Litter decomposition is a globally important and enzymatically-complex biogeochemical process. It is mediated by a diverse assemblage of saprophytic microorganisms, and can be suppressed by anthropogenic N deposition. In a northern hardwood forest ecosystem in Michigan, USA, twenty years of experimentally increased N deposition has reduced forest floor decay, as well as increased soil C storage and dissolved organic carbon leaching. This ecosystem-level response occurred concomitantly with reduced soil respiration, microbial biomass, and fungal laccase gene expression. Here, we paired extracellular enzyme assays with high-throughput sequencing of co-extracted DNA and RNA from decaying leaf litter to determine if experimental atmospheric N deposition has lowered the diversity and altered the composition of whole communities of fungi (i.e., DNA-based) and well as its active members (i.e., RNA-based). Further, shotgun metagenomes were generated and probed against manually curated functional gene databases to gain insight into whether experimental N deposition altered the metabolic capacity of the soil fungal community to decay lignocellulose.
Experimental N deposition reduced lignocellulolytic enzyme activity and changed the phylogenetic composition of the active fungal community inhabiting decaying forest floor, providing indirect evidence that compositional shifts elicited a functional response in our long-term field experiment. The activity of extracellular enzymes mediating plant litter and humus decay, cellobiohydrolase and peroxidase, were ~50% lower under experimental N deposition. The active fungal community was less diverse under experimental N deposition than in the ambient treatment (-6% change from ambient). Further, the active fungal community exhibited greater phylogenetic clustering under experimental N deposition (+91%), which suggests the “environmental filtering” of these functionally important organisms. However, neither the composition of the total (i.e., DNA based) fungal community, nor the abundance or composition of fungal lignocellulolytic genes from shotgun metagenomes were impacted by experimental N deposition. Results presented here provide evidence that compositional changes in the active saprotrophic soil fungal community may mediate how anthropogenic N deposition increases the storage of C in soil.