Successional dynamics of the emerging bacterial leaf phyllosphere in spring

Every year, deciduous trees shed their leaves. As leaves emerge next spring they eventually establish a characteristic bacterial leaf community. The plant phyllosphere generally refers to the microbial habitat associated with the aboveground parts of the plant, which consists of multiple niches. We studied the bacterial phyllosphere of eight London plane trees (Platanus x acerifolia) in two different cities by sampling them every week, throughout spring. Besides the leaf surface, we sampled the surfaces of the leaf buds, branch, and trunk as well. Using 16S rRNA gene amplicon sequencing, we found that phyllosphere community variation was most strongly determined by the sampled phyllosphere niche , with only the communities on the emerging leaves showing changing dynamics over time. The change in leaf community composition was very high following leaf emergence, with decreasing speed over time. This indicates the communities stabilize over time and implies a deterministic trend. However, the different individual trees had leaf communities that developed towards different stable states. We also identified different co-occurring groups of bacteria associated with different stages of colonization in the leaf niche and accordingly named them general cluster, early cluster, mid cluster, and mid-late cluster. The mid-late cluster was most pronounced in trees next to busy streets, compared to trees in green parks, at the cost of the general cluster. Furthermore, we observed that especially the general cluster shared bacterial taxa/ASVs with the other phyllosphere niches, and between different trees. These observations also imply that the woody tree phyllosphere contributes to the leaf community, as new leaves emerge in spring. Our study contributes to a better understanding of the development of the leaf phyllosphere and the relation between different tree phyllosphere niches and their bacterial inhabitants. Additionally, this study managed to unravel the ecological succession in the emerging leaf phyllosphere of London plane trees, including how it is impacted by urban land use.