CTXφ contains a hybrid genome derived from tandemly integrated elements

Davis, Brigid M.; Waldor, Matthew K.

doi:10.1073/pnas.140109997

Cited by 70 publications

(55 citation statements)

References 20 publications

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“…In contrast, most El Tor strains produce low but measurable levels of pCTX ET , and it appears that production of pCTX is an early step in CTX synthesis (7). Initially, we believed that pCTX was generated from a prophage by site-specific recombination between the 17-or 18-bp direct repeats that flank each prophage and RS1, since these are known to mediate integration of CTX DNA (16).…”

Section: Resultsmentioning

confidence: 99%

“…The CTX insertion sites in classical strains instead contain either a solitary prophage or a prophage array composed of two truncated, fused prophages. Neither of these arrangements is predicted to yield extrachromosomal CTX phage DNA (7). The inability of classical strains to produce this extrachromosomal replicative form of the classical prophage DNA, which is thought to be an early and critical step in production of virions from CTX prophages (7), probably accounts for the absence of detectable classical CTX (CTX class ).…”

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confidence: 99%

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CTX Prophages in Classical Biotype Vibrio cholerae : Functional Phage Genes but Dysfunctional Phage Genomes

et al. 2000

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CTX is a filamentous, lysogenic bacteriophage whose genome encodes cholera toxin, the primary virulence factor produced by Vibrio cholerae. CTX prophages in O1 El Tor and O139 strains of V. cholerae are found within arrays of genetically related elements integrated at a single locus within the V. cholerae large chromosome. The prophages of O1 El Tor and O139 strains generally yield infectious CTX. In contrast, O1 classical strains of V. cholerae do not produce CTX, although they produce cholera toxin and they contain CTX prophages integrated at two sites. We have identified the second site of CTX prophage integration in O1 classical strains and characterized the classical prophage arrays genetically and functionally. The genes of classical prophages encode functional forms of all of the proteins needed for production of CTX. Classical CTX prophages are present either as solitary prophages or as arrays of two truncated, fused prophages. RS1, a genetic element that is closely related to CTX and is often interspersed with CTX prophages in El Tor strains, was not detected in classical V. cholerae. Our model for CTX production predicts that the CTX prophage arrangements in classical strains will not yield extrachromosomal CTX DNA and thus will not yield virions, and our experimental results confirm this prediction. Thus, failure of O1 classical strains of V. cholerae to produce CTX is due to overall deficiencies in the structures of the arrays of classical prophages, rather than to mutations affecting individual CTX prophage genes.The severe diarrheal disease cholera results from colonization of the human small intestine by pathogenic strains of a gram-negative bacterium, Vibrio cholerae. Cholera has afflicted human populations in many parts of the world for more than a millenium (2). Widespread outbreaks have been common; in the last 200 years alone, seven cholera pandemics have occurred. Most epidemic strains of V. cholerae have been of the O1 serogroup, although in the last 8 years O139 serogroup strains of V. cholerae have also been linked to disease outbreaks (23). The O1 serogroup of V. cholerae has been divided into strains of the classical biotype, thought to have been responsible for the first six cholera pandemics, and the El Tor biotype, which has caused the ongoing seventh pandemic (2). These El Tor and classical strains have traditionally been differentiated in the laboratory with assays of hemolysis, hemagglutination, phage sensitivity, and polymyxin sensitivity and with the Voges-Proskauer reaction (23). Genetic typing of strains has also become possible in recent years. However, despite their phenotypic and genotypic differences, the symptoms of infection with strains of the two O1 biotypes are clinically indistinguishable. The clinical manifestations of cholera are almost entirely due to production of cholera toxin, a potent A-B-type exotoxin that is secreted by pathogenic V. cholerae (10).The genes that encode cholera toxin, ctxAB, reside within the genome of a filamentous, lysogenic bacteriophage k...

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Section: Resultsmentioning

confidence: 99%

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confidence: 99%

CTX Prophages in Classical Biotype Vibrio cholerae : Functional Phage Genes but Dysfunctional Phage Genomes

et al. 2000

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“…Furthermore, the replication of the CTX proviral genome via a rolling-circle-like mechanism occurs between two origins of replication. One is provided by the CTX provirus itself, but the second one is encountered within the downstream RS1 element, thereby leading to the production of hybrid viral genomes composed of DNA sequences contributed by both integrated elements (63,185). Indeed, V. cholerae strains containing a single chromosomally integrated filamentous phage genome have never been isolated (223).…”

Section: Inoviridaementioning

confidence: 99%

Genomics of Bacterial and Archaeal Viruses: Dynamics within the Prokaryotic Virosphere

Krupovìč

Prangishvili

Hendrix

et al. 2011

Microbiol Mol Biol Rev

216

176

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SUMMARY Prokaryotes, bacteria and archaea, are the most abundant cellular organisms among those sharing the planet Earth with human beings (among others). However, numerous ecological studies have revealed that it is actually prokaryotic viruses that predominate on our planet and outnumber their hosts by at least an order of magnitude. An understanding of how this viral domain is organized and what are the mechanisms governing its evolution is therefore of great interest and importance. The vast majority of characterized prokaryotic viruses belong to the order Caudovirales, double-stranded DNA (dsDNA) bacteriophages with tails. Consequently, these viruses have been studied (and reviewed) extensively from both genomic and functional perspectives. However, albeit numerous, tailed phages represent only a minor fraction of the prokaryotic virus diversity. Therefore, the knowledge which has been generated for this viral system does not offer a comprehensive view of the prokaryotic virosphere. In this review, we discuss all families of bacterial and archaeal viruses that contain more than one characterized member and for which evolutionary conclusions can be attempted by use of comparative genomic analysis. We focus on the molecular mechanisms of their genome evolution as well as on the relationships between different viral groups and plasmids. It becomes clear that evolutionary mechanisms shaping the genomes of prokaryotic viruses vary between different families and depend on the type of the nucleic acid, characteristics of the virion structure, as well as the mode of the life cycle. We also point out that horizontal gene transfer is not equally prevalent in different virus families and is not uniformly unrestricted for diverse viral functions.

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“…Several additional genomic regions have also been identified, predominantly among epidemic O1 and O139 serogroup isolates; these include RS1w, Vibrio seventh pandemic island-I (VSP-I), VSP-II and VPI-2 (Faruque et al, 2002;Davis et al, 2002;Dziejman et al, 2002;Jermyn & Boyd, 2002;O'Shea et al, 2004a). RS1w is associated with the CTX prophage in V. cholerae El Tor isolates and is required for the production of CTXw (Davis & Waldor, 2000). VSP-I and VSP-II are genomic islands identified by microarray analysis among V. cholerae El Tor isolates (Dziejman et al, 2002).…”

Section: Introductionmentioning

confidence: 99%

Molecular evolution of Vibrio pathogenicity island-2 (VPI-2): mosaic structure among Vibrio cholerae and Vibrio mimicus natural isolates

Jermyn

Boyd

2005

Microbiology

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Vibrio cholerae is a Gram-negative rod that inhabits the aquatic environment and is the aetiological agent of cholera, a disease that is endemic in much of Southern Asia. The 57·3 kb Vibrio pathogenicity island-2 (VPI-2) is confined predominantly to toxigenic V. cholerae O1 and O139 serogroup isolates and encodes 52 ORFs (VC1758 to VC1809), which include homologues of an integrase (VC1758), a restriction modification system, a sialic acid metabolism gene cluster (VC1773–VC1783), a neuraminidase (VC1784) and a gene cluster that shows homology to Mu phage. In this study, a 14·1 kb region of VPI-2 comprising ORFs VC1773 to VC1787 was identified by PCR and Southern blot analyses in all 17 Vibrio mimicus isolates examined. The VPI-2 region in V. mimicus was inserted adjacent to a serine tRNA similar to VPI-2 in V. cholerae. In 11 of the 17 V. mimicus isolates examined, an additional 5·3 kb region encoding VC1758 and VC1804 to VC1809 was present adjacent to VC1787. The evolutionary history of VPI-2 was reconstructed by comparative analysis of the nanH (VC1784) gene tree with the species gene tree, deduced from the housekeeping gene malate dehydrogenase (mdh), among V. cholerae and V. mimicus isolates. Both gene trees showed an overall congruence; on both gene trees V. cholerae O1 and O139 serogroup isolates clustered together, whereas non-O1/non-O139 serogroup isolates formed separate divergent branches with similar clustering of strains within the branches. One exception was noted: on the mdh gene tree, V. mimicus sequences formed a distinct divergent lineage from V. cholerae sequences; however, on the nanH gene tree, V. mimicus clustered with V. cholerae non-O1/non-O139 isolates, suggesting horizontal transfer of this region between these species.

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CTXφ contains a hybrid genome derived from tandemly integrated elements

Cited by 70 publications

References 20 publications

CTX Prophages in Classical Biotype Vibrio cholerae : Functional Phage Genes but Dysfunctional Phage Genomes

CTX Prophages in Classical Biotype Vibrio cholerae : Functional Phage Genes but Dysfunctional Phage Genomes

Genomics of Bacterial and Archaeal Viruses: Dynamics within the Prokaryotic Virosphere

Molecular evolution of Vibrio pathogenicity island-2 (VPI-2): mosaic structure among Vibrio cholerae and Vibrio mimicus natural isolates

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