Origins of pandemic Vibrio cholerae from environmental gene pools

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Abstract

Some microorganisms can transition from an environmental lifestyle to a pathogenic one13. 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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Figure 1: Comparative genomics reveals candidate VAPs.
Figure 2: Phenotypic characterization of ompU alleles.
Figure 3: Model of pandemic clone emergence from an environmental gene pool.

Change history

  • 14 July 2017

    In the PDF version of this article previously published, the year of publication provided in the footer of each page and in the 'How to cite' section was erroneously given as 2017, it should have been 2016. This error has now been corrected. The HTML version of the article was not affected.

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Acknowledgements

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.

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S.A.-M. conceived the study. B.J.S., R.K.T. and S.A.-M. designed the study. I.L. sequenced genomes. B.J.S. performed computational analysis. G.K. and S.A.-M. performed phenotypic characterization. B.J.S. and S.A.-M. analysed and interpreted data and wrote the article. All authors have read a version of the manuscript.

Corresponding author

Correspondence to Salvador Almagro-Moreno.

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The authors declare no competing financial interests.

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Supplementary Notes 1 and 2, Supplementary Figures 1–10, Supplementary Tables 1–8. (PDF 3641 kb)

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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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