Pseudomonas virulence factor SaxA detoxifies plant glucosinolate hydrolysis products, rescuing a commensal that suppresses virulence gene expression

Abstract

Plants produce a plethora of specialised metabolites that often play important roles in their defence against pathogenic microbes or herbivorous insects. Exposure of leaf colonising microbes to these metabolites influences their growth and we hypothesize that it also has consequences for microbe-microbe interactions and bacterial recruitment to leaves. In Brassicaceae plants like the model plant Arabidopsis thaliana, glucosinolates and their biologically active derivatives, the isothiocyanates, are major defence metabolites. Adapted plant pathogens like Pseudomonas spp. use the hydrolase SaxA to convert the antimicrobial isothiocyanate sulforaphane to a non-toxic amine, whereas non-adapted commensal microbes are inhibited by this plant toxin. We used Plantibacter sp. 2H11-2 as a model commensal in co-culture with either Pseudomonas viridiflava 3D9 wildtype or a saxA-knock-out mutant. Both strains were isolated from the same wild A. thaliana population. Without isothiocyanate, Plantibacter grew better alone than with Pseudomonas, a potential competitor. At high isothiocyanate concentrations, however, the commensal was dependent on SaxA-mediated isothiocyanate degradation in both solid and liquid medium. At intermediate isothiocyanate concentrations, Plantibacters transcriptome changed in response to sulforaphane in mono-culture but not in co-culture with Pseudomonas, suggesting it was fully protected from this toxin. In return, Plantibacter caused transcriptional changes in Pseudomonas, suppressing biofilm formation and increasing amino acids metabolism gene expression which might suppress virulence and so contribute to plant health. Together, we find that an antimicrobial plant metabolite can force a commensal to depend on a pathogen-produced virulence factor, but that the interaction overall might benefit the plant by limiting pathogenicity.