mechanism has global implications for soil C storage and should be represented in coupled climate-biogeochemical models simulating the influence of enhanced terrestrial C storage on atmospheric CO2 and the future climate of an N-enriched Earth.

Riverine floodplains are ecologically and economically valuable ecosystems that are heavily threatened by anthropogenic stressors. Microbial communities in floodplain soils mediate critical biogeochemical processes, yet we understand little about the relationship between these communities and variation in hydrologic connectivity related to land management or topography. Here, we present metagenomic evidence that differences among microbial communities in three floodplain soils correspond to a long-term gradient of hydrologic connectivity. Specifically, all strictly anaerobic taxa and metabolic pathways were positively associated with increased hydrologic connectivity and flooding frequency. In contrast, most aerobic taxa and all strictly aerobic pathways were negatively related to hydrologic connectivity and flooding frequency. Furthermore, the genetic potential to metabolize organic compounds tended to decrease as hydrologic connectivity increased, which may reflect either the observed concomitant decline of soil organic matter or the parallel increase in both anaerobic taxa and pathways. A decline in soil N, accompanied by an increased genetic potential for oligotrophic N acquisition subsystems, suggests that soil nutrients also shape microbial communities in these soils. We conclude that differences among floodplain soil microbial communities can be conceptualized along a gradient of hydrologic connectivity. Additionally, we show that these differences are likely due to connectivity-related variation in flooding frequency, soil organic matter, and soil N. Our findings are particularly relevant to the restoration and management of microbially mediated biogeochemical processes in riverine floodplain wetlands.

The extent to which ectomycorrhizal (ECM) fungi enable plants to access organic nitrogen (N) bound in soil organic matter (SOM) and transfer this growth-limiting nutrient to their plant host, has important implications for our understanding of plant-fungal interactions, and the cycling and storage of carbon (C) and N in terrestrial ecosystems. Empirical evidence currently supports a range of perspectives, suggesting that ECM vary in their ability to provide their host with N bound in SOM, and that this capacity can both positively and negatively influence soil C storage. To help resolve the multiplicity of observations, we gathered a group of researchers to explore the role of ECM fungi in soil C dynamics, and propose new directions that hold promise to resolve competing hypotheses and contrasting observations. In this Viewpoint, we summarize these deliberations and identify areas of inquiry that hold promise for increasing our understanding of these fundamental and widespread plant symbionts and their role in ecosystem-level biogeochemistry.

Here, we present evidence that ca. 20 years of experimental N deposition altered the composition of lignin-decaying class II peroxidases expressed by forest floor fungi, a response which has occurred concurrently with reductions in plant litter decomposition and a rapid accumulation of soil organic matter. This finding suggests that anthropogenic N deposition has induced changes in the biological mediation of lignin decay, the rate limiting step in plant litter decomposition. Thus, an altered composition of transcripts for a critical gene that is associated with terrestrial C cycling may explain the increased soil C storage under long-term increases in anthropogenic N deposition. IMPORTANCE Fungal class II peroxidases are enzymes that mediate the rate-limiting step in the decomposition of plant material, which involves the oxidation of lignin and other polyphenols. In field experiments, anthropogenic N deposition has increased soil C storage in forests, a result which could potentially arise from anthropogenic N-induced changes in the composition of class II peroxidases expressed by the fungal community. In this study, we have gained unique insight into how anthropogenic N deposition, a widespread agent of global change, affects the expression of a functional gene encoding an enzyme that plays a critical role in a biologically mediated ecosystem process.

Predicting the impact of environmental change on soil microbial functions requires an understanding of how environmental factors shape microbial composition. Here, we investigated the influence of environmental factors on bacterial and fungal communities across an expanse of northern hardwood forest in Michigan, USA, which spans a 500-km regional climate gradient. We quantified soil microbial community composition using high-throughput DNA sequencing on coextracted rDNA (i.e. total community) and rRNA (i.e. active community). Within both bacteria and fungi, total and active communities were compositionally distinct from one another across the regional gradient (bacteria P = 0.01; fungi P < 0.01). Taxonomically, the active community was a subset of the total community. Compositional differences between total and active communities reflected changes in the relative abundance of dominant taxa. The composition of both the total and active microbial communities varied by site across the gradient (P < 0.01) and was shaped by differences in soil moisture, pH, SOM carboxyl content, as well as C and N concentration. Our study highlights the importance of distinguishing between metabolically active microorganisms and the total community, and emphasizes that the same environmental factors shape the total and active communities of bacteria and fungi in this ecosystem.