Bacterial community complexity in the phyllosphere penalises specialists over generalists

The leaf surface, i.e. the phylloplane, is an oligotrophic and heterogeneous environment due to its topography and uneven distribution of resources. Despite being a limiting environment, leaves host bacteria that are abundant and establish spatially-structured communities. However, factors that drive spatial distribution patterns are not well understood. Since leaf-associated bacteria can have beneficial effects to their host, understanding the rules of the community assembly can lead to novel strategies for crop protection. To investigate changes in population density and spatial distribution of bacteria in synthetic communities, we examined the behaviour of two prevalent bacterial groups in the Arabidopsis thaliana leaf microbiota: Methylobacterium spp. (specialists) and Sphingomonas spp. (generalists). We designed synthetic communities composed of two (S2) or three strains (S3) in a full factorial design and tested whether density and spatial structure of communities in S3 can be explained by pairwise comparisons in S2. Our results showed that specialists are more susceptible to changes in population densities and spatial distribution patterns than generalists, with lower densities and aggregation patterns when a specialist is in S3 than in S2. Additionally, pairwise comparisons were not sufficient to explain the observed patterns in S3, suggesting that higher-order interactions play a role in the resulting structure of complex communities at the micrometre scale.