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Phylogeography of the marine pathogen, Vibrio vulnificus, revealed the ancestral scenarios of its evolution.

ABSTRACT: Vibrio vulnificus is the leading cause of seafood-associated deaths worldwide. Despite the growing knowledge about the population structure of V. vulnificus, the evolutionary history and the ancestral relationships of strains isolated from various regions around the world have not been determined. Using the largest collection of sequence and isolate data of V. vulnificus to date, we applied ancestral character reconstruction to study the phylogeography of V. vulnificus. Multilocus sequence typing data from 10 housekeeping genes were used for the inference of ancestral states and reconstruction of the evolutionary history. The findings showed that the common ancestor of all V. vulnificus populations originated from East Asia, and later evolved into two main clusters that spread with time and eventually evolved into distinct populations in different parts of the world. While we found no meaningful insights concerning the evolution of V. vulnificus populations in the Middle East; however, we were able to reconstruct the ancestral scenarios of its evolution in East Asia, North America, and Western Europe.

SUBMITTER: Bisharat N

PROVIDER: S-EPMC7520988 | biostudies-literature | 2020 Sep

REPOSITORIES: biostudies-literature

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Phylogeography of the marine pathogen, Vibrio vulnificus, revealed the ancestral scenarios of its evolution.

Bisharat Naiel N Koton Yael Y Oliver James D JD

MicrobiologyOpen 20200810 9

Vibrio vulnificus is the leading cause of seafood-associated deaths worldwide. Despite the growing knowledge about the population structure of V. vulnificus, the evolutionary history and the ancestral relationships of strains isolated from various regions around the world have not been determined. Using the largest collection of sequence and isolate data of V. vulnificus to date, we applied ancestral character reconstruction to study the phylogeography of V. vulnificus. Multilocus sequence typin ...[more]

PMID: 32779403

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Project description:Vibrio vulnificus is an aquatic bacterium and an important human pathogen. Strains of V. vulnificus are biochemically classified into three biotypes. The newly emerged biotype 3 appears to be rather clonal and geographically restricted to Israel, where it caused an outbreak of wound infections and bacteremia. To understand the evolution of the bacterium's genome, we sequenced and analyzed the genome of biotype 3 strain VVyb1(BT3), and then conducted a microbial environmental survey of the hypothesized niche from which it probably evolved. The genome of this environmental isolate revealed higher similarity to the published biotype 1 genomes of clinical strains (90%) than to the environmental strains (87%), supporting the virulence of the biotype 3 group. Moreover, 214 of the total 5361 genes were found to be unique to strain VVyb1(BT3), having no sequence similarity to any of the known genomes of V. vulnificus; 35 of them function in DNA mobility and rearrangement, supporting the role of horizontal gene transfer in genome evolution. Interestingly, 29 of the "unique" genes had homologies among Shewanella species. In a survey conducted in aquaculture ponds in Israel, we successfully co-isolated Shewanella and V. vulnificus from the same niche, further supporting the probable contribution of Shewanella to the genome evolution of biotype 3. Indeed, one gene was found in a S. algae isolate. Surprisingly, molecular analysis revealed that some of the considered unique genes are harbored by non-sequenced biotype 1 strains isolated from the same environment. Finally, analyses of the biotype 3 genome together with the environmental survey suggested that its genome originated from a biotype 1 Israeli strain that acquired a rather small number of genes from other bacterial species in the niche, such as Shewanella. Therefore, aquaculture is likely to play a major role as a man-made ecological niche in bacterial evolution, leading the emergence of new pathogenic groups in V. vulnificus.

Project description:In 1996 a common-source outbreak of severe soft tissue and bloodstream infections erupted among Israeli fish farmers and fish consumers due to changes in fish marketing policies. The causative pathogen was a new strain of Vibrio vulnificus, named biotype 3, which displayed a unique biochemical and genotypic profile. Initial observations suggested that the pathogen erupted as a result of genetic recombination between two distinct populations. We applied a whole genome shotgun sequencing approach using several V. vulnificus strains from Israel in order to study the pan genome of V. vulnificus and determine the phylogenetic relationship of biotype 3 with existing populations. The core genome of V. vulnificus based on 16 draft and complete genomes consisted of 3068 genes, representing between 59 and 78% of the whole genome of 16 strains. The accessory genome varied in size from 781 to 2044 kbp. Phylogenetic analysis based on whole, core, and accessory genomes displayed similar clustering patterns with two main clusters, clinical (C) and environmental (E), all biotype 3 strains formed a distinct group within the E cluster. Annotation of accessory genomic regions found in biotype 3 strains and absent from the core genome yielded 1732 genes, of which the vast majority encoded hypothetical proteins, phage-related proteins, and mobile element proteins. A total of 1916 proteins (including 713 hypothetical proteins) were present in all human pathogenic strains (both biotype 3 and non-biotype 3) and absent from the environmental strains. Clustering analysis of the non-hypothetical proteins revealed 148 protein clusters shared by all human pathogenic strains; these included transcriptional regulators, arylsulfatases, methyl-accepting chemotaxis proteins, acetyltransferases, GGDEF family proteins, transposases, type IV secretory system (T4SS) proteins, and integrases. Our study showed that V. vulnificus biotype 3 evolved from environmental populations and formed a genetically distinct group within the E-cluster. The unique epidemiological circumstances facilitated disease outbreak and brought this genotype to the attention of the scientific community.

Dataset Information

Phylogeography of the marine pathogen, Vibrio vulnificus, revealed the ancestral scenarios of its evolution.

Publications

Phylogeography of the marine pathogen, Vibrio vulnificus, revealed the ancestral scenarios of its evolution.

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