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

TL;DR

A bacterial enzyme detoxifies plant toxins, allowing a commensal microbe to thrive and reduce pathogen virulence in plant environments.

Contribution

Discovery that Pseudomonas SaxA detoxifies plant isothiocyanates, enabling commensal survival and suppressing pathogen virulence.

Findings

Plantibacter sp. requires Pseudomonas-produced SaxA to survive high isothiocyanate concentrations.

Commensal presence suppresses Pseudomonas biofilm formation and virulence gene expression.

SaxA-mediated detoxification alters microbial interactions and community dynamics in plant environments.

Abstract

Plants produce a plethora of specialized metabolites that often play important roles in their defence against pathogenic microbes or herbivorous insects. Exposure of leaf-colonizing microbes to these metabolites influences their growth, and we hypothesize that it also has consequences for microbe–microbe interactions. 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, Plantibacter’s transcriptome changed in response to sulforaphane in monoculture but not in co-culture with Pseudomonas, suggesting that it was fully protected from this toxin. In return, Plantibacter caused transcriptional changes in Pseudomonas, suppressing biofilm formation and increasing amino acid metabolism gene expression which might suppress virulence and so contribute to plant health. Together, we find that degradation of an antimicrobial plant metabolite can protect a commensal to depend on a pathogen-produced virulence factor, suggesting effects on community composition in environments where microbes are exposed to ITCs.

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