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Eukaryotes continuously interact with diverse microbial populations and communities, forming relationships spanning a continuum from beneficial to pathogenic. Pathogenic effectors are central to these associations since they directly target host cellular components to promote microbial fitness 1,2 . Although effectors are necessary for virulence and well-studied from the context of single pathogenic strains 3,4 , the extent to which they can modulate population or community dynamics is largely unknown. Here we show that type III effectors of the bacterium Pseudomonas syringae act as public goods to promote the emergence of collective virulence in the plant Arabidopsis thaliana. We disaggregated the effector suite of a P. syringae strain highly virulent on A. thaliana into a coisogenic population with each strain carrying only one effector, (i.e., a metaclone), and showed that while each coisogenic strain in the metaclone is individually unfit, the metaclone cooperates mutualistically to fully restore virulence. We also show that this state of collective virulence emerged irrespective of the microbe's genetic background, being capable of transforming the rhizosphere-inhabiting, beneficial bacterium Pseudomonas fluorescens 5 into a foliar pathogen. These results expand our knowledge of the mechanisms available to polyclonal populations and polymicrobial communities to exploit hosts. They also raise potential evolutionary routes for the emergence of new host-specific pathogens and expand the ecological scale at which disease may be attributed.

Pseudomonas is a highly diverse genus that includes species that cause disease in both plants and animals. Recently, pathogenic pseudomonads from the Pseudomonas syringae and Pseudomonas fluorescens species complexes have caused significant outbreaks in several agronomically important crops in Turkey, including tomato, citrus, artichoke and melon. We characterized 169 pathogenic Pseudomonas strains associated with recent outbreaks in Turkey via multilocus sequence analysis and whole-genome sequencing, then used comparative and evolutionary genomics to characterize putative virulence mechanisms. Most of the isolates are closely related to other plant pathogens distributed among the primary phylogroups of P. syringae , although there are significant numbers of P. fluorescens isolates, which is a species better known as a rhizosphere-inhabiting plant-growth promoter. We found that all 39 citrus blast pathogens cluster in P. syringae phylogroup 2, although strains isolated from the same host do not cluster monophyletically, with lemon, mandarin orange and sweet orange isolates all being intermixed throughout the phylogroup. In contrast, 20 tomato pith pathogens are found in two independent lineages: one in the P. syringae secondary phylogroups, and the other from the P. fluorescens species complex. These divergent pith necrosis strains lack characteristic virulence factors like the canonical tripartite type III secretion system, large effector repertoires and the ability to synthesize multiple bacterial phytotoxins, suggesting they have alternative molecular mechanisms to cause disease. These findings highlight the complex nature of host specificity among plant pathogenic pseudomonads.

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