Origins of pandemic Vibrio cholerae from environmental gene pools

Abstract

Some microorganisms can transition from an environmental lifestyle to a pathogenic one. This ecological switch typically occurs through the acquisition of horizontally acquired virulence genes. 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.

Environmental Role of Pathogenic Traits in Vibrio cholerae

“…It remains to be determined which other abiotic and biotic factors have driven the emergence of virulence traits of V. cholerae in its natural environment. We recently discovered that pandemic V. cholerae strains encode allelic variations in core genes in the form of virulence adaptive polymorphisms (VAPs) that enhance their pathogenic potential (117). VAPs confer preadaptations to virulence prior to the acquisition of virulence genes such as CT or TCP and are also encoded by environmental strains (117).…”

“…We recently discovered that pandemic V. cholerae strains encode allelic variations in core genes in the form of virulence adaptive polymorphisms (VAPs) that enhance their pathogenic potential (117). VAPs confer preadaptations to virulence prior to the acquisition of virulence genes such as CT or TCP and are also encoded by environmental strains (117). Since some of the virulence traits of V. cholerae appear to have evolved prior to host colonization, we speculate that VAPs circulate in nonpathogenic environmental populations of V. cholerae and are selected for and enriched in the environment.…”

“…It has been shown that OmpU provides resistance to bile and organic acids and confers an advantage in intestinal colonization (113)(114)(115). OmpU also confers resistance against phage predation, facilitates survival inside the amoebal lysosome, and is involved in biofilm formation (44,116,117). These traits provide an evolutionary advantage in the natural environment of V. cholerae that likely led to the emergence of virulence traits (Fig.…”

“…These traits provide an evolutionary advantage in the natural environment of V. cholerae that likely led to the emergence of virulence traits (Fig. 2B) (44,116,117).…”

Alignment- and reference-free phylogenomics with colored de Bruijn graphs

“…Splits reconstructed for the V. cholerae dataset[14] by SANS (left) and by Shapiro et al[14] (right) visualized with SplitsTree[8,10].…”