Parallel yet asymmetric community assembly patterns of phyllosphere fungi and bacteria in subtropical forests

Abstract

As an important component of forest biodiversity, the phyllosphere microbiome plays an essential role in maintaining forest health, nutrient cycling, and plant resilience. However, the assembly and maintenance of its high community diversity remain poorly understood. In this study, we employed high-throughput sequencing to investigate the microbial communities associated with 61 phyllosphere samples from 12 dominant tree species and 25 samples from rare and occasional species in the subtropical forests of Mt. Huangshan, a key biodiversity hotspot in China. We first assessed the diversity of bacterial and fungal communities and explored their relationships with surrounding plant diversity, host functional traits, and topographic factors. We then quantified the ecological processes shaping phyllosphere microbial community assembly and identified biotic and abiotic factors that potentially regulate these dynamics. The results indicate that bacterial and fungal communities are governed predominantly by homogeneous selection. Specifically, the maintenance of bacterial diversity is driven mainly by plant community diversity, whereas fungal diversity responds more strongly to host traits (e.g., leaf C:N and pH). Moreover, fungal assembly is further constrained by dispersal limitation; accordingly, environmental selection accounts for a much smaller variation explanation rate in fungal diversity than in bacterial diversity. These results suggest that phyllosphere microbial diversity and its assembly processes are tightly linked to forest structural complexity and landscape heterogeneity. Finally, Mantel test results suggest that the homogeneous selection acting on bacterial communities assembly may be weaker through the mediating effects of fungal diversity, topographic factors, and host chemical traits. In contrast, bacterial diversity can directly reverse fungal community assembly from being controlled by selection to a neutral process. This study provides new insight into phyllosphere fungi-bacteria interactions, contributing to a deeper understanding of aboveground biodiversity maintenance mechanisms in subtropical forests.