The Dynamics of Genetic Interactions betweenVibrio metoecusandVibrio cholerae, Two Close Relatives Co-Occurring in the Environment

Abstract

Vibrio metoecus is the closest relative of Vibrio cholerae, the causative agent of the potent diarrheal disease cholera. Although the pathogenic potential of this new species is yet to be studied in depth, it has been co-isolated with V. cholerae in coastal waters and found in clinical specimens in the United States. We used these two organisms to investigate the genetic interaction between closely related species in their natural environment. The genomes of 20 V. cholerae and 4 V. metoecus strains isolated from a brackish coastal pond on the US east coast, as well as 4 clinical V. metoecus strains were sequenced and compared with reference strains. Whole genome comparison shows 86–87% average nucleotide identity (ANI) in their core genes between the two species. On the other hand, the chromosomal integron, which occupies approximately 3% of their genomes, shows higher conservation in ANI between species than any other region of their genomes. The ANI of 93–94% observed in this region is not significantly greater within than between species, meaning that it does not follow species boundaries. Vibrio metoecus does not encode toxigenic V. cholerae major virulence factors, the cholera toxin and toxin-coregulated pilus. However, some of the pathogenicity islands found in pandemic V. cholerae were either present in the common ancestor it shares with V. metoecus, or acquired by clinical and environmental V. metoecus in partial fragments. The virulence factors of V. cholerae are therefore both more ancient and more widespread than previously believed. There is high interspecies recombination in the core genome, which has been detected in 24% of the single-copy core genes, including genes involved in pathogenicity. Vibrio metoecus was six times more often the recipient of DNA from V. cholerae as it was the donor, indicating a strong bias in the direction of gene transfer in the environment.

A genomic island in Vibrio cholerae with VPI-1 site-specific recombination characteristics contains CRISPR-Cas and type VI secretion modules

“…Previous studies have observed variations in VPI-1 through PCR analysis of V. cholerae strains or BLASTN analysis of V. cholerae genomes for VPI-1 genes. For the most part, the variations identified represent minor gene gain/loss events or sequence changes to known ORFs in VPI-1101112. GI Vch S12 is different in that it shares practically no gene content with VPI-1.…”

“…GI Vch S12 and associated islands can be divided into sub-clusters or islets, as has been previously done for V. cholerae pathogenicity island 2 (VPI-2)12, consisting of the CRISPR-Cas cluster, the T6SS cluster, and the ORFs 16–25 cluster. Given that multiple GIs (Fig.…”

“…Most important to pathogenicity of the pandemic strains are genes found on two MGEs, the cholera toxin bacteriophage (CTXϕ) and a GI called the V. cholerae pathogenicity island 1 (VPI-1)89. Although these MGEs are common in pandemic strains, examples of CTXϕ and VPI-1 in non-O1/O139 strains have been documented and are indicative of their mobility across natural populations of V. cholerae and close relatives101112. The CTXϕ contains genes encoding a potent enterotoxin that, when secreted in the human intestinal tract, results in significant loss of fluid that can lead to death within 24 hours if left untreated1.…”

A Small Number of Phylogenetically Distinct Clonal Complexes Dominate a Coastal Vibrio cholerae Population

“…Different evolutionary trajectories for various clonal complexes. In order to find the possible genetic determinants of the different spatial distribution found for some of the V. cholerae CCs, we analyzed 20 genomes from the 5 dominant CCs recovered in sampling from both August and September (CC1, CC2, CC3, CC5, and CC13) that we sequenced in a previous study (50). A 3,410,640-bp whole-genome alignment of these isolates displays 98.6% average pairwise nucleotide identity, with 120,730 phylogenetically informative sites.…”

“…This indicates that less than half the number of recombination events in V. metoecus than in V. cholerae account for the same amount of introduced nucleotides. We have previously noted that V. metoecus receives considerably more DNA from V. cholerae than vice versa, presumably due to their sympatric occurrence, where V. cholerae is the most abundant donor of nucleic acids (50). A situation where large V. cholerae populations cooccur with smaller V. metoecus populations could lead to a dynamic where the rarer V. metoecus more often takes up distantly related DNA, while V. cholerae predominantly exchanges DNA with the more abundant members of its own species.…”