Characterization and possible functions of a new filamentous bacteriophage from Vibrio cholerae 0139

Jouravleva, Elena A.; McDonald, Gregory A.; Garon, Claude F.; Boesman-Finkelstein, Mary; Finkelstein, Richard A.

doi:10.1099/00221287-144-2-315

Cited by 27 publications

(28 citation statements)

References 36 publications

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“…Seven filamentous bacteriophages hosted by V. cholerae have been described so far: CTXw, fs1, fs2, VSK, 493, VGJw and KSF-1 (Campos et al, 2003b;Ehara et al, 1997;Faruque et al, 2005;Jouravleva et al, 1998;Kar et al, 1996;Nakasone et al, 1998;Waldor & Mekalanos, 1996). Some of them have been implicated in the horizontal transfer of genetic material between strains of V. cholerae.…”

Section: Discussionmentioning

confidence: 99%

“…Vibrio cholerae, the Gram-negative bacterium causing the acute diarrhoeal disease cholera, hosts several filamentous phages (Campos et al, 2003b;Ehara et al, 1997;Faruque et al, 2005;Jouravleva et al, 1998;Kar et al, 1996;Waldor & Mekalanos, 1996). Some of them are able to transduce portions of alien DNA among bacterial populations, including the transmission of virulence genes mediated by different mechanisms of horizontal gene transfer (Campos et al, 2003a;Davis & Waldor, 2003;Faruque et al, 2002).…”

Section: Introductionmentioning

confidence: 99%

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VEJφ, a novel filamentous phage of Vibrio cholerae able to transduce the cholera toxin genes

et al. 2010

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A novel filamentous bacteriophage, designated VEJw, was isolated from strain MO45 of Vibrio cholerae of the O139 serogroup. A molecular characterization of the phage was carried out, which included sequencing of its whole genome, study of the genomic structure, identification of the phage receptor, and determination of the function of some of the genes, such as those encoding the major capsid protein and the single-stranded DNA-binding protein. The genome nucleotide sequence of VEJw, which consists of 6842 bp, revealed that it is organized in modules of functionally related genes in an array that is characteristic of the genus Inovirus (filamentous phages). VEJw is closely related to other previously described filamentous phages of V. cholerae, including VGJw, VSK and fs1. Like these phages, VEJw uses as a cellular receptor the type IV fimbria called the mannose-sensitive haemagglutinin (MSHA). It was also demonstrated that VEJw, like phage VGJw, is able to transmit the genome of phage CTXw, and therefore the genes encoding the cholera toxin (CT), horizontally among populations of V. cholerae expressing the MSHA receptor fimbria. This suggests that the variety of phages implicated in the horizontal transmission of the CT genes could be more diverse than formerly thought.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

VEJφ, a novel filamentous phage of Vibrio cholerae able to transduce the cholera toxin genes

et al. 2010

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“…Phages also play a role in the emergence of pathogenic clones and may also be involved in territorialism between different strains of V. cholerae (3)(4)(5). For example, cholera toxin genes are transferred to nontoxigenic strains through a lysogenic filamentous phage (6), and the emergence and dominance of V. cholerae O139 in Bangladesh and India during 1992-1993 may have involved phages both as a means of horizontal gene transfer as well as a bacteriocidal selective mechanism (3)(4)(5)7). Recently, it has also been recognized that some bacteriophages carry powerful diversitygenerating retroelements (DGR) that are used to alter host range of the phages (8,9).…”

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confidence: 99%

Self-limiting nature of seasonal cholera epidemics: Role of host-mediated amplification of phage

Faruque

Islam

Ahmad

et al. 2005

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

206

248

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Phage predation of Vibrio cholerae has recently been reported to be a factor that influences seasonal epidemics of cholera in Bangladesh.To understand more about this phenomenon, we studied the dynamics of the V. cholerae-phage interaction during a recent epidemic in Dhaka. Because the outbreak strain causing this epidemic was resistant to multiple antibiotics, including streptomycin, we used a selective medium containing streptomycin to monitor accurately the abundance of this strain in the environment. The changing prevalence in the environment of the epidemic V. cholerae O1 strain and a particular lytic cholera phage (JSF4) to which it was sensitive was measured every 48 -72 h for 17 weeks. We also monitored the incidence of phage excretion in stools of 387 cholera patients during the epidemic. The peak of the epidemic was preceded by high V. cholerae prevalence in the environment and was followed by high JSF4 phage levels as the epidemic ended. The buildup to the phage peak in the environment coincided with increasing excretion of the same phage in the stools of cholera patients. These results suggest that patients toward the end of the epidemic ingested both JSF4 phage and the outbreak V. cholerae strain. Host-mediated phage amplification during the cholera epidemic likely contributed to increased environmental phage abundance, decreased load of environmental V. cholerae and, hence, the collapse of the epidemic. Thus, in vivo phage amplification in patients and subsequent phage predation in the environment may explain the self-limiting nature of seasonal cholera epidemics in Bangladesh.Vibrio cholerae ͉ vibriophage T oxigenic strains of Vibrio cholerae belonging to the O1 and O139 serogroups cause cholera, a devastating diarrhea disease that occurs frequently as epidemics in many developing countries (1). Epidemics of cholera occur regularly in the Ganges Delta region of Bangladesh and India. In Bangladesh, outbreaks usually occur twice during a year, with the highest number of cases just after the monsoon and a somewhat smaller number of cholera cases during the spring. The occurrence of epidemics are known to coincide with increased prevalence of the causative V. cholerae strain in the aquatic environment (2). A variety of physical and biological parameters are likely to influence the survival and abundance of V. cholerae as a species in the environment, but these factors do not exclusively modulate the prevalence of toxigenic V. cholerae O1 and O139 strains. In contrast, bacterial viruses (phage or bacteriophage) in the environment have recently been found to inversely correlate with the abundance of toxigenic V. cholerae in water samples and the incidence rates of cholera (3). These data strongly suggest that phage predation in the environment likely influences the temporal dynamics of cholera epidemics. Phages also play a role in the emergence of pathogenic clones and may also be involved in territorialism between different strains of V. cholerae (3-5). For example, cholera toxin genes are transferred ...

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“…More recently, we isolated another related filamentous phage, designated VEJ, from the V. cholerae O139 strain MO45, which is also able to transmit CTX by the mechanism described here mediated by VGJ (results not shown). Phages such as VGJ and VEJ seem to be relatively abundant in strains of the O139 serogroup of V. cholerae, since other related filamentous phages have been isolated from strains of this serogroup, such as VSK, fs1, and 493 (30,31,32,42).…”

Section: Discussionmentioning

confidence: 99%

Novel Type of Specialized Transduction forCTXφ or Its Satellite Phage RS1 Mediated by Filamentous PhageVGJφ in Vibriocholerae

et al. 2003

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The main virulence factor of Vibrio cholerae, the cholera toxin, is encoded by the ctxAB operon, which is contained in the genome of the lysogenic filamentous phage CTX. This phage transmits ctxAB genes between V. cholerae bacterial populations that express toxin-coregulated pilus (TCP), the CTX receptor. In investigating new forms of ctxAB transmission, we found that V. cholerae filamentous phage VGJ, which uses the mannose-sensitive hemagglutinin (MSHA) pilus as a receptor, transmits CTX or its satellite phage RS1 by an efficient and highly specific TCP-independent mechanism. This is a novel type of specialized transduction consisting in the site-specific cointegration of VGJ and CTX (or RS1) replicative forms to produce a single hybrid molecule, which generates a single-stranded DNA hybrid genome that is packaged into hybrid viral particles designated HybP (for the VGJ/CTX hybrid) and HybRS (for the VGJ/RS1 hybrid). The hybrid phages replicate by using the VGJ replicating functions and use the VGJ capsid, retaining the ability to infect via MSHA. The hybrid phages infect most tested strains more efficiently than CTX, even under in vitro optimal conditions for TCP expression. Infection and lysogenization with HybP revert the V. cholerae live attenuated vaccine strain 1333 to virulence. Our results reinforce that TCP is not indispensable for the acquisition of CTX. Thus, we discuss an alternative to the current accepted evolutionary model for the emergence of new toxigenic strains of V. cholerae and the importance of our findings for the development of an environmentally safer live attenuated cholera vaccine.The filamentous phage CTX contains the ctxAB genes encoding cholera toxin (CT), the main virulence factor of the pathogenic gram-negative bacterium Vibrio cholerae (49). In toxigenic El Tor and O139 strains of V. cholerae CTX is integrated at the dif site in the bacterial genome arrayed in different tandem structures along with the related satellite phage RS1 (11,39). The genome of RS1 is a short version of the genome of CTX, which contains genes encoding proteins needed for replication (RstA), integration (RstB), and regulation of gene expression (RstR and RstC) but lacks the genes encoding proteins needed for assembling and secretion of viral particles (Psh, Cep, pIII CTX , Ace, and Zot), as well as CT, which is not necessary for phage morphogenesis (11). Thus, satellite phage RS1 can replicate autonomously but depends on its helper phage CTX for assembly and secretion and thereby for transmission of RS1 viral particles (11). Conversely, RS1 encodes the antirepressor RstC, which is not present in CTX (9). This protein promotes transcription of CTX and RS1 genes by counteracting the activity of the phage repressor RstR (9). Thus, RS1 enhances transmission of both CTX and itself by means of RstC antirepressor activity (9).Classical strains of V. cholerae contain nonfunctional CTX prophages, whereas El Tor and O139 strains contain fully active prophages that produce infective CTX viral particles (10). CTX si...

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Characterization and possible functions of a new filamentous bacteriophage from Vibrio cholerae 0139

Cited by 27 publications

References 36 publications

VEJφ, a novel filamentous phage of Vibrio cholerae able to transduce the cholera toxin genes

VEJφ, a novel filamentous phage of Vibrio cholerae able to transduce the cholera toxin genes

Self-limiting nature of seasonal cholera epidemics: Role of host-mediated amplification of phage

Novel Type of Specialized Transduction forCTXφ or Its Satellite Phage RS1 Mediated by Filamentous PhageVGJφ in Vibriocholerae

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