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. Here, through phylogenetic analysis of 1,765 Xanthomonadales genomes, we show that immunomodulation is a highly conserved, ancestral trait across this core order of the plant microbiota, and preceded specialization of these bacteria as host-adapted pathogens. Rhodanobacter R179, from the deepest branch of the Xanthomonadales, activates immune responses which are dependent on EFR and SOBIR1 cell-surface receptor complexes, yet root transcriptomics suggest the commensal evades host recognition upon prolonged association. This commensal camouflage is likely due to the combined activities of the conserved ABC transporter permease (dssA) and the TonB-dependent transporter (dssB) and the selective elimination of immunogenic elicitors produced by R179, other microbiota members, and the plant host. The ability of R179 to mask itself and other commensals from host recognition is consistent with a convergence of distinct root transcriptomes triggered by immunosuppressive or non-suppressive synthetic communities upon R179 co-inoculation. Although root load of R179 on wild-type and efr fls2 sobir1 mutant plants was indistinguishable in mono-associations, immunomodulation through dssAB provided R179 with a competitive advantage in a community context in the absence of other immunosuppressive bacteria. Furthermore, root colonization of diverse commensal Xanthomonadales strains varied 1,000-fold without detrimental impacts on the host. We propose that conservation of 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.

INSTRUMENT(S): Orbitrap Exploris 480

ORGANISM(S): Arabidopsis Thaliana (mouse-ear Cress)

TISSUE(S): Plant Cell

SUBMITTER: Sara Christina Stolze  

LAB HEAD: Hirofumi Nakagami

PROVIDER: PXD045054 | Pride | 2024-12-12

REPOSITORIES: Pride