Modular Traits of the Rhizobiales Root Microbiota and Their Evolutionary Relationship with Symbiotic Rhizobia

Summary

Rhizobia are a paraphyletic group of soil-borne bacteria that induce nodule organogenesis in legume roots and fix atmospheric nitrogen for plant growth. In non-leguminous plants, species from the Rhizobiales order define a core lineage of the plant microbiota, suggesting additional functional interactions with plant hosts. In this work, genome analyses of 1,314 Rhizobiales isolates along with amplicon studies of the root microbiota reveal the evolutionary history of nitrogen-fixing symbiosis in this bacterial order. Key symbiosis genes were acquired multiple times, and the most recent common ancestor could colonize roots of a broad host range. In addition, root growth promotion is a characteristic trait of Rhizobiales in Arabidopsis thaliana, whereas interference with plant immunity constitutes a separate, strain-specific phenotype of root commensal Alphaproteobacteria. Additional studies with a tripartite gnotobiotic plant system reveal that these traits operate in a modular fashion and thus might be relevant to microbial homeostasis in healthy roots.

Graphical Abstract

Highlights

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  Comparative genomics of >1,300 Rhizobiales isolated from diverse plant hosts

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  Commensalism predates nitrogen-fixing nodule symbiosis in rhizobia

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  Root growth promotion is a conserved trait of commensal Rhizobiales

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  Microbiota members exhibit strain-specific interference of Arabidopsis immune responses

Abstract

Garrido-Oter, Nakano, Dombrowski, et al. employ comparative genomics of ∼1,000 Rhizobiales strains that were isolated from diverse plant species to reconstruct the evolutionary history of nitrogen-fixing symbiosis. Arabidopsis re-colonization experiments reveal that root growth promotion and interference with host immune responses are modular traits of the root microbiota.