Environmental factors, bacterial interactions and plant traits jointly regulate epiphytic bacterial community composition of two alpine grassland species

Epiphytic microbes on the surfaces of leaves and roots can bring substantial benefits or damages to their plant hosts. Although various factors have been proposed for shaping the epiphytic microbial composition, the contributions of environment factors, endogenous microbial taxa interactions, host plant traits, and their interactive effects are poorly understood. Here, we conducted a field investigation along a precipitation gradient and collected leaf and root surface microbes of two alpine plant species for 16S rRNA sequencing. We found that epiphytic bacterial community composition significantly changed along the precipitation gradient through ordination analyses and permutational multivariate analysis of variance. Beneficial bacterial taxa from Caulobacteraceae, Sphingomonadaceae, Comamonadaceae and Rhizobiales were enriched in the high precipitation zones. The stress-tolerant Hymenobacteraceae, Micrococcaceae, and Geodermatophilaceae occurred more frequently in the phyllosphere, and the Thermoleophilia, Thermomicrobiales and Bacillales were enriched in the rhizosphere at the drier sites. Mean annual precipitation was the most important factor regulating the epiphytic bacterial community composition. The direct effect of climate on bacterial community composition was higher in the phyllosphere than in the rhizosphere where joint effects of climate, plant traits and soil properties predominated. Distinct leaf trichome cover and plant height clearly explained the host effect on the phyllosphere bacterial community composition while belowground traits did not explain the host effect well on the rhizosphere bacterial community composition. We detected a significant role of bacterial taxa interactions in shaping microbial communities, where greater negative taxa interactions led to lesser composition changes. Structural equation modeling showed that environmental factors and bacterial interactions substantially contributed to the variation in epiphytic community composition, followed by host plant traits. This study advances our understanding of complex factors affecting alpine epiphytic community assembly and further confirms the role of biotic interactions.