Abstract
Vibrio vulnificus, an opportunistic pathogen, is the causative agent of a life-threatening septicemia and a rising problem for aquaculture worldwide. The genetic factors that differentiate its clinical and environmental strains remain enigmatic. Furthermore, clinical strains have emerged from every clade of V. vulnificus In this work, we investigated the underlying genomic properties and population dynamics of the V. vulnificus species from an evolutionary and ecological point of view. Genome comparisons and bioinformatic analyses of 113 V. vulnificus isolates indicate that the population of V. vulnificus is made up of four different clusters. We found evidence that recombination and gene flow between the two largest clusters (cluster 1 [C1] and C2) have drastically decreased to the point where they are diverging independently. Pangenome and phenotypic analyses showed two markedly different lifestyles for these two clusters, indicating commensal (C2) and bloomer (C1) ecotypes, with differences in carbohydrate utilization, defense systems, and chemotaxis, among other characteristics. Nonetheless, we identified frequent intra- and interspecies exchange of mobile genetic elements (e.g., antibiotic resistance plasmids, novel "chromids," or two different and concurrent type VI secretion systems) that provide high levels of genetic diversity in the population. Surprisingly, we identified strains from both clusters in the mucosa of aquaculture species, indicating that manmade niches are bringing strains from the two clusters together. We propose an evolutionary model of V. vulnificus that could be broadly applicable to other pathogenic vibrios and facultative bacterial pathogens to pursue strategies to prevent their infections and emergence.IMPORTANCEVibrio vulnificus is an emergent marine pathogen and is the cause of a deadly septicemia. However, the genetic factors that differentiate its clinical and environmental strains and its several biotypes remain mostly enigmatic. In this work, we investigated the underlying genomic properties and population dynamics of the V. vulnificus species to elucidate the traits that make these strains emerge as a human pathogen. The acquisition of different ecological determinants could have allowed the development of highly divergent clusters with different lifestyles within the same environment. However, we identified strains from both clusters in the mucosa of aquaculture species, indicating that manmade niches are bringing strains from the two clusters together, posing a potential risk of recombination and of emergence of novel variants. We propose a new evolutionary model that provides a perspective that could be broadly applicable to other pathogenic vibrios and facultative bacterial pathogens to pursue strategies to prevent their infections.
Highlights
Vibrio vulnificus, an opportunistic pathogen, is the causative agent of a life-threatening septicemia and a rising problem for aquaculture worldwide
While the majority of the more than 100 described Vibrio species are harmless to humans, several species have emerged as opportunistic human pathogens, most notably Vibrio cholerae, V. parahaemolyticus, and V. vulnificus [9, 10]
In order to investigate the evolutionary changes that led to the divergent expansion of V. vulnificus, we compared 113 publicly available genomes in GenBank, complete or draft, using a phylogenomic tree based on both single nucleotide polymorphisms (SNPs) and average nucleotide identity (ANI)
Summary
An opportunistic pathogen, is the causative agent of a life-threatening septicemia and a rising problem for aquaculture worldwide. We investigated the underlying genomic properties and population dynamics of the V. vulnificus species to elucidate the traits that make these strains emerge as a human pathogen. The number of Vibrio-related human infections rose steadily, with a similar increase observed in Vibrio infections in aquaculture environments [2,3,4,5]. This rise in Vibrio virulence and pathogenicity is often attributed to the ongoing increase in sea surface temperatures associated with climate change [6, 7]. Most deaths occur in patients with preexisting conditions, such as a compromised immune system or elevated serum iron levels (primarily in alcohol-associated liver cirrhosis), where primary septicemia may lead to mortality rates of over 50% [18, 19]
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