Richness and composition of phyllosphere Methylobacterium communities cause variation in Arabidopsis thaliana growth

The phyllosphere – the aerial parts of plants – forms a vast microbial habitat that harbors diverse bacterial communities playing key roles in ecosystem function. The foliar surface is thus a promising study system to investigate biodiversity-ecosystem function relationships. Researchers have found a positive correlation between leaf bacterial diversity and ecosystem productivity, but the causality of this relationship has yet to be demonstrated. To understand how the diversity and composition of phyllosphere bacterial communities could cause variation in the growth of their host plants, we assembled synthetic communities composed of different diversity and compositions of Methylobacterium strains – a plant growth-promoting bacterial genus ubiquitous in the phyllosphere – that we inoculated on Arabidopsis thaliana grown in gnotobiotic conditions. We hypothesized that (1) increasing Methylobacterium diversity should cause an increase in host growth; (2) strains should differ in their impact on host growth; and (3) the relationship between bacterial diversity and plant productivity should be strain-dependent. Our results supported our three hypotheses but revealed unpredicted patterns in how A. thaliana leaf biomass varied according to inoculated Methylobacterium strain richness and identity. Increasing bacterial richness induced a higher host leaf biomass, but only after an initial reduction in biomass, suggesting competition alleviation by multispecies interactions. Two Methylobacterium strains showed beneficial effects on A. thaliana growth, and one strain was detrimental for the plant. Community composition shaped the relationship between diversity and productivity, highlighting the importance of community mutualistic and antagonistic interactions. Furthermore, niche complementarity was likely the main ecological mechanism driving the diversity-productivity relationship in our study system. By demonstrating the causal effects of Methylobacterium community diversity and composition on host plant growth, our experiment shed light on the importance of phyllosphere bacteria in terrestrial ecosystem functioning.