Population Structure and Evolution of Non-O1/Non-O139 Vibrio cholerae by Multilocus Sequence Typing

Octavia, Sophie; Salim, Anna C. M.; Kurniawan, Jacob; Lam, Connie; Leung, Queenie; Ahsan, Sunjukta; Reeves, Peter R.; Nair, G. Balakrish; Lan, Ruiting

doi:10.1371/journal.pone.0065342

Cited by 67 publications

(87 citation statements)

References 68 publications

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“…These findings are consistent with a recent report by Octavia et al, in which 77 clinical and environmental non-O1/O139 isolates from a number of different countries were found to form 66 STs (13). The majority of these STs were unique, and only three clonal complexes were formed; as in our study, the clonal complexes cen- tered on epidemic or pandemic, ctx-positive strains, highlighting the close phylogenetic relationship among such strains, in contrast to the diversity seen among non-O1/O139 strains.…”

Section: Discussionsupporting

confidence: 92%

“…MLST was performed as described previously (13). Seven housekeeping genes were targeted for MLST analysis: adk, gyrB, metE, mdh, pntA, purM, and pyrC (see Table S2 in the supplemental material).…”

Section: Methodsmentioning

confidence: 99%

“…We hypothesize that carriage of these and other virulence factors by non-O1/O139 strains creates an environmental reservoir of critical virulence genes, which may contribute to evolution of pathogenic V. cholerae. To explore this hypothesis, we report here results of screening of a collection of 295 environmental non-O1/O139 strains, isolated from 2001 to 2010 from different regions and aquatic environments in China, to determine the frequency of carriage of virulence-associated genes and the underlying phylogenetic relationships on the basis of multilocus sequence typing (MLST) (13).…”

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confidence: 99%

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Distribution of Virulence-Associated Genes and Genetic Relationships in Non-O1/O139 Vibrio cholerae Aquatic Isolates from China

Li³

et al. 2014

Appl Environ Microbiol

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e Non-O1/O139 Vibrio cholerae is naturally present in aquatic ecosystems and has been linked with cholera-like diarrhea and local outbreaks. The distribution of virulence-associated genes and genetic relationships among aquatic isolates from China are largely unknown. In this study, 295 aquatic isolates of V. cholerae non-O1/O139 serogroups from different regions in China were investigated. Only one isolate was positive for ctxB and harbored a rare genotype; 10 (3.4%) isolates carried several types of rstR sequences, eight of which carried rare types of toxin-coregulated pili (tcpA There was no correlation between the prevalence of putative virulence genes and that of CTX prophage or TCP genes, whereas there were correlations among the putative virulence genes. Further multilocus sequence typing (MLST) placed selected isolates (n ‫؍‬ 70) into 69 unique sequence types (STs), which were different from those of the toxigenic O1 and O139 counterparts, and each isolate occupied a different position in the MLST tree. The V. cholerae non-O1/O139 aquatic isolates predominant in China have high genotypic diversity; these strains constitute a reservoir of potential virulence genes, which may contribute to evolution of pathogenic isolates. Vibrio cholerae is the causative agent of cholera, a life-threatening diarrheal disease. Of the more than 200 known V. cholerae serogroups, only O1 and O139 are associated with epidemic and pandemic cholera (1). V. cholerae strains in other serogroups (non-O1/O139 V. cholerae) are often nonpathogenic or associated with only mild illness (2). However, depending in part on the virulence factors which they carry, they have been linked with more-severe, cholera-like illness and have been associated with sporadic cases and outbreaks of gastroenteritis and extraintestinal infections in both developing and developed countries (2-7).Two genetic elements associated with virulence in pathogenic O1 and O139 V. cholerae are a lysogenic filamentous bacteriophage (CTX prophage), which encodes cholera toxin (CT) (8), and the toxin coregulated pilus (TCP) pathogenicity island, which encodes factors involved in intestinal colonization. The CTX prophage uses TCP as a receptor, allowing V. cholerae infection and prophage integration into the bacterial chromosome (8), resulting in the emergence of new toxigenic strains. Non-O1/O139 strains that carry the genes for the CTX prophage and TCP and express CT have been linked with occurrences of severe disease. Other factors that have been associated with virulence include heat-stable toxin (NAG-ST) and hemolysin (Hly) (9). Recently, several novel virulence mechanisms, including a type III secretion system (TTSS) and a type 6 secretion system (T6SS), have been identified in non-O1/O139 isolates (10, 11).Non-O1/O139 V. cholerae strains are naturally present in aquatic ecosystems, such as rivers, estuaries, and coastal waters (4, 12). We hypothesize that carriage of these and other virulence factors by non-O1/O139 strains creates an environmental reservoir of criti...

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Section: Discussionsupporting

confidence: 92%

Section: Methodsmentioning

confidence: 99%

mentioning

confidence: 99%

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Distribution of Virulence-Associated Genes and Genetic Relationships in Non-O1/O139 Vibrio cholerae Aquatic Isolates from China

Li³

et al. 2014

Appl Environ Microbiol

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“…It is also regularly isolated from marine vertebrates, algae, sediment, or directly from the water column (7). Perhaps owing to the wide variety of such macro-and microhabitats, V. cholerae displays a large degree of genetic diversity (8)(9)(10)(11). Horizontal gene transfer by transduction (12), transformation (13), or conjugation (14) is a major factor in the creation of this diversity.…”

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confidence: 99%

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

Kirchberger

Orata

Barlow

et al. 2016

Appl Environ Microbiol

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Vibrio cholerae is a ubiquitous aquatic microbe in temperate and tropical coastal areas. It is a diverse species, with many isolates that are harmless to humans, while others are highly pathogenic. Most notable among them are strains belonging to the pandemic O1/O139 serogroup lineage, which contains the causative agents of cholera. The environmental selective regimes that led to this diversity are key to understanding how pathogens evolve in environmental reservoirs. A local population of V. cholerae and its close relative Vibrio metoecus from a coastal pond and lagoon system was extensively sampled during two consecutive months across four size fractions (480 isolates). In stark contrast to previous studies, the observed population was highly clonal, with 60% of V. cholerae isolates falling into one of five clonal complexes, which varied in abundance in the short temporal scale sampled. V. cholerae clonal complexes had significantly different distributions across size fractions and the two environments sampled, the pond and the lagoon. Sequencing the genomes of 20 isolates representing these five V. cholerae clonal complexes revealed different evolutionary trajectories, with considerable variations in gene content with potential ecological significance. Showing genotypic differentiation and differential spatial distribution, the dominant clonal complexes are likely ecologically divergent. Temporal variation in the relative abundance of these complexes suggests that transient blooms of specific clones could dominate local diversity. IMPORTANCEVibrio cholerae is commonly found in coastal areas worldwide, with only a single group of this bacterium capable of causing severe cholera outbreaks. However, the potential to evolve the ability to cause disease exists in many strains of this species in its aquatic reservoir. Understanding how pathogenic bacteria evolve requires the study of their natural environments. By extensive sampling in a geographically restricted location in the United States, we found that most cells of a V. cholerae population belong to only a small number of strains. Analysis of their genome composition and spatial distribution indicates differential environmental adaptations between these strains. Other strains exist in smaller numbers, and the population was found to be temporally varied. This suggests frequent bloom and collapse cycles on a time scale of weeks. These population dynamics make it possible that more virulent strains could stochastically rise to large numbers, allowing for infection to occur. W hile long thought of as being specifically adapted to life as a pathogen in the human gut (1), numerous strains of Vibrio cholerae with varied degrees of virulence thrive in the brackish waters of lagoons and estuaries of the world (2), from the coast of Australia (3) to Iceland (4). The bacterium is believed to form close associations with aquatic invertebrates, preferentially living a life attached to the chitinous surfaces of those animals (5, 6). It is also regularly isolated f...

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“…Unfortunately, there are no genome sequence-based data for recombination in environmental strains, but several MLST studies on environmental strains have shown high diversity, indicating high recombination rates, which have also been supported by several additional criteria (44)(45)(46). Each of these referenced studies used strains with a sampling bias toward human-associated strains in countries with often inadequate treatment of sewage, adding the complication that some of the "environmental" strains were from fecal contamination.…”

Section: Significance Of the Asian Homeland-middle East-makassar Migrmentioning

confidence: 99%

Origins of the current seventh cholera pandemic

Liu

Feng

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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Vibrio choleraehas caused seven cholera pandemics since 1817, imposing terror on much of the world, but bacterial strains are currently only available for the sixth and seventh pandemics. The El Tor biotype seventh pandemic began in 1961 in Indonesia, but did not originate directly from the classical biotype sixth-pandemic strain. Previous studies focused mainly on the spread of the seventh pandemic after 1970. Here, we analyze in unprecedented detail the origin, evolution, and transition to pandemicity of the seventh-pandemic strain. We used high-resolution comparative genomic analysis of strains collected from 1930 to 1964, covering the evolution from the first available El Tor biotype strain to the start of the seventh pandemic. We define six stages leading to the pandemic strain and reveal all key events. The seventh pandemic originated from a nonpathogenic strain in the Middle East, first observed in 1897. It subsequently underwent explosive diversification, including the spawning of the pandemic lineage. This rapid diversification suggests that, when first observed, the strain had only recently arrived in the Middle East, possibly from the Asian homeland of cholera. The lineage migrated to Makassar, Indonesia, where it gained the important virulence-associated elementsVibrioseventh pandemic island I (VSP-I), VSP-II, and El Tor type cholera toxin prophage by 1954, and it then became pandemic in 1961 after only 12 additional mutations. Our data indicate that specific niches in the Middle East and Makassar were important in generating the pandemic strain by providing gene sources and the driving forces for genetic events.

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Population Structure and Evolution of Non-O1/Non-O139 Vibrio cholerae by Multilocus Sequence Typing

Cited by 67 publications

References 68 publications

Distribution of Virulence-Associated Genes and Genetic Relationships in Non-O1/O139 Vibrio cholerae Aquatic Isolates from China

Distribution of Virulence-Associated Genes and Genetic Relationships in Non-O1/O139 Vibrio cholerae Aquatic Isolates from China

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

Origins of the current seventh cholera pandemic

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