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

Li, Fengjuan; Du, Pengcheng; Li, Baisheng; Ke, Changwen; Chen, Aiping; Chen, Jie; Zhou, Haijian; Li, Jie; Morris, J. Glenn; Kan, Biao; Wang, Duochun

doi:10.1128/aem.01021-14

Cited by 34 publications

(42 citation statements)

References 31 publications

Supporting

Mentioning

Contrasting

Unclassified

Order By: Relevance

“…Our findings differ from the relatively rare detection of these two putative virulence factors in environmental isolates worldwide (13,44). Given the role of NAG-ST in severe diarrheal disease in human volunteers reported previously by Morris et al (9), the widespread distribution of this pathogenic factor in non-O1/non-O139 V. cholerae in the Chesapeake Bay should be noted by public health authorities.…”

Section: Discussioncontrasting

confidence: 83%

“…In some cases, these factors are accompanied by rtxA cytotoxic activity, causing mammalian cells to detach and round up (7). In our analysis, hlyA, hap, and rtxA were common virulence factors, with frequencies similar to those reported by environmental surveillance studies in Argentina (15), Iceland (19), Italy (23), Bangladesh (20), and China (13). Almost ubiquitous in this study was the V. cholerae type 6 secretion system, with 76% of the isolates carrying all three genes (vasAKH).…”

Section: Discussionsupporting

confidence: 82%

“…Although non-O1/non-O139 V. cholerae strains generally do not produce cholera toxin, other virulence factors contribute to their pathogenicity, including the hemolysin gene hlyA (5), the protease gene hapA (6), the cytotoxic actin cross-linking repeats in toxin gene rtxA (7), the sialidase gene nanH (8), the heat-stable toxin (NAG-ST) (9), a type 6 secretion system (T6SS) (10), and a type 3 secretion system (T3SS) (11). Occasionally, the cholera toxin gene ctxA and the toxin-coregulated-pilus-associated genes tcpA and tcpI are reported to be present in non-O1/non-O139 V. cholerae isolates (12,13).…”

mentioning

confidence: 99%

See 2 more Smart Citations

Non-O1/Non-O139 Vibrio cholerae Carrying Multiple Virulence Factors and V. cholerae O1 in the Chesapeake Bay, Maryland

Ceccarelli

Chen

Hasan

et al. 2015

Appl Environ Microbiol

View full text Add to dashboard Cite

f Non-O1/non-O139 Vibrio cholerae inhabits estuarine and coastal waters globally, but its clinical significance has not been sufficiently investigated, despite the fact that it has been associated with septicemia and gastroenteritis. The emergence of virulent non-O1/non-O139 V. cholerae is consistent with the recognition of new pathogenic variants worldwide. Oyster, sediment, and water samples were collected during a vibrio surveillance program carried out from 2009 to 2012 in the Chesapeake Bay, Maryland. V. cholerae O1 was detected by a direct fluorescent-antibody (DFA) assay but was not successfully cultured, whereas 395 isolates of non-O1/non-O139 V. cholerae were confirmed by multiplex PCR and serology. Only a few of the non-O1/non-O139 V. cholerae isolates were resistant to ampicillin and/or penicillin. Most of the isolates were sensitive to all antibiotics tested, and 77 to 90% carried the El Tor variant hemolysin gene hlyA ET , the actin cross-linking repeats in toxin gene rtxA, the hemagglutinin protease gene hap, and the type 6 secretion system. About 19 to 21% of the isolates carried the neuraminidase-encoding gene nanH and/or the heat-stable toxin (NAG-ST), and only 5% contained a type 3 secretion system. None of the non-O1/non-O139 V. cholerae isolates contained Vibrio pathogenicity island-associated genes. However, ctxA, ace, or zot was present in nine isolates. Fifty-five different genotypes showed up to 12 virulence factors, independent of the source of isolation, and represent the first report of both antibiotic susceptibility and virulence associated with non-O1/non-O139 V. cholerae from the Chesapeake Bay. Since these results confirm the presence of potentially pathogenic non-O1/non-O139 V. cholerae, monitoring for total V. cholerae, regardless of serotype, should be done within the context of public health. Vibrio cholerae, a waterborne bacterial pathogen, is an autochthonous inhabitant of riverine and estuarine aquatic environments. There are Ͼ200 serogroups, based on O antigenic characters, but only serogroups O1 and O139 have been associated with epidemic cholera, and both are considered a major public health threat for developing countries (1).Developed countries today rarely witness cholera cases caused by epidemic strains of V. cholerae, and outbreaks are typically travel associated (2). However, infections other than cholera can be caused by nonepidemic V. cholerae serogroups that are collectively referred to as non-O1/non-O139 V. cholerae and are generally acquired through the consumption of raw or undercooked seafood. Non-O1/non-O139 V. cholerae infections are continuously reported worldwide (3, 4), emphasizing their clinical significance. Although non-O1/non-O139 V. cholerae strains generally do not produce cholera toxin, other virulence factors contribute to their pathogenicity, including the hemolysin gene hlyA (5), the protease gene hapA (6), the cytotoxic actin cross-linking repeats in toxin gene rtxA (7), the sialidase gene nanH (8), the heat-stable toxin (NAG-ST) (9), a type 6...

show abstract

Section: Discussioncontrasting

confidence: 83%

Section: Discussionsupporting

confidence: 82%

mentioning

confidence: 99%

See 1 more Smart Citation

Non-O1/Non-O139 Vibrio cholerae Carrying Multiple Virulence Factors and V. cholerae O1 in the Chesapeake Bay, Maryland

Ceccarelli

Chen

Hasan

et al. 2015

Appl Environ Microbiol

View full text Add to dashboard Cite

show abstract

“…The serotype O1 has been further divided into the classical (CL) and El Tor (ET) biotypes (21,22). The pathogenicity of V. cholerae depends on a combination of properties, including the presence of cholera toxin (CT), encoded by ctxA, and the colonization and adhesion factor encoded by tcpA (22,23). Studies have shown seasonal patterns for this species, with increased occurrence and incidence of wound infections at warmer temperatures (24).…”

mentioning

confidence: 99%

Season-Specific Occurrence of Potentially Pathogenic Vibrio spp. on the Southern Coast of South Korea

Lee

Jang

et al. 2017

Appl Environ Microbiol

View full text Add to dashboard Cite

Vibrio species are widely distributed in warm estuarine and coastal environments, and they can infect humans through the consumption of raw and mishandled contaminated seafood. In this study, we aimed to isolate and observe the distribution of enteropathogenic Vibrio spp. from environments of the southern coast of South Korea over a season cycle. A total of 10,983 isolates of Vibrio spp. were obtained from tidal water and mud samples over a 1-year period from five sampling sites along the southwest coast of South Korea. We found that Vibrio alginolyticus (n ϭ 6,262) and Vibrio parahaemolyticus (n ϭ 1,757) were ubiquitous in both tidal water and mud year round, whereas Vibrio cholerae (n ϭ 24) and Vibrio vulnificus (n ϭ 130) were seasonally specific to summer. While all V. cholerae isolates were nontoxigenic (non-O1 and non-O139), more than 88% of V. vulnificus isolates possessed the virulence factor elastolytic protease (encoded by vvp). Interestingly, V. parahaemolyticus, which was omnipresent in all seasons, contained the virulence factors thermostable direct hemolysin (encoded by tdh) and thermostable direct hemolysin-related hemolysin (encoded by trh) in larger amounts in June (29 trh-positive strains) and September (14 tdh-, 36 trh-, and 12 tdh-and trh-positive strains) than in December (4 trh-positive strains) and February (3 tdh-positive strains), and virulence factors were absent from isolates detected in April. To understand why virulence factors were detected only in the warm season and were absent in the cold season although the locations are static, long-term monitoring and particularly seasonal study are necessary. IMPORTANCEThe presence of enteropathogenic Vibrio species (Vibrio cholerae, Vibrio parahaemolyticus, and Vibrio vulnificus), which cause acute diarrheal infection, septicemia, and wound infections upon ingestion through food and water, is usually associated with temperature. The World Health Organization (WHO) has estimated that there are 1.4 to 4.3 million cases and 28,000 to 142,000 deaths per year worldwide caused by cholera disease. In South Korea alone, consumption is as much as 52.4 kg of fish and shellfish per year per capita. Our findings suggested that seasonally specific acceleration of these possible pathogenic Vibrio spp. may threaten seafood safety and increase the risk of illness in South Korea, where local people consume raw fish during warmer months.

show abstract

“…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.

171

139

View full text Add to dashboard Cite

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.

show abstract

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

Cited by 34 publications

References 31 publications

Non-O1/Non-O139 Vibrio cholerae Carrying Multiple Virulence Factors and V. cholerae O1 in the Chesapeake Bay, Maryland

Non-O1/Non-O139 Vibrio cholerae Carrying Multiple Virulence Factors and V. cholerae O1 in the Chesapeake Bay, Maryland

Season-Specific Occurrence of Potentially Pathogenic Vibrio spp. on the Southern Coast of South Korea

Origins of the current seventh cholera pandemic

Contact Info

Product

Resources

About