Microbial functional traits in phyllosphere are more sensitive to anthropogenic disturbance than in soil

Soil-plant microbiome plays a critical role in the regulation of terrestrial ecosystem function and service, including biogeochemical cycling and primary production. The lack of knowledge regarding the differences in microbial functional traits, i.e. the functional genes related to carbon (C), nitrogen (N), phosphorus (P) and sulfur (S) cycles, between soil and plant microbiomes hampers our prediction of the terrestrial nutrient cycling processes under the pressure of anthropogenic disturbance. Herein, a quantitative microbial element cycling (QMEC) method and amplicon sequencing was employed to characterize CNPS cycling genes and microbial communities in soil and plant samples collected from peri-urban farmland with high anthropogenic disturbance and forest ecosystem with minimal disturbance. The soil-plant system harbored a diverse array of CNPS cycling genes, which were significantly more abundant in soil than in phyllosphere. The overall CNPS gene profiles in farmland samples was distinct from that of forest samples in both soil and plant phyllosphere. Farmland samples had a lower abundance of CNPS cycling genes than forest samples, indicating that intensive agricultural management practices may consequently compromise the biogeochemical cycling potential of nutrients. Significant positive correlations between the abundance of CNPS cycling genes and microbial diversity were observed in phyllosphere microbiome but not in soil, suggesting that the functional redundancy in soil microbiome may be higher than that of phyllosphere microbiome. Taken together, we provide experimental evidence for the substantial impacts of anthropogenic disturbance on CNPS cycling genes in the soil-plant system and necessitate future efforts to unravel the plant microbiome diversity and functionality under the pressure of global changes.