Conserved immunomodulation and variation in host association by Xanthomonadales commensals in Arabidopsis root microbiota

Abstract

Suppression of chronic Arabidopsis immune responses is a widespread but typically strain-specific trait across the major bacterial lineages of the plant microbiota. We show by phylogenetic analysis and in planta associations with representative strains that immunomodulation is a highly conserved, ancestral trait across Xanthomonadales, and preceded specialization of some of these bacteria as host-adapted pathogens. Rhodanobacter R179 activates immune responses, yet root transcriptomics suggest this commensal evades host immune perception upon prolonged association. R179 camouflage likely results from combined activities of two transporter complexes (dssAB) and the selective elimination of immunogenic peptides derived from all partners. The ability of R179 to mask itself and other commensals from the plant immune system is consistent with a convergence of distinct root transcriptomes triggered by immunosuppressive or non-suppressive synthetic microbiota upon R179 co-inoculation. Immunomodulation through dssAB provided R179 with a competitive advantage in synthetic communities in the root compartment. We propose that extensive immunomodulation by Xanthomonadales is related to their adaptation to terrestrial habitats and might have contributed to variation in strain-specific root association, which together accounts for their prominent role in plant microbiota establishment. The authors show that immunosuppression is highly conserved in the bacterial order Xanthomonadales. This feature, which preceded their specialization as host-adapted pathogens, probably contributes to their prominence as core members of the plant microbiota.