Microbial mediators of plant community response to long-term N and P fertilization: Evidence of a role of plant responsiveness to mycorrhizal fungi

Climate changes and anthropogenic nutrient enrichment widely threaten plant diversity and ecosystem functions. Understanding the mechanisms governing plant species turnover across nutrient gradients is crucial to developing successful management and restoration strategies. We tested whether and how soil microbes, particularly arbuscular mycorrhizal fungi (AMF), could mediate plant community response to a 15 years long-term N (0, 4, 8, and 16 g N m^-2 year^-1 ) and P (0 and 8 g N m^-2 year^-1 ) enrichment in a grassland system. We found N and P enrichment resulted in plant community diversity decrease and composition change, in which perennial C₄ graminoids were dramatically reduced while annuals and perennial forbs increased. Metabarcoding analysis of soil fungal community showed that N and P changed fungal diversity and composition, of which only a cluster of AMF identified by the co-occurrence networks analysis was highly sensitive to P treatments and was negatively correlated with shifts in percentage cover of perennial C₄ graminoids. Moreover, by estimating the mycorrhizal responsiveness (MR) of 41 plant species in the field experiment from 264 independent tests, we found that the community weighted mean MR of the plant community was substantially reduced with nutrient enrichment and was positively correlated with C₄ graminoids percentage cover. Both analyses of covariance and structural equation modeling indicated that the shift in MR rather than AMF composition change was the primary predictor of the decline in perennial C₄ graminoids, suggesting that the energy cost invested by C₄ plants on those sensitive AMF might drive the inferior competitive abilities compared with other groups. Our results suggest that shifts in the competitive ability of mycorrhizal responsive plants can drive plant community change to anthropogenic eutrophication, suggesting a functional benefit of mycorrhizal mutualism in ecological restoration following climatic or anthropogenic degradation of soil communities.