Differential responses of saprotrophic and ectomycorrhizal fungi explain N enrichment effects on decay

Background/Question/Methods

Nitrogen (N) fertilization frequently changes the biochemistry of decomposition in ecosystems. In low N systems, fertilization with mineral N can increase cellulose decomposition, reduce lignin decay and the activity of lignin-degrading enzymes, and alter the community composition of decomposers. Nevertheless, it is unclear which groups of decomposers are responsible for changes in biochemical decay processes under N fertilization and how shifts in decomposer physiology may account for these changes. We addressed this issue by studying the community structure and function of fungi on decomposing litter of a model plant system, Arabidopsis thaliana for one year in control and N-fertilized plots in an Alaskan boreal forest. We measured fungal communities on the litters collected from the field with high-throughput sequencing, then assessed function of individual taxa by re-sequencing the fungal communities after incubation of decomposed litter with pure substrates. We then categorized OTUs as ectomycorrhizal or saprotrophic based on current knowledge of metabolic lifestyle of the BLAST matches for each individual taxa. We hypothesized that 1) N fertilization increases cellulose decay by selecting for cellulolytic-saprotrophic fungi that compete well for N and 2) N fertilization reduces lignin decay when ligninolytic-saprotrophs or peroxidase-producing, protein-degrading ectomycorrhizal fungi are outcompeted by cellulolytic-saprotrophs.

Results/Conclusions

N fertilization caused a shift in decomposer community composition (P = 0.021) that coincided with increased cellulose loss from litter (P = 0.0382) and reduced lignin losses (P = 0.0528), suggesting that cellulose degraders were competitively dominant under high N availability. No shifts in the relative abundances of saprotrophic or ectomycorrhizal functional guilds were observed. Instead, changes in community composition were associated with shifts in specific taxa with unique functional profiles. After 2 months of decay, changes in the abundance of saprotrophs under N fertilization were negatively associated with the ability to degrade sucrose (P = 0.017) and marginally positively associated with glycine uptake (P = 0.077). There were no detectable shifts in the community composition of saprotrophs with different functional profiles under N fertilization after one year of decay. Instead, ectomycorrhizal fungi that decomposed glycine increased in abundance under N fertilization (P = 0.012), while ectomycorrhizal fungi that degraded pure lignin declined under N fertilization (P = 0.008). These results challenge the conventional view that declines in lignin decomposition and oxidative enzyme activity under N fertilization result from shifts in saprotrophic fungal abundance and support the emerging view that ectomycorrhizal fungi are important regulators of the slow carbon cycle in soil.