Host-microbial taxonomic associations have been reported in a range of natural systems, but the adaptive mechanisms driving these associations remain relatively unknown, especially for plants and their leaf (phyllosphere) bacterial communities. In addressing the mechanisms behind these associations, plant functional traits have been targeted as a potential proxy for explaining bacterial community turnover among plant species, since plant trait values largely determine the resource availability, micro-environmental conditions, and habitat quality experienced by phyllosphere bacteria. However, the microbial traits that mediate adaptation to the host environment, and how host and symbiont traits associate through time and space remain hypothetical. We used metagenomic sequencing and functional annotation of bacterial communities from the phyllosphere of 17 tree species in a tropical forest on Barro Colorado Island to assess the functional composition of phyllosphere microbial communities. Using whole-organism and leaf functional trait measurements on these tree species, we then determined which bacterial and plant functions drove microbial community turnover among the different species of trees.
Results/Conclusions
Microbial functions linked to carbohydrate metabolism, amino acid metabolism, energy metabolism and environmental information processing appear to be the most important for mediating bacterial adaptation to the phyllosphere of tropical trees. Tree host traits including height at maturity and leaf potassium and phosphorus content were the most strongly associated with functional turnover in microbial communities. More specifically, the ability to degrade antimicrobial volatiles emitted by the plant (e.g. limonene and pinene), to respond and coordinate response to environmental change (e.g. via two-component systems and quorum sensing) and to fuel metabolism (e.g. oxidative phosphorylation and photosynthesis) were the main axes of microbial adaptation to variation in plant traits. Bacterial members of most communities were more functionally similar than expected by chance, suggesting strong environmental filtering by the host leaves. Overall, our results demonstrate a cross-species adaptive coupling between plants and their phyllosphere microbes based on a community-level assessment of functions at both the host and the microbial levels, with implications for our understanding of the evolutionary emergence of co-adaptive associations in plants and their symbionts.