Reactivation of the vanchrobactin siderophore system of <i>Vibrio anguillarum</i> by removal of a chromosomal insertion sequence originated in plasmid pJM1 encoding the anguibactin siderophore system

Naka, Hiroaki; López, Clàudia; Crosa, Jorge H.

doi:10.1111/j.1462-2920.2007.01450.x

Cited by 37 publications

(78 citation statements)

References 45 publications

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“…The majority of the genes were conserved throughout the strains; however, the anguibactin biosynthesis and transport genes were found only on the pJM1 plasmid in the 775 strain, although the RV22 strain had homologues of the fatABCD genes. These genes appeared not to be expressed (5,51). The tonB1 and tonB2-ttpC clusters were found in all of the V. anguillarum strains, but only the tonB1 system was identified in V. ordalii.…”

Section: Fig 3 Genomic Islands Of Strain 775 Predicted By Islandviementioning

confidence: 86%

“…The fur gene is located on Chr1, which also harbors the heme determinants, although we have also identified a heme-related V. cholerae hutR homologue on Chr2 (42,48,49,70). Genes involved in ferric vanchrobactin and/or ferric enterobactin transport are located on Chr1, although vanchrobactin biosynthesis in 775 is abrogated by a mutation in vabF and there are no biosynthesis genes for enterobactin (51). It is of interest that potential ABC transporters FvtB-FvtE for vanchrobactin and enterobactin uptake are found on Chr2.…”

Section: Resultsmentioning

confidence: 99%

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Complete Genome Sequence of the Marine Fish Pathogen Vibrio anguillarum Harboring the pJM1 Virulence Plasmid and Genomic Comparison with Other Virulent Strains of V. anguillarum and V. ordalii

et al. 2011

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We dissected the complete genome sequence of the O1 serotype strain Vibrio anguillarum 775(pJM1) and determined the draft genomic sequences of plasmidless strains of serotype O1 (strain 96F) and O2␤ (strain RV22) and V. ordalii. All strains harbor two chromosomes, but 775 also harbors the virulence plasmid pJM1, which carries the anguibactin-producing and cognate transport genes, one of the main virulence factors of V. anguillarum. Genomic analysis identified eight genomic islands in chromosome 1 of V. anguillarum 775(pJM1) and two in chromosome 2. Some of them carried potential virulence genes for the biosynthesis of O antigens, hemolysins, and exonucleases as well as others for sugar transport and metabolism. The majority of genes for essential cell functions and pathogenicity are located on chromosome 1. In contrast, chromosome 2 contains a larger fraction (59%) of hypothetical genes than does chromosome 1 (42%). Chromosome 2 also harbors a superintegron, as well as host "addiction" genes that are typically found on plasmids. Unique distinctive properties include homologues of type III secretion system genes in 96F, homologues of V. cholerae zot and ace toxin genes in RV22, and the biofilm formation syp genes in V. ordalii. Mobile genetic elements, some of them possibly originated in the pJM1 plasmid, were very abundant in 775, resulting in the silencing of specific genes, with only few insertions in the 96F and RV22 chromosomes.Vibrio anguillarum is a marine pathogen that causes vibriosis in close to 50 species of fish, including cultured and wild fish, mollusks, and crustaceans, in marine, brackish, and fresh water (1). Vibriosis is a hemorrhagic septicemia with dire consequences for fish rearing, especially in countries that depend heavily on fish for their food consumption. Despite the fact that V. anguillarum is a dramatic cause of vibriosis in fish, little is known about the genomic composition of this important pathogen. Although 23 serotypes have been reported in V. anguillarum, the O1 and O2 serotypes are the major causative agent of fish vibriosis (32,66,75). Many O1 serotype strains harbor 65-kb pJM1-type plasmids, which carry the siderophore anguibactin biosynthesis and transport genes, a main virulence factor of V. anguillarum, while one of the O1 serotype strains and other serotypes, such as all of the O2 strains, are plasmidless (1, 13, 33, 76). Many virulence factors have been characterized, but we are still far from getting the whole picture of the virulence mechanisms of this pathogen (1, 50). The fact that the pJM1 plasmid is an important component of virulence for the 775 strain but that the other three strains examined do not harbor this plasmid and are still virulent indicates that they must have different mechanisms to cause disease. Moreover, O1 serotype strains cause disease in salmonid fish, whereas O2␤ strains are usually isolated from cod and other nonsalmonids (1, 32, 43). We have previously performed random genome sequencing of V. anguillarum 775 genomic DNA and identified potent...

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Section: Fig 3 Genomic Islands Of Strain 775 Predicted By Islandviementioning

confidence: 86%

Section: Resultsmentioning

confidence: 99%

Complete Genome Sequence of the Marine Fish Pathogen Vibrio anguillarum Harboring the pJM1 Virulence Plasmid and Genomic Comparison with Other Virulent Strains of V. anguillarum and V. ordalii

et al. 2011

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“…This finding is supported by the negative results in all attempts to detect fatDCBA transcripts by RT-PCR (data not shown). Furthermore, Naka et al (28) detected FatA in the OM of strain RV22 only when it was transformed with a pJM1 plasmid. These findings not only demonstrate that the FatA-mediated anguibactin acquisition system is inappropriate for use in the Trojan horse strategy but also bring up interesting questions about the origin and evolution of the vanchrobactin and anguibactin systems in V. anguillarum.…”

Section: Resultsmentioning

confidence: 99%

“…The presence of the pJM1 plasmid, containing most genes necessary for anguibactin production and transport, has been associated with the lack of production of vanchrobactin. Naka et al (28) showed that vabF in the V. anguillarum 775 (a strain carrying pJM1) chromosome is disrupted by the insertion sequence (IS) RS1. In the present study we detected the presence of RS1, an insertion that abolishes vanchrobactin biosynthesis, in vabF in all strains that carry pJM1 or pJM1-like plasmids (Table 3).…”

Section: Resultsmentioning

confidence: 99%

FvtA Is the Receptor for the Siderophore Vanchrobactin inVibrio anguillarum: Utility as a Route of Entry for Vanchrobactin Analogues

Balado

Osorio

Lemos

2009

Appl Environ Microbiol

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Some strains of Vibrio anguillarum, the causative agent of vibriosis in a variety of marine animals, produce a catechol-type siderophore named vanchrobactin. The biosynthetic pathway and regulation of vanchrobactin are quite well understood. However, aspects concerning its entry into the cell have remained uncharacterized. In the present study we characterized two genes, fvtA and orf13, encoding potential TonB-dependent ferricvanchrobactin receptors in serotype O2 V. anguillarum strain RV22. We found that an fvtA mutant was defective for growth under iron limitation conditions and for utilization of vanchrobactin, suggesting that fvtA encodes the vanchrobactin receptor of V. anguillarum. Interestingly, an orf13 mutant was not significantly affected, and results of reverse transcriptase PCR, as well as analysis of outer membrane proteins by sodium dodecyl sulfate-polyacrylamide gel electrophoresis, suggested that this gene is not expressed. Furthermore, fatA, a plasmid gene coding for the anguibactin receptor in plasmid pJM1-harboring strains, is also present in the chromosome of RV22, although it is inactivated by insertion of transposases. In addition, we found that FvtA is the route of entry for vanchrobactin analogues, and there is evidence that it recognizes primarily the catechol-iron center. These analogues are potential candidate vectors for a Trojan horse strategy aimed at generating antimicrobial compounds exploiting the same route of entry for native siderophores. We found that fvtA and vanchrobactin biosynthesis genes are ubiquitous in both vanchrobactin-and anguibactin-producing V. anguillarum strains, which reinforces the utility of the vanchrobactin route of entry for the design of future strategies for the control of vibriosis.Vibrio anguillarum strains possess an array of specific virulence factors that enable them to cause a hemorrhagic septicemia called vibriosis in a variety of marine animals (41). There are more than 20 recognized serotypes, but serotypes O1 and O2 are the serotypes predominantly implicated in vibriosis outbreaks (43). Although the virulence mechanisms of V. anguillarum are not fully understood, it is known that the ability to scavenge iron through utilization of siderophores contributes significantly to the virulence of this bacterium (11,20,45). Currently, two clearly different siderophore-mediated iron uptake systems in V. anguillarum are known. One of them is the vanchrobactin-mediated system encoded by a chromosomal gene cluster. The chemical structure of the siderophore in this system and its biosynthesis and regulation pathways were recently established (3,4,36). The other system is a plasmid pJM1-encoded system called the anguibactin system that is found only in pJM1-containing serotype O1 strains (10, 40), whose synthesis requires additional chromosomal genes that are also involved in vanchrobactin production (1, 4).Uptake of ferric iron-siderophore complexes into the cell requires a specific outer membrane (OM) receptor protein connected to a TonB-ExbB-ExbD complex ...

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“…The FvtE protein is involved in the uptake of vanchrobactin, a chromosomally encoded siderophore found in many V. anguillarum strains (193,194). In strains harboring pJM1-type plasmids, genes of the vanchrobactin system, including the fvtE gene, are present on the chromosome, but this system is inactivated by an insertion in one of the vanchrobactin biosynthesis genes (195).…”

Section: Transportmentioning

confidence: 99%

Plasmid-Encoded Iron Uptake Systems

Lorenzo

Stork

2014

Microbiol Spectr

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Plasmids confer genetic information that benefits the bacterial cells containing them. In pathogenic bacteria, plasmids often harbor virulence determinants that enhance the pathogenicity of the bacterium. The ability to acquire iron in environments where it is limited, for instance the eukaryotic host, is a critical factor for bacterial growth. To acquire iron, bacteria have evolved specific iron uptake mechanisms. These systems are often chromosomally encoded, while those that are plasmid-encoded are rare. Two main plasmid types, ColV and pJM1, have been shown to harbor determinants that increase virulence by providing the cell with essential iron for growth. It is clear that these two plasmid groups evolved independently from each other since they do not share similarities either in the plasmid backbones or in the iron uptake systems they harbor. The siderophores aerobactin and salmochelin that are found on ColV plasmids fall in the hydroxamate and catechol group, respectively, whereas both functional groups are present in the anguibactin siderophore, the only iron uptake system found on pJM1-type plasmids. Besides siderophore-mediated iron uptake, ColV plasmids carry additional genes involved in iron metabolism. These systems include ABC transporters, hemolysins, and a hemoglobin protease. ColV-and pJM1-like plasmids have been shown to confer virulence to their bacterial host, and this trait can be completely ascribed to their encoded iron uptake systems.

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Reactivation of the vanchrobactin siderophore system of Vibrio anguillarum by removal of a chromosomal insertion sequence originated in plasmid pJM1 encoding the anguibactin siderophore system

Cited by 37 publications

References 45 publications

Complete Genome Sequence of the Marine Fish Pathogen Vibrio anguillarum Harboring the pJM1 Virulence Plasmid and Genomic Comparison with Other Virulent Strains of V. anguillarum and V. ordalii

Complete Genome Sequence of the Marine Fish Pathogen Vibrio anguillarum Harboring the pJM1 Virulence Plasmid and Genomic Comparison with Other Virulent Strains of V. anguillarum and V. ordalii

FvtA Is the Receptor for the Siderophore Vanchrobactin inVibrio anguillarum: Utility as a Route of Entry for Vanchrobactin Analogues

Plasmid-Encoded Iron Uptake Systems

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