Although we understand the ecological processes eliciting changes in plant community composition during secondary succession, we do not understand whether co-occurring changes in plant detritus shape saprotrophic microbial communities in soil. In this study, we investigated soil microbial composition and function across an old-field chronosequence ranging from 16 to 86 years following agricultural abandonment, as well as three forests representing potential late-successional ecosystems. Fungal and bacterial community composition was quantified from ribosomal DNA, and insight into the functional potential of the microbial community to decay plant litter was gained from shotgun metagenomics and extracellular enzyme assays. Accumulation of soil organic matter across the chronosequence exerted a positive and significant effect on fungal phylogenetic β-diversity and the activity of extracellular enzymes with lignocellulolytic activity. In addition, the increasing abundance of lignin-rich C4 grasses was positively related to the composition of fungal genes with lignocellulolytic function, thereby linking plant community composition, litter biochemistry, and microbial community function. However, edaphic properties were the primary agent shaping bacterial communities, as bacterial β-diversity and variation in functional gene composition displayed a significant and positive relationship to soil pH across the chronosequence. The late-successional forests were compositionally distinct from the oldest old fields, indicating that substantial changes occur in soil microbial communities as old fields give way to forests. Taken together, our observations demonstrate that plants govern the turnover of soil fungal communities and functional characteristics during secondary succession, due to the continual input of detritus and differences in litter biochemistry among plant species.

It is commonly assumed that microbial communities are structured by "bottom-up" ecological forces, although few experimental manipulations have rigorously tested the mechanisms by which resources structure soil communities. We investigated how plant substrate availability might structure fungal communities and belowground processes along an experimental plant richness gradient in a grassland ecosystem. We hypothesized that variation in total plant-derived substrate inputs, plant functional group diversity, as well as the relative abundance of C grasses and legumes would modulate fungal α- and β-diversity and their rates of soil carbon (C) and nitrogen (N) cycling. To test these predictions, we molecularly characterized fungal communities, as well as potential extracellular enzyme activity, net N mineralization, and soil organic matter respiration. We found higher fungal richness was associated with increasing aboveground plant biomass; whereas, fungal β-diversity was explained by contributions from C grass and legume relative dominance, plant functional group diversity, as well as plant biomass. Furthermore, aboveground plant biomass consistently shaped the richness and composition of individual fungal trophic modes (i.e., saprotrophs, symbiotrophs, pathotrophs). Finally, variation in extracellular enzyme activity, net N mineralization rates, and soil organic matter respiration was significantly explained by fungal β-diversity when fungi were functionally classified. Via changes in the supply and composition of organic substrates entering soil, our study demonstrates that changes in the plant species richness and functional composition collectively influence fungal communities and rates of soil C and N cycling.

Priority effects are an important ecological force shaping biotic communities and ecosystem processes, in which the establishment of early colonists alters the colonization success of later-arriving organisms via competitive exclusion and habitat modification. However, we do not understand which biotic and abiotic conditions lead to strong priority effects and lasting historical contingencies. Using saprotrophic fungi in a model leaf decomposition system, we investigated whether compositional and functional consequences of initial colonization were dependent on initial colonizer traits, resource availability or a combination thereof. To test these ideas, we factorially manipulated leaf litter biochemistry and initial fungal colonist identity, quantifying subsequent community composition, using neutral genetic markers, and community functional characteristics, including enzyme potential and leaf decay rates. During the first 3 months, initial colonist respiration rate and physiological capacity to degrade plant detritus were significant determinants of fungal community composition and leaf decay, indicating that rapid growth and lignolytic potential of early colonists contributed to altered trajectories of community assembly. Further, initial colonization on oak leaves generated increasingly divergent trajectories of fungal community composition and enzyme potential, indicating stronger initial colonizer effects on energy-poor substrates. Together, these observations provide evidence that initial colonization effects, and subsequent consequences on litter decay, are dependent upon substrate biochemistry and physiological traits within a regional species pool. Because microbial decay of plant detritus is important to global C storage, our results demonstrate that understanding the mechanisms by which initial conditions alter priority effects during community assembly may be key to understanding the drivers of ecosystem-level processes.

Litter decomposition is an enzymatically-complex process that is mediated by a diverse assemblage of saprophytic microorganisms. It is a globally important biogeochemical process that can be suppressed by anthropogenic N deposition. In a northern hardwood forest ecosystem located in Michigan, USA, 20 years of experimentally increased atmospheric N deposition has reduced forest floor decay and increased soil C storage. Here, we paired extracellular enzyme assays with shotgun metagenomics to assess if anthropogenic N deposition has altered the functional potential of microbial communities inhabiting decaying forest floor. Experimental N deposition significantly reduced the activity of extracellular enzymes mediating plant cell wall decay, which occurred concurrently with changes in the relative abundance of metagenomic functional gene pathways mediating the metabolism of carbohydrates, aromatic compounds, as well as microbial respiration. Moreover, experimental N deposition increased the relative abundance of 50 of the 60 gene pathways, the majority of which were associated with saprotrophic bacteria. Conversely, the relative abundance and composition of fungal genes mediating the metabolism of plant litter was not affected by experimental N deposition. Future rates of atmospheric N deposition have favored saprotrophic soil bacteria, whereas the metabolic potential of saprotrophic fungi appears resilient to this agent of environmental change. Results presented here provide evidence that changes in the functional capacity of saprotrophic soil microorganisms mediate how anthropogenic N deposition increases C storage in soil.

Microbial communities in soil mediate biogeochemical processes; however, understanding forces shaping their composition and function remains a gap in our ecological knowledge. We investigated phylogenetic turnover and functional gene composition of saprotrophic fungi along a 4000-year glacial chronosequence. A direct relationship between β-diversity and geographic distance, a proxy for time since deglaciation, indicated that dispersal limitation shapes saprotrophic fungal communities. Further, we infer that dispersal limitation may also influence fungal functional properties as metabolic potential and functional richness increased with site age. Despite attempts to minimize environmental variation, a direct relationship between β-diversity and biogeochemical differences across sites indicated that environmental filtering further shapes fungal community composition. However, environmental filtering was overshadowed by the effect of dispersal limitation when tested by multiple regression. Fungal β-diversity and composition of functional genes involved in plant litter decay were unrelated, suggesting that functional traits are not phylogenetically conserved across this chronosequence. Our study suggests that dispersal limitation operates in structuring present-day fungal community composition and functional potential. Further, we demonstrate the need to integrate functional and phylogenetic approaches to more accurately portray microbial communities and their functional capacities.