Extended MLST-based population genetics and phylogeny of Vibrio parahaemolyticus with high levels of recombination

e Vibrio parahaemolyticus is a seafood-borne pathogenic bacterium that is a major cause of gastroenteritis worldwide. We investigated the genetic and evolutionary relationships of 101 V. parahaemolyticus isolates originating from clinical, human carrier, and various environmental and seafood production sources in Thailand using multilocus sequence analysis. The isolates were recovered from clinical samples (n ‫؍‬ 15), healthy human carriers (n ‫؍‬ 18), various types of fresh seafood (n ‫؍‬ 18), frozen shrimp (n ‫؍‬ 16), fresh-farmed shrimp tissue (n ‫؍‬ 18), and shrimp farm water (n ‫؍‬ 16). Phylogenetic analysis revealed a high degree of genetic diversity within the V. parahaemolyticus population, although isolates recovered from clinical samples and from farmed shrimp and water samples represented distinct clusters. The tight clustering of the clinical isolates suggests that disease-causing isolates are not a random sample of the environmental reservoir, although the source of infection remains unclear. Extensive serotypic diversity occurred among isolates representing the same sequence types and recovered from the same source at the same time. These findings suggest that the O-and K-antigen-encoding loci are subject to exceptionally high rates of recombination. There was also strong evidence of interspecies horizontal gene transfer and intragenic recombination involving the recA locus in a large proportion of isolates. As the majority of the intragenic recombinational exchanges involving recA occurred among clinical and carrier isolates, it is possible that the human intestinal tract serves as a potential reservoir of donor and recipient strains that is promoting horizontal DNA transfer, driving evolutionary change, and leading to the emergence of new, potentially pathogenic strains. Vibrio parahaemolyticus is a seafood-borne pathogenic bacterium and is the leading cause of traveler's diarrhea and gastroenteritis worldwide due to the consumption of undercooked contaminated seafood, particularly shellfish. The organism possesses a number of virulence factors, including a thermostable direct hemolysin (TDH) (1), a thermostable direct hemolysinrelated hemolysin (TRH) (2), and type 3 secretion system 1 (TTSS1) and TTSS2 (3). Strains that possess tdh, trh, and TTSS2-encoding genes are generally pathogenic and responsible for the vast majority of clinical cases. While such strains account for only 1 to 2% of isolates sampled from water and different marine species (4-6), they are known to have a widespread global distribution, having been reported from cases of infection in Japan, India, Thailand, Malaysia, China, Indonesia, the United Kingdom, Italy, and the East and Gulf Coasts of the United States (7-19).The public health and commercial burdens associated with V. parahaemolyticus contamination are very high in Thailand due to the wide consumption of seafood. Although undercooked seafood has been identified as a source of V. parahaemolyticus infection (20, 21), the relative likelihood of contamination from differ...

Section: Discussionsupporting

confidence: 91%

mentioning

confidence: 98%

Genetic Relationships of Vibrio parahaemolyticus Isolates from Clinical, Human Carrier, and Environmental Sources in Thailand, Determined by Multilocus Sequence Analysis

Theethakaew

Feil

Castillo-Ramírez

et al. 2013

“…Strains collected worldwide all group within the phylogeny of GBE isolates that were collected in a relatively isolated northern estuary. As observed in other studies of Vibrio populations (19,31,61,69), this population displayed a history of recombination; however, the extent observed here is noteworthy because most prior analyses of this species have focused on epidemic (and hence clonal) lineages (5,18,37). Even so, the influence of recombination on population structure was modest (r/m, 1.33) compared to a parallel study with environmental V. cholerae samples isolated from central coastal California and Hawaii (r/m, 4 to 8) (31).…”

Section: Discussionsupporting

confidence: 83%

Ecology and Genetic Structure of a Northern Temperate Vibrio cholerae Population Related to Toxigenic Isolates

Schuster

Tyzik

Donner

et al. 2011

Although Vibrio cholerae is an important human pathogen, little is known about its populations in regions where the organism is endemic but where cholera disease is rare. A total of 31 independent isolates confirmed as V. cholerae were collected from water, sediment, and oysters in 2008 and 2009 from the Great Bay Estuary (GBE) in New Hampshire, a location where the organism has never been detected. Environmental analyses suggested that abundance correlates most strongly with rainfall events, as determined from data averaged over several days prior to collection. Phenotyping, genotyping, and multilocus sequence analysis (MLSA) revealed a highly diverse endemic population, with clones recurring in both years. Certain isolates were closely related to toxigenic O1 strains, yet no virulence genes were detected. Multiple statistical tests revealed evidence of recombination among strains that contributed to allelic diversity equally as mutation. This relatively isolated population discovered on the northern limit of detection for V. cholerae can serve as a model of natural population dynamics that augments predictive models for disease emergence.Vibrio cholerae is a ubiquitous waterborne bacterium found commonly in estuarine environments (37). Although V. cholerae is comprised of over 200 serotypes, only serotypes O1 and O139 are currently responsible for epidemic and pandemic cholera outbreaks (1,9,14,15,37,49,57,60). Closely related clones of types O1 and O139 are found rarely in the environment and only in warm waters (16,54). Whereas these pandemic serotypes and their associated populations have been the subjects of intense study, investigations of the remaining ecotypes are less common (29, 31-33, 36, 53). Yet other serotypes could be reservoirs of new pathogenic lineages that emerge by horizontal transfer and recombination. Recombination has been observed in several V. cholerae collections (31, 61) and is thought to have driven the emergence of new infective variants (16).Only 40 domestically acquired toxigenic V. cholerae cases have been reported in the United States since 1995 (66), but epidemics are ongoing in warm, subtropical climates, the most recent occurring in Haiti, which had been cholera-free for decades (6). Variation in disease incidence is caused in part by transmission between patients by feces-contaminated drinking water and by endemic populations of toxigenic cholera organisms in warm subtropical environments (11,12,37). Endemic cholera has not posed a public health threat in temperate regions in modern times (38, 60). Toxigenic O1 and O139 serotypes of V. cholerae are not regularly isolated from temperate waters in the United States, but some environmental non-O1/non-O139 populations, a few of which are associated with disease, have been described (11,31,43,58). Even so, the pathogenic potential and ecology of most endemic populations are not well understood.Here we describe the genotypic and phenotypic characteristics of a newly identified and highly diverse population of non-O1 V. cholerae is...

“…1; also see Table S1 in the supplemental material). The lack of population structure is consistent with the findings from other MLSA studies of V. parahaemolyticus (11,30,32). More notably, isolates from cold water (Ͻ11°C) tended to cluster into certain clades (Fig.…”

supporting

confidence: 90%

“…Previously, the diversity and the extent of recombination among clinical and environmental V. parahaemolyticus populations were examined in three studies using multilocus sequence analysis (MLSA) (3,11,32). These studies revealed highly diverse populations resulting from frequent recombination, and in one population, diversity was associated with geography (11).…”

mentioning

confidence: 99%

Influence of Seasonality on the Genetic Diversity of Vibrio parahaemolyticus in New Hampshire Shellfish Waters as Determined by Multilocus Sequence Analysis

Ellis

Schuster

Striplin

et al. 2012