Fine-Scale Adaptations to Environmental Variation and Growth Strategies Drive Phyllosphere Diversity.

is a prevalent bacterial genus of the phyllosphere. Despite its ubiquity, little is known about the extent to which its diversity reflects neutral processes like migration and drift, versus environmental filtering of life history strategies and adaptations. In two temperate forests, we investigated how phylogenetic diversity within is structured by biogeography, seasonality, and growth strategies. Using deep, culture-independent barcoded marker gene sequencing coupled with culture-based approaches, we uncovered a considerable diversity of in the phyllosphere. We cultured different subsets of lineages depending upon the temperature of isolation and growth (20°C or 30°C), suggesting long-term adaptation to temperature. To a lesser extent than temperature adaptation, diversity was also structured across large (>100 km; between forests) and small (<1.2 km; within forests) geographical scales, among host tree species, and was dynamic over seasons. By measuring the growth of 79 isolates during different temperature treatments, we observed contrasting growth performances, with strong lineage- and season-dependent variations in growth strategies. Finally, we documented a progressive replacement of lineages with a high-yield growth strategy typical of cooperative, structured communities in favor of those characterized by rapid growth, resulting in convergence and homogenization of community structure at the end of the growing season. Together, our results show how is phylogenetically structured into lineages with distinct growth strategies, which helps explain their differential abundance across regions, host tree species, and time. This work paves the way for further investigation of adaptive strategies and traits within a ubiquitous phyllosphere genus. is a bacterial group tied to plants. Despite the ubiquity of methylobacteria and the importance to their hosts, little is known about the processes driving community dynamics. By combining traditional culture-dependent and -independent (metabarcoding) approaches, we monitored diversity in two temperate forests over a growing season. On the surface of tree leaves, we discovered remarkably diverse and dynamic communities over short temporal (from June to October) and spatial (within 1.2 km) scales. Because we cultured different subsets of diversity depending on the temperature of incubation, we suspected that these dynamics partly reflected climatic adaptation. By culturing strains under laboratory conditions mimicking seasonal variations, we found that diversity and environmental variations were indeed good predictors of growth performances. Our findings suggest that community dynamics at the surface of tree leaves results from the succession of strains with contrasting growth strategies in response to environmental variations.