Some microorganisms can transition from an environmental lifestyle to a pathogenic one1–3. This ecological switch typically occurs through the acquisition of horizontally acquired virulence genes4,5. However, the genomic features that must be present in a population before the acquisition of virulence genes and emergence of pathogenic clones remain unknown. We hypothesized that virulence adaptive polymorphisms (VAPs) circulate in environmental populations and are required for this transition. We developed a comparative genomic framework for identifying VAPs, using Vibrio cholerae as a model. We then characterized several environmental VAP alleles to show that while some of them reduced the ability of clinical strains to colonize a mammalian host, other alleles conferred efficient host colonization. These results show that VAPs are present in environmental bacterial populations before the emergence of virulent clones. We propose a scenario in which VAPs circulate in the environment and become selected and enriched under certain ecological conditions, and finally a genomic background containing several VAPs acquires virulence factors that allow for its emergence as a pathogenic clone.
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The authors thank the anonymous reviewers for their comments and suggestions, and O. Cordero, Y. Terrat, N. Tromas and B. Privett for comments on the manuscript. The authors thank L. Shelven for his technical assistance. B.J.S. was supported by a Canada Research Chair and the Canadian Institutes for Health Research. R.K.T. was supported by National Institutes of Health grants AI039654 and AI025096. S.A.-M. was supported by startup funds from the Burnett School of Biomedical Sciences at the University of Central Florida and Dartmouth College's E. E. Just Postdoctoral Fellowship. This Letter is dedicated to the memory of R.K. Taylor.
The authors declare no competing financial interests.
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Shapiro, B., Levade, I., Kovacikova, G. et al. Origins of pandemic Vibrio cholerae from environmental gene pools. Nat Microbiol 2, 16240 (2017). https://doi.org/10.1038/nmicrobiol.2016.240
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