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

Abstract

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.

Bacterial Genome Instability

“…Second, these systems can stabilize other mobile elements in the cell population. RM genes are often linked to sequences resembling or being mobile genetic elements (within plasmids [254], bacteriophages [255], transposons [256], ICEs [257], integrons [242], or genomic islands [258] or near transposases [259], resolvases [259], invertases [260], integrases [261], topoisomerases [247], or phage-related sequences [262]). Third, they have been described as selfish elements that promote mainly their own survival.…”

The Membrane Proteins SiaQ and SiaM Form an Essential Stoichiometric Complex in the Sialic Acid Tripartite ATP-independent Periplasmic (TRAP) Transporter SiaPQM (VC1777–1779) from Vibrio cholerae

“…The nanA gene is carried on a pathogenicity island (VPI-2) present in toxigenic strains of V. cholerae (20,21), which also encodes a secreted sialidase, that presumably releases the substrate (the common sialic acid N-acetylneuraminic acid) for use by the cell, while at the same time revealing binding sites for the cholera toxin (22). How sialic acid is taken into the cell has not been formally demonstrated, but it is likely to be through a TRAP transporter (VC1777-1779) encoded in the VPI-2, which is orthologous to HiSiaPQM (15, 19 -21, 23, 24).…”

The neuraminidase gene is present in the non-toxigenic Vibrio cholerae Amazonia strain: a different allele in comparison to the pandemic strains

“…In the second lectin wing, comprising 15 β-strands and 2 α-helices, 6 of the substitutions are in β-strands (1 conservative, 5 non-conservative), 1 in an α-helix (nonconservative), and 6 in connection loops. Jermyn and Boyd (2005) used a 0.7 kb PCR fragment from various strains of V. cholerae and V. mimicus, in a study of variation of nanH. A comparison of our data to the corresponding stretch analyzed in that paper shows that the Amazonia strain presents an allele 2 for nanH, identical, in this region, to the allele in strain E714.…”

“…Nucleotides 1105 to 1581 encompass fourteen amino acid substitutions for V. cholerae Amazonia, as compared to only two changes in the region analyzed for various strains (approximately 264 to 858, Jermyn & Boyd 2005).…”

“…Recently, Jermyn and Boyd (2002) showed that the neuraminidase gene, nanH, is present inside a region fulfilling all the criteria to be considered a pathogenicity island. They named this new island as VPI-2, and showed that it is present in its original version in toxigenic strains, being absent in nontoxigenic strains, and present in modified versions in O139 epidemic strains, and also in the sister species V. mimicus (Jermyn & Boyd 2002, 2005 In this paper we report the presence of nanH in V. cholerae Amazonia, sequence the whole gene, compare it to nucleotide and amino acid sequences available for this gene, and map it to a 150 kb NotI fragment of chromosome 1, and the corresponding genomic fragments with the SfiI and I-CeuI enzymes.…”