Linking tree leaf bacterial communities with plant traits and productivity in a tree biodiversity experiment

Background/Question/Methods: A multitude of trees surfaces are colonized by microorganisms that have important effects on their plant host’s fitness and survival. In the rhizosphere, these host-microbe interactions have been intensively studied because of their key role in host productivity. Less is known about the ecological factors driving community assembly in tree leaf microbial communities. We address this lack of knowledge using high-throughput sequencing of the leaf (phyllosphere) bacterial communities of a high-density tree diversity experiment that varied community composition along a gradient of functional trait diversity. We ask two questions: 1) what is the relative influence of host species identity, neighbor species identity, host functional trait diversity and host species richness on leaf bacterial community structure?; and 2) what is the relationship between leaf bacterial diversity and tree productivity? The experiment is located at the IDENT site in Sainte-Anne-de-Bellevue, Québec, Canada. The tree species pool consisted of 12 North American species (five broadleaf, seven conifers) as well as seven exotic species (three broadleaf, and four conifers). Plots diversity levels included monocultures of all species, 14 combinations of two-species mixtures, eighteen combinations of four-species mixtures and three mixtures including 12 species. Each community was replicated four times in a randomized block design.

Results/Conclusions: Host species identity, plot treatment, species-plot interaction, exotic origin, and neighbor identity were all significant drivers of leaf bacterial community structure. As demonstrated in previous studies of natural forest, host species identity was the strongest driver of leaf bacterial community structure. The effect of neighbor tree relative abundance on leaf community structure suggests that although the host species possesses mechanisms to select its leaf microbiome, the biotic environment surrounding a tree also impacts community structure. Through structural equation modeling, we demonstrate that tree productivity (estimated by tree biomass and volume) is significantly correlated with the alpha diversity of leaf bacterial communities, host tree functional traits, and plot tree taxonomic and functional diversity. Tree functional traits and plot-level taxonomic diversity indirectly affected tree productivity through leaf bacterial community alpha diversity. These findings reveal the importance of the biotic environment in driving the leaf microbiome, strengthening our understanding of tree leaf communities’ dynamics. In the context of studying the effects of biodiversity on ecosystem functioning (BEF), our results suggest that, in parallel with host functional traits and taxonomic diversity, leaf bacterial communities play a role in driving tree productivity.