From nature to urbanity: exploring phyllosphere microbiome and functional gene responses to the Anthropocene

The Anthropocene exerts various pressures and influences on the stability and function of the Earth's ecosystems. However, our understanding of how the microbiome responds in form and function to these disturbances is still limited, particularly when considering the phyllosphere, which represents one of the largest microbial reservoirs in the terrestrial ecosystem. In this study, we comprehensively characterized tree phyllosphere bacteria and associated nutrient-cycling genes in natural, rural, suburban, and urban habitats in China. Results revealed that phyllosphere bacterial community diversity, richness, stability, and composition heterogeneity were greatest at the most disturbed sites. Stochastic processes primarily governed the assembly of phyllosphere bacterial communities, although the role of deterministic processes (environmental selection) in shaping these communities gradually increased as we moved from rural to urban sites. Our findings also suggest that human disturbance is associated with the reduced influence of drift as increasingly layered environmental filters deterministically constrain phyllosphere bacterial communities. The intensification of human activity was mirrored in changes in functional gene expression within the phyllosphere microbiome, resulting in enhanced gene abundance, diversity, and compositional variation in highly human-driven disturbed environments. Furthermore, we found that while the relative proportion of core microbial taxa decreased in disturbed habitats, a core set of microbial taxa shaped the distributional characteristics of both microbiomes and functional genes at all levels of disturbance. In sum, this study offers valuable insights into how anthropogenic disturbance may influence phyllosphere microbial dynamics and improves our understanding of the intricate relationship between environmental stressors, microbial communities, and plant function within the Anthropocene.