Contrasting patterns of microbial dominance in the Arabidopsis thaliana phyllosphere

Pseudomonas and Sphingomonas are among the most abundant bacterial genera in the phyllosphere of wild Arabidopsis thaliana. Relative to Pseudomonas, the ecology of Sphingomonas and its interaction with plants remains elusive, despite its global ubiquity and known representatives of plant-beneficial strains. We analyzed the genomic features of over 400 endophytic Sphingomonas isolates collected from A. thaliana and neighboring plants, revealing high intergenomic diversity compared to much more homogenous Pseudomonas populations on the same plants.

Variation in plasmid complement and additional genomic features suggest high adaptability, and the widespread presence of protein secretion systems hints at frequent biotic interactions. While some of the isolates showed plant-protective properties, this was a rare trait. To begin to understand the bacterial populations at the investigated A. thaliana sites and the alternate hosts of these strains when A. thaliana becomes limiting, we employed amplicon sequencing and a novel bulk-culturing metagenomics approach on A. thaliana and neighboring plants, both in spring when A. thaliana was flowering and in late summer before the emergence of the A. thaliana winter cohort.

Our data reveal that Sphingomonas and Pseudomonas strains from A. thaliana not only survive, but also thrive on other diverse local plant hosts, suggesting that leaf-to-leaf transmission from these biotic reservoirs may be a major source of microbes to the next generation.