Cooperative virulence via the collective action of secreted pathogen effectors

Tatiana Ruiz-Bedoya,  Pauline W. Wang,  Darrell Desveaux & David S. Guttman

Although virulence is typically attributed to single pathogenic strains, here we investigated whether effectors secreted by a population of non-virulent strains could function as public goods to enable the emergence of collective virulence. We disaggregated the 36 type III effectors of the phytopathogenic bacterium Pseudomonas syringae strain PtoDC3000 into a ‘metaclone’ of 36 coisogenic strains, each carrying a single effector in an effectorless background. Each coisogenic strain was individually unfit, but the metaclone was collectively as virulent as the wild-type strain on Arabidopsis thaliana, suggesting that effectors can drive the emergence of cooperation-based virulence through their public action. We show that independently evolved effector suits can equally drive this cooperative behaviour by transferring the effector alleles native to the strain PmaES4326 into the conspecific but divergent strain PtoDC3000. Finally, we transferred the disaggregated PtoDC3000 effector arsenal into Pseudomonas fluorescens and show that their cooperative action was sufficient to convert this rhizosphere-inhabiting beneficial bacterium into a phyllosphere pathogen. These results emphasize the importance of microbial community interactions and expand the ecological scale at which disease may be attributed.

https://doi.org/10.1038/s41564-023-01328-8

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