The El Tor Biotype of
            <i>Vibrio cholerae</i>
            Exhibits a Growth Advantage in the Stationary Phase in Mixed Cultures with the Classical Biotype

Pradhan, Subhra; Baidya, Amit K.; Ghosh, A. K.; Paul, Kalidas; Chowdhury, Rukhsana

doi:10.1128/jb.01180-09

Cited by 29 publications

(18 citation statements)

References 31 publications

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“…As has been reported earlier [26], the El Tor N16961 strain had a growth advantage in the cocultures (data not shown). CFU of the classical strain O395 in the individual cultures and cocultures were comparable until the onset of the stationary phase when the CFU of O395 in the cocultures started decreasing more rapidly than that in the individual cultures and by 18 to 20 hours the CFU of O395 in the cocultures was more than 1000 fold lower than that in individual cultures (Fig.…”

Section: Resultssupporting

confidence: 88%

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Vibrio cholerae Classical Biotype Is Converted to the Viable Non-Culturable State when Cultured with the El Tor Biotype

2013

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A unique event in bacterial epidemiology was the emergence of the El Tor biotype of Vibrio cholerae O1 and the subsequent rapid displacement of the existing classical biotype as the predominant cause of epidemic cholera. We demonstrate that when the El Tor and classical biotypes were cocultured in standard laboratory medium a precipitous decline in colony forming units (CFU) of the classical biotype occurred in a contact dependent manner. Several lines of evidence including DNA release, microscopy and flow cytometric analysis indicated that the drastic reduction in CFU of the classical biotype in cocultures was not accompanied by lysis, although when the classical biotype was grown individually in monocultures, lysis of the cells occurred concomitant with decrease in CFU starting from late stationary phase. Furthermore, uptake of a membrane potential sensitive dye and protection of genomic DNA from extracellular DNase strongly suggested that the classical biotype cells in cocultures retained viability in spite of loss of culturability. These results suggest that coculturing the classical biotype with the El Tor biotype protects the former from lysis allowing the cells to remain viable in spite of the loss of culturability. The stationary phase sigma factor RpoS may have a role in the loss of culturability of the classical biotype in cocultures. Although competitive exclusion of closely related strains has been reported for several bacterial species, conversion of the target bacterial population to the viable non-culturable state has not been demonstrated previously and may have important implications in the evolution of bacterial strains.

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Section: Resultssupporting

confidence: 88%

“…O395 Sm r Nal r was cocultured with N16961 Sm r , C6709 Sm r , E7946 and SG-24 Sm r as described previously [26]. To examine if the antibiotic resistance markers affected fitness the marker was switched between the strains and O395 Sm r was cocultured with N16961 Sm r Nal r .…”

Section: Methodsmentioning

confidence: 99%

Vibrio cholerae Classical Biotype Is Converted to the Viable Non-Culturable State when Cultured with the El Tor Biotype

2013

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“…Acetoin biosynthesis in the presence of exogenous sugar such as glucose is crucial for biotyping the seventh pandemic El Tor strains and O139 strains (24). El Tor strains have a competitive growth advantage both in vitro and in vivo in cocultures with Classical strains and express higher levels of virulence factors in the tested cocultures (36).…”

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confidence: 99%

Suppressed Induction of Proinflammatory Cytokines by a Unique Metabolite Produced by Vibrio cholerae O1 El Tor Biotype in Cultured Host Cells

2011

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Vibrio cholerae O1 has two biotypes, El Tor and Classical, and the latter is now presumed to be extinct in nature. Under carbohydrate-rich growth conditions, El Tor biotype strains produce the neutral fermentation end product 2,3-butanediol (2,3-BD), which prevents accumulation of organic acids from mixed acid fermentation and thus avoids a lethal decrease in the medium pH, while the Classical biotype strains fail to do the same. In this study, we investigated the inhibitory effect of 2,3-BD on the production of two proinflammatory biomarkers, intreleukin-8 (IL-8) and tumor necrosis factor alpha (TNF-␣), in human intestinal epithelial HT29 and alveolar epithelial A549 cells. Cell-free culture supernatants of El Tor strain N16961 grown in LB supplemented with 1% glucose induced a negligible amount of IL-8 or TNF-␣, while the Classical O395 strain induced much higher levels of these proinflammatory cytokines. On the other hand, three mutant strains constructed from the N16961 strain with defects in the constitutive 2,3-BD pathway were also able to induce high levels of cytokines. When HT29 and A549 cells were treated with bacterial flagella, known proinflammatory cytokine inducers, and chemically synthesized 2,3-BD at various concentrations, a dose-dependent decrease in IL-8 and TNF-␣ production was observed, demonstrating the suppressive effect of 2,3-BD on the production of proinflammatory cytokines in epithelial cells. Upon cotreatment with extraneous 2,3-BD, elevated levels of IB␣, the inhibitor of the NF-B pathway, were detected in both HT29 and A549 cells. Furthermore, treatments containing 2,3-BD elicited lower levels of NF-B-responsive luciferase activity, demonstrating that the reduced cytokine production is likely through the inhibition of the NF-B pathway. These results reveal a novel and potential role of 2,3-BD as an immune modulator that might have conferred a superior pathogenic potential of the El Tor over the Classical biotype.Cholera, an acute watery diarrheal disease, is caused by toxigenic strains of the enteric pathogen Vibrio cholerae and is mainly associated with consumption of contaminated water (39). On the basis of O-antigen typing, V. cholerae has more than 200 identified serogroups, among which only O1 and O139 are reported to be toxigenic. Seven recent pandemics of cholera have been caused by O1 serogroup strains, although O139 strains were reported to be associated with Asiatic cholera epidemics (7, 24, 37). The O1 serogroup of V. cholerae has further been classified into two biotypes, El Tor and Classical. Among the seven worldwide historical pandemics, the Classical strains are presumed to be the etiologic agent for the first six but are only presumed to be the etiologic agent due to the lack of ample epidemiologic surveillance, while the El Tor strains emerged as the major cause during the ongoing seventh pandemic. The reasons behind the extinction of the Classical biotype and the emergence of the El Tor biotype remain unclear, although several hypotheses have been proposed. The tw...

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“…Our results show that the advantage in stationary phase, GASP, is observed in c. 90% (18 of 20) of death‐ or survival‐phase cultures. This frequency of GASP phenotype is similar to that observed in other microorganisms (Zambrano et al ., ; Farrell & Finkel, ; Martinez‐Garcia et al ., ; Silby et al ., ; Dong et al ., ; Pradhan et al ., ). The transition from mid‐log phase to stationary and eventually to starvation phase involves not only changes in gene expression but also changes in the predominant genotype encoded by the population (Thorne & Williams, ; Finkel et al ., ; Zinser & Kolter, ).…”

Section: Discussionmentioning

confidence: 99%

Growth advantage in stationary-phase (GASP) phenotype in long-term survival strains of Geobacter sulfurreducens

Helmus¹,

Liermann²,

Brantley³

2011

FEMS Microbiol Ecol

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Geobacter sulfurreducens exists in the subsurface and has been identified in sites contaminated with radioactive metals, consistent with its ability to reduce metals under anaerobic conditions. The natural state of organisms in the environment is one that lacks access to high concentrations of nutrients, namely electron donors and terminal electron acceptors (TEAs). Most studies have investigated G. sulfurreducens under high-nutrient conditions or have enriched for it in environmental systems via acetate amendments. We replicated the starvation state through long-term batch culture of G. sulfurreducens, where both electron donor and TEA were scarce. The growth curve revealed lag, log, stationary, death, and survival phases using acetate as electron donor and either fumarate or iron(III) citrate as TEA. In survival phase, G. sulfurreducens persisted at a constant cell count for as long as 23 months without replenishment of growth medium. Geobacter sulfurreducens demonstrated an ability to acquire a growth advantage in stationary-phase phenotype (GASP), with strains derived from subpopulations from death- or survival phase being able to out-compete mid-log-phase populations when co-cultured. The molecular basis for GASP was not because of any detectable mutation in the rpoS gene (GSU1525) nor because of a mutation in a putative homolog to Escherichia coli lrp, GSU3370.

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The El Tor Biotype of Vibrio cholerae Exhibits a Growth Advantage in the Stationary Phase in Mixed Cultures with the Classical Biotype

Cited by 29 publications

References 31 publications

Vibrio cholerae Classical Biotype Is Converted to the Viable Non-Culturable State when Cultured with the El Tor Biotype

Vibrio cholerae Classical Biotype Is Converted to the Viable Non-Culturable State when Cultured with the El Tor Biotype

Suppressed Induction of Proinflammatory Cytokines by a Unique Metabolite Produced by Vibrio cholerae O1 El Tor Biotype in Cultured Host Cells

Growth advantage in stationary-phase (GASP) phenotype in long-term survival strains of Geobacter sulfurreducens

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