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

Campos, Javier; Martínez, Eriel; Izquierdo, Yovanny; Fando, Rafael

doi:10.1099/mic.0.032235-0

Cited by 38 publications

(32 citation statements)

References 30 publications

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“…1), each sharing similarity in size, genome position, and sequence with the corresponding capsid proteins of other filamentous phages (3,4,8,9). For instance, ORF6 exhibits similar size and genome position to gIII of CTX, which encodes a minor capsid protein, pIII, that recognizes and interacts with receptors and coreceptors.…”

Section: Resultsmentioning

confidence: 99%

High Frequency of a Novel Filamentous Phage, VCYϕ, within an Environmental Vibrio cholerae Population

Xue

Boucher

et al. 2012

Appl Environ Microbiol

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Environmental Vibrio cholerae strains isolated from a coastal brackish pond (Oyster Pond, Woods Hole, MA) carried a novel filamentous phage, VCY, which can exist as a host genome integrative form (IF) and a plasmid-like replicative form (RF). Outside the cell, the phage displays a morphology typical of Inovirus, with filamentous particles ϳ1.8 m in length and 7 nm in width. Four independent RF isolates had identical genomes, except for 8 single nucleotide polymorphisms clustered in two regions. The overall genome size is 7,103 bp with 11 putative open reading frames organized into three functional modules (replication, structure and assembly, and regulation). VCY shares sequence similarity with other filamentous phages (including cholera disease-associated CTX) in a highly mosaic manner, indicating evolution by horizontal gene transfer and recombination. VCY integrates in the vicinity of the putative translation initiation factor Sui1 in chromosome II of V. cholerae. A screen of 531 closely related host isolates showed that ϳ40% harbored phages, with 27% and 13% carrying the IF and RF, respectively. The relative frequencies of the RF and IF differed among strains isolated from the pond or lagoon of Oyster Pond, suggesting that the host habitat influences intracellular phage biology. The overall high prevalence within the host population shows that filamentous phages can be an important component of the environmental biology of V. cholerae. Filamentous phages of the genus Inovirus are unusual among bacterial viruses in that they do not lyse host cells when new phage particles are produced. Instead, new virions are packaged on the cell surface and extruded (24). These virions contain singlestranded DNA (ssDNA) that typically enters new hosts via a variety of pili positioned on the cell surface (26). Inside the host, inoviruses can persist as a circular, double-stranded replicative form (RF); alternatively, they can integrate into the host chromosome by a variety of mechanisms, including phage-encoded transposases (19) and host-encoded XerC/D (11, 13), which normally resolve chromosome dimers. Production of new phage ssDNA can proceed via rolling-circle replication from the RF. The genomes of inoviruses are composed of modules that encode genome replication, virion structure and assembly, and regulation (3); additionally, like many other phages, inoviruses can undergo extensive recombination, often picking up new genes in the process so that they may act as important mechanisms of gene transfer among hosts (7,9).Vibrio cholerae, an environmental bacterium containing strains capable of eliciting the diarrheal disease cholera, has become somewhat of a model for studying Inovirus biology and diversity. This is because an important pathogenicity factor, the cholera toxin (CT), is encoded and transferred by the filamentous phage CTX (21). Infection is mediated by the recognition of a type IV pilus (toxin-coregulated pilus), and the phage genome can irreversibly integrate into the host chromosome at one of two dif sites ...

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Section: Resultsmentioning

confidence: 99%

High Frequency of a Novel Filamentous Phage, VCYϕ, within an Environmental Vibrio cholerae Population

Xue

Boucher

et al. 2012

Appl Environ Microbiol

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“…Also seen were the expected diversity of lysins (Seo et al 2010), holins (Wang et al 2000), bacteriocins (Dawid et al 2007), restriction/modification systems (Kobayashi 2001), and virulence factors (O'Brien et al 1984;Lainhart et al 2009;Campos et al 2010).…”

Section: Genome Research 1621mentioning

confidence: 99%

The human gut virome: Inter-individual variation and dynamic response to diet

Minot¹,

Sinha²,

Chen³

et al. 2011

Genome Res.

822

902

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Immense populations of viruses are present in the human gut and other body sites. Understanding the role of these populations (the human “virome”) in health and disease requires a much deeper understanding of their composition and dynamics in the face of environmental perturbation. Here, we investigate viromes from human subjects on a controlled feeding regimen. Longitudinal fecal samples were analyzed by metagenomic sequencing of DNA from virus-like particles (VLP) and total microbial communities. Assembly of 336 Mb of VLP sequence yielded 7175 contigs, many identifiable as complete or partial bacteriophage genomes. Contigs were rich in viral functions required in lytic and lysogenic growth, as well as unexpected functions such as viral CRISPR arrays and genes for antibiotic resistance. The largest source of variance among virome samples was interpersonal variation. Parallel deep-sequencing analysis of bacterial populations showed covaration of the virome with the larger microbiome. The dietary intervention was associated with a change in the virome community to a new state, in which individuals on the same diet converged. Thus these data provide an overview of the composition of the human gut virome and associate virome structure with diet.

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“…This transfer may have been facilitated by the JUMPstart sequence, which has nucleotide similarity to a DNA uptake signal that causes the preferential uptake of free DNA containing that sequence in the Pasteurellaceae and is present in front of a laterally transferred O-antigen region in V. cholerae (20). DNA transfer in V. cholerae also occurs by phage transduction (7,21).Numerous studies have focused on the variability and origins of O-antigen genes in enteric bacteria. Reeves et al (35,36) have undertaken extensive studies of the genetic basis of Oantigen variation in Salmonella enterica and Escherichia coli.…”

mentioning

confidence: 99%

mentioning

confidence: 99%

Genetic Diversity of O-Antigen Biosynthesis Regions in Vibrio cholerae

Aydanian

Tang

Morris

et al. 2011

Appl Environ Microbiol

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O-antigen biosynthetic (wbf) regions for Vibrio cholerae serogroups O5, O8, and O108 were isolated and sequenced. Sequences were compared to those of other published V. cholerae O-antigen regions. These wbf regions showed a high degree of heterogeneity both in gene content and in gene order. Genes identified frequently showed greater similarities to polysaccharide biosynthesis genes from species other than V. cholerae. Our results demonstrate the plasticity of O-antigen genes in V. cholerae, the diversity of the genetic pool from which they are drawn, and the likelihood that new pandemic serogroups will emerge.Cholera is a pandemic diarrheal disease that continues to be an important cause of morbidity and mortality worldwide. Cholera is associated with a clonally related subset of Vibrio cholerae strains, which carry ctxAB (cholera toxin subunits A and B), the vibrio pathogenicity island (VPI), and other cholera-associated genes (15,40). Until 1992, only serogroup O1 (out of more than 206 serogroups currently described) was recognized as a cause of cholera. In 1992, a new, non-O1 V. cholerae strain (subsequently designated V. cholerae O139) appeared in India and rapidly spread across much of Asia (32). Extensive studies (5,12,31,41) demonstrated that the O139 strain was closely related to the O1 El Tor strains of the 7th pandemic, except that the genes responsible for O1-antigen biosynthesis were deleted and replaced with DNA that encodes the O139 antigen. Since the O antigen is the major protective epitope, its alteration was sufficient to allow O139 strains to move in epidemic form through populations previously immune to cholera caused by O1. Thus, adults were more commonly affected than children (1). Recent studies suggest that the pandemic cluster carries other serogroups as well, including O37, O27, O53, O65, and O75 (31, 40, 43). These observations are consistent with the hypothesis that pathogenic V. cholerae strains are able to easily acquire and/or exchange O-antigen genes, with the new O antigen allowing strains to evade preexisting immunity to cholera.Changes in O-antigen structure also may provide selective advantages in the environment. During epidemics, bacteriophage may play a crucial role in controlling the number of V. cholerae in the environment (19), and since the O-antigen may serve as bacteriophage receptors, serogroup conversion also may be beneficial for evading phage predation (33). It is well documented that mobile genetic elements, bacteriophage, and the competence of V. cholerae to take up and assimilate free DNA from the environment significantly contribute to genetic diversity in V. cholerae (18). Serogroup conversion was demonstrated while V. cholerae was growing on a chitin substrate (6). This transfer may have been facilitated by the JUMPstart sequence, which has nucleotide similarity to a DNA uptake signal that causes the preferential uptake of free DNA containing that sequence in the Pasteurellaceae and is present in front of a laterally transferred O-antigen region in V. chole...

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

Cited by 38 publications

References 30 publications

High Frequency of a Novel Filamentous Phage, VCYϕ, within an Environmental Vibrio cholerae Population

High Frequency of a Novel Filamentous Phage, VCYϕ, within an Environmental Vibrio cholerae Population

The human gut virome: Inter-individual variation and dynamic response to diet

Genetic Diversity of O-Antigen Biosynthesis Regions in Vibrio cholerae

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