Modular traits of the Rhizobiales root microbiota and their evolutionary relationship with symbiotic rhizobia

Rhizobia are a paraphyletic group of soil-borne bacteria characterized by their ability to induce nodule organogenesis in legume roots and fix atmospheric nitrogen for plant growth. In non-leguminous plants, species within the Rhizobiales order define a core lineage of the plant microbiota, suggesting alternative forms of interactions with plant hosts. Genome analysis of 1,314 Rhizobiales isolates along with amplicon studies of the root microbiota showed that key symbiosis genes were acquired multiple times and that their most recent common ancestor had the capacity to colonize the roots of a broad range of hosts. We identify root growth promotion as a characteristic trait of Rhizobiales in Arabidopsis thaliana, whereas interference with the plant immune system constitutes a separate, strain-specific phenotype of root commensal Alphaproteobacteria. Using a tripartite gnotobiotic plant system, we show that these traits operate in a modular fashion and might be relevant to microbial homeostasis in healthy roots.