Neighbor predation linked to natural competence fosters the transfer of large genomic regions in Vibrio cholerae.

Melanie Blokesch,Nicolas Guex,Noémie Matthey,Christian Iseli,Candice Stoudmann,Sandrine Stutzmann

doi:10.7554/elife.48212

Abstract

Natural competence for transformation is a primary mode of horizontal gene transfer. Competent bacteria are able to absorb free DNA from their surroundings and exchange this DNA against pieces of their own genome when sufficiently homologous. However, the prevalence of non-degraded DNA with sufficient coding capacity is not well understood. In this context, we previously showed that naturally competent Vibrio cholerae use their type VI secretion system (T6SS) to actively acquire DNA from non-kin neighbors. Here, we explored the conditions of the DNA released through T6SS-mediated killing versus passive cell lysis and the extent of the transfers that occur due to these conditions. We show that competent V. cholerae acquire DNA fragments with a length exceeding 150 kbp in a T6SS-dependent manner. Collectively, our data support the notion that the environmental lifestyle of V. cholerae fosters the exchange of genetic material with sufficient coding capacity to significantly accelerate bacterial evolution.

Highlights

The causative agent of the diarrheal disease cholera, Vibrio cholerae, is responsible for seven major pandemics since 1817, one of which is still ongoing
As an example of the significant power of this natural competence for gene uptake, we previously witnessed the gain of an ~40 kbp O139-antigen cluster at the expense of the original ~30 kbp O1-antigen cluster through natural transformation, which significantly changed the phenotypes of these bacteria
We show that the DNA transfer frequency is significantly enhanced in T6SS-positive compared to T6SS-negative strains and that large genomic regions are transferred from the killed prey to the competent acceptor bacterium

Summary

Introduction

The causative agent of the diarrheal disease cholera, Vibrio cholerae, is responsible for seven major pandemics since 1817, one of which is still ongoing. Many disease-causing bacteria have developed mechanisms for rapidly evolving in response to environmental pressures, and these rapid changes are often responsible for the formation of new serogroups with pandemic potential. A major mode of HGT is natural competence for transformation in which bacteria are able to absorb free DNA from their surroundings using their competence-induced DNAuptake complex (Chen and Dubnau, 2004; Johnston et al, 2014; Matthey and Blokesch, 2016). As an example of the significant power of this natural competence for gene uptake, we previously witnessed the gain of an ~40 kbp O139-antigen cluster at the expense of the original ~30 kbp O1-antigen cluster through natural transformation (followed by strong selective pressure exerted by antibiotics or phages; Blokesch and Schoolnik, 2007), which significantly changed the phenotypes of these bacteria.

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Conclusion