Abstract
Prevalence of toxigenic Vibrio cholerae O1 in aquatic reservoirs in Bangladesh apparently increases coinciding with the occurrence of seasonal cholera epidemics. In between epidemics, these bacteria persist in water mostly as dormant cells, known as viable but non-culturable cells (VBNC), or conditionally viable environmental cells (CVEC), that fail to grow in routine culture. CVEC resuscitate to active cells when enriched in culture medium supplemented with quorum sensing autoinducers CAI-1 or AI-2 which are signal molecules that regulate gene expression dependent on cell density. V. cholerae O1 mutant strains with inactivated cqsS gene encoding the CAI-1 receptor has been shown to overproduce AI-2 that enhance CVEC resuscitation in water samples. Since V. cholerae non-O1 non-O139 (non-cholera-vibrios) are abundant in aquatic ecosystems, we identified and characterized naturally occurring variant strains of V. cholerae non-O1 non-O139 which overproduce AI-2, and monitored their co-occurrence with V. cholerae O1 in water samples. The nucleotide sequence and predicted protein products of the cqsS gene carried by AI-2 overproducing variant strains showed divergence from that of typical V. cholerae O1 or non-O1 strains, and their culture supernatants enhanced resuscitation of CVEC in water samples. Furthermore, prevalence of V. cholerae O1 in the aquatic environment was found to coincide with an increase in AI-2 overproducing non-O1 non-O139 strains. These results suggest a possible role of non-cholera vibrios in the environmental biology of the cholera pathogen, in which non-O1 non-O139 variant strains overproducing AI-2 presumably contribute in resuscitation of the latent pathogen, leading to seasonal cholera epidemics. Importance. Toxigenic Vibrio cholerae which causes seasonal epidemics of cholera persists in aquatic reservoirs in endemic areas. The bacteria mostly exist in a dormant state during inter-epidemic periods, but periodically resuscitate to the active form. The resuscitation is enhanced by signal molecules called autoinducers (AIs). Toxigenic V. cholerae can be recovered from water samples that normally test negative for the organism in conventional culture, by supplementing the culture medium with exogenous AIs. V. cholerae belonging to the non-O1 non-O139 serogroups which do not cause cholera are also abundant in natural waters, and they are capable of producing AIs. In this study we characterized V. cholerae non-O1 non-O139 variant strains which overproduce an autoinducer called AI-2, and found that the abundance of the cholera pathogen in aquatic reservoirs correlates with an increase in the AI-2 overproducing strains. Our results suggest a probable role of these variant strains in the environmental biology and epidemiology of toxigenic V. cholerae, and may lead to novel means for surveillance, prevention and control of cholera.
Highlights
The natural habitat of the species Vibrio cholerae is the aquatic ecosystem, and comprises more than 250 O-serogroups
To identify V. cholerae non-O1 nonO139 variant strains which might overproduce either of the two autoinducers CAI-1 and AI-2 associated with conditionally viable environmental cells (CVEC) resuscitation, we initially analyzed 61 different isolates of V. cholerae non-O1 non-O139 from water samples using two bioluminescent reporter strains MM920 and BB170 [12,19,20]
We identified 2 strains of V. cholerae non-O1 designated as 86V-1216 and 107V-1216, both of which overproduced the autoinducer AI-2 in their culture supernatants (Fig 1)
Summary
The natural habitat of the species Vibrio cholerae is the aquatic ecosystem, and comprises more than 250 O-serogroups. Quorum sensing in V. cholerae involves at least three autoinducers (CAI-1, AI-2 and DPO) and their respective receptors CqsS, LuxP, and VqmA together with intricate signal transduction cascades [9,10,11,12,13,14]. These three AIs in different combinations may allow V. cholerae to sense the total bacteria in a mixed population as well as the relative concentration of Vibrio cells present, and regulate appropriate metabolic pathways [9]. VqmA activates expression of vqmR gene that encodes the VqmR small RNA (sRNA) [10,15,16] which regulates target mRNAs
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