Nitrogen (N) deposition has enhanced the ability of trees to capture atmospheric carbon (C). The effect of elevated N on belowground C cycling, however, is variable and response mechanisms are largely unknown. Recent research has highlighted distinct differences between ectomycorrhizal (ECM) and arbuscular mycorrhizal (AM) trees in the strength of root-microbial interactions. In particular, ECM trees send more C to rhizosphere microbes to stimulate enzyme activity and nutrient mobilization than AM trees, which primarily rely on saprotrophic microbes to mobilize N. As such, we hypothesized that N fertilization would weaken root-microbial interactions and soil decomposition in ECM stands more than in AM stands. To test this hypothesis, we measured root-microbial interactions in ECM and AM plots in two long-term N fertilization studies, the Fernow Experimental Forest, WV and Bear Brook Watershed, ME. We measured the activity of hydrolytic and oxidative enzymes, and examined the bacterial and fungal metagenome and metatranscriptome in rhizosphere, bulk, and organic horizons. We then linked these to assays of plant-C investment belowground including fine root responses, mycorrhizal colonization, and root exudation.
Our results indicate that N fertilization decreased fine root biomass, root branching, root exudation, and mycorrhizal colonization in both mycorrhizal types with the greatest declines occurring in ECM stands. As ECM roots are tightly coupled to the soil microbiome through energy and nutrient exchange, these declines in belowground C allocation were mirrored by shifts in both fungal and bacterial community structure and function. In contrast, as the AM soil microbiome is less reliant on trees for carbon and are more adapted to high inorganic nutrient environments, the soil metagenome and transcriptome were more resilient to decreases in belowground C allocation. As such, we observed greater declines in fungal gene expression in ECM stands, which was accompanied by larger reductions in fungal-derived lignolytic and hydrolytic enzyme activity. Collectively, our results indicate the N fertilization decoupled root-microbial interactions by reducing belowground carbon allocation in ECM stands. Thus, N fertilization may reduce soil turnover and increase soil C storage to a greater extent in forests dominated by ECM than AM trees.