Abstract

BackgroundThe phyllosphere is an important microbial habitat, but our understanding of how plant hosts drive the composition of their associated leaf microbial communities and whether taxonomic associations between plants and phyllosphere microbes represent adaptive matching remains limited. In this study, we quantify bacterial functional diversity in the phyllosphere of 17 tree species in a diverse neotropical forest using metagenomic shotgun sequencing. We ask how hosts drive the functional composition of phyllosphere communities and their turnover across tree species, using host functional traits and phylogeny.ResultsNeotropical tree phyllosphere communities are dominated by functions related to the metabolism of carbohydrates, amino acids, and energy acquisition, along with environmental signalling pathways involved in membrane transport. While most functional variation was observed within communities, there is non-random assembly of microbial functions across host species possessing different leaf traits. Metabolic functions related to biosynthesis and degradation of secondary compounds, along with signal transduction and cell–cell adhesion, were particularly important in driving the match between microbial functions and host traits. These microbial functions were also evolutionarily conserved across the host phylogeny.ConclusionsFunctional profiling based on metagenomic shotgun sequencing offers evidence for the presence of a core functional microbiota across phyllosphere communities of neotropical trees. While functional turnover across phyllosphere communities is relatively small, the association between microbial functions and leaf trait gradients among host species supports a significant role for plant hosts as selective filters on phyllosphere community assembly. This interpretation is supported by the presence of phylogenetic signal for the microbial traits driving inter-community variation across the host phylogeny. Taken together, our results suggest that there is adaptive matching between phyllosphere microbes and their plant hosts.C8J94f4-7ASkUzZkyuU9TtVideo abstract.

Highlights

  • The phyllosphere is an important microbial habitat, but our understanding of how plant hosts drive the composition of their associated leaf microbial communities and whether taxonomic associations between plants and phyllosphere microbes represent adaptive matching remains limited

  • Metagenomic shotgun sequencing characterization of phyllosphere microbial functions Overall, we detected 4587 different functional genes across all samples based on the annotation of metagenomic shotgun sequencing of tropical tree phyllosphere communities

  • The principal metabolic functions in the phyllosphere were related to metabolism of amino acids, nucleotides, carbohydrates, and energy (e.g., oxidative phosphorylation & citric acid (TCA) cycle; Fig. 1)

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Summary

Introduction

The phyllosphere is an important microbial habitat, but our understanding of how plant hosts drive the composition of their associated leaf microbial communities and whether taxonomic associations between plants and phyllosphere microbes represent adaptive matching remains limited. The phyllosphere—the aerial surfaces of plants including leaves—is a widespread microbial habitat that hosts a diversity of microorganisms that play key roles in plant ecology and evolution [1]. Phyllosphere microbes play key roles in plant health [2, 3] and human health [4], and can influence ecosystem function [5]. At a broad taxonomic scale, phyllosphere bacterial communities are consistently dominated by taxa including Actinobacteria, Bacteroidetes, Firmicutes, and Proteobacteria [6], indicating that plants influence the composition of their microbial partners. Plants and associated bacteria show cophylogenetic associations, with clades of plants and bacteria consistently occurring together [9, 12, 13], suggesting close adaptive associations between plants and their phyllosphere microbes

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