Fungal Community Composition Regulates Fine Root Decay: Implications for the Cycling and Storage of Carbon in Terrestrial Ecosystems

Abstract

A central goal in ecology is to understand how the environment modifies the composition of ecological communities and, in turn, the functioning of ecosystems. Fine root litter accounts for half of plant litter production in forest ecosystems and is a primary source of soil organic matter. However, the ecological factors controlling the decay of fine root litter remain a critical gap in our understanding of the terrestrial carbon cycle and its responses to environmental change. Using experimental and observational approaches, I explored how microbial community composition influences the decay of fine root litter into soil organic matter in temperate forest ecosystems. First, I tested whether shifts in fungal and bacterial community composition have slowed fine root litter in a long-term (ca. 20 years) field experiment simulating future rates of anthropogenic atmospheric nitrogen deposition in northern hardwood forests. My work revealed that experimental nitrogen deposition reduced the relative abundance of saprotrophic Agaricomycete fungi that use peroxidase enzymes to fully oxidize lignin. In contrast, experimental nitrogen deposition favored Actinobacteria, which only partially decay lignin. Furthermore, molecular characterization using pyrolysis gas chromatography-mass spectrometry demonstrated that nitrogen deposition increased the abundance of lignin-derived compounds in soil organic matter. Previous studies have shown that anthropogenic nitrogen deposition slows fine root decay and enhances soil carbon storage – plausibly acting as a sink for anthropogenic carbon dioxide emissions – and my findings demonstrate that shifts in microbial community composition that slow the decay of lignin in fine root litter underlie these biogeochemical responses. Second, I explored how turnover in fungal community composition along a natural soil inorganic nitrogen gradient across northern temperate forests influences fine root decay and the accumulation of soil organic matter. I found that differences in the composition of fungal communities inhabiting decomposing fine root litter did not explain soil organic matter stocks and biochemistry across the soil nitrogen gradient. However, within the soil fungal community, the relative abundance of ectomycorrhizal fungi that have retained genes encoding peroxidase enzymes declined with increasing inorganic nitrogen availability. This response was correlated with an increase in lignin-derived soil organic matter and overall soil carbon storage, suggesting that the decomposition of lignin-derived soil organic matter by certain symbiotic ectomycorrhizal fungi with peroxidase enzymes constrains soil organic matter accumulation across soil nitrogen gradients. Lastly, I used a field decay study with fine root litterbags to quantify the relative importance of environmental and fungal controls over fine root decay rates. I found that ligninolytic saprotrophs, ectomycorrhizal fungi with peroxidases, and their influence on community-level genetic potential for decay, better predict rates of fine root decay than environmental factors. Together, these findings provide evidence that microbial community composition and its responses to the environment regulate the decay of fine roots into soil organic matter. Thus, explicitly accounting for turnover in microbial community composition and its implications for community functioning may improve our ability to accurately predict terrestrial carbon cycling and its responses to environmental change.