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Transcriptome sequencing reveals the virulence and environmental genetic programs of Vibrio vulnificus exposed to host and estuarine conditions.

ABSTRACT: Vibrio vulnificus is a natural inhabitant of estuarine waters worldwide and is of medical relevance due to its ability to cause grievous wound infections and/or fatal septicemia. Genetic polymorphisms within the virulence-correlated gene (vcg) serve as a primary feature to distinguish clinical (C-) genotypes from environmental (E-) genotypes. C-genotypes demonstrate superior survival in human serum relative to E-genotypes, and genome comparisons have allowed for the identification of several putative virulence factors that could potentially aid C-genotypes in disease progression. We used RNA sequencing to analyze the transcriptome of C-genotypes exposed to human serum relative to seawater, which revealed two divergent genetic programs under these two conditions. In human serum, cells displayed a distinct "virulence profile" in which a number of putative virulence factors were upregulated, including genes involved in intracellular signaling, substrate binding and transport, toxin and exoenzyme production, and the heat shock response. Conversely, the "environmental profile" exhibited by cells in seawater revealed upregulation of transcription factors such as rpoS, rpoN, and iscR, as well as genes involved in intracellular signaling, chemotaxis, adherence, and biofilm formation. This dichotomous genetic switch appears to be largely governed by cyclic-di-GMP signaling, and remarkably resembles the dual life-style of V. cholerae as it transitions from host to environment. Furthermore, we found a "general stress response" module, known as the stressosome, to be upregulated in seawater. This signaling system has been well characterized in Gram-positive bacteria, however its role in V. vulnificus is not clear. We examined temporal gene expression patterns of the stressosome and found it to be upregulated in natural estuarine waters indicating that this system plays a role in sensing and responding to the environment. This study advances our understanding of gene regulation in V. vulnificus, and brings to the forefront a number of previously overlooked genetic networks.

SUBMITTER: Williams TC

PROVIDER: S-EPMC4260858 | biostudies-literature | 2014

REPOSITORIES: biostudies-literature

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Transcriptome sequencing reveals the virulence and environmental genetic programs of Vibrio vulnificus exposed to host and estuarine conditions.

Williams Tiffany C TC Blackman Elliot R ER Morrison Shatavia S SS Gibas Cynthia J CJ Oliver James D JD

PloS one 20141209 12

Vibrio vulnificus is a natural inhabitant of estuarine waters worldwide and is of medical relevance due to its ability to cause grievous wound infections and/or fatal septicemia. Genetic polymorphisms within the virulence-correlated gene (vcg) serve as a primary feature to distinguish clinical (C-) genotypes from environmental (E-) genotypes. C-genotypes demonstrate superior survival in human serum relative to E-genotypes, and genome comparisons have allowed for the identification of several put ...[more]

PMID: 25489854

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Project description:BackgroundAn attenuated mutant (designated NY303) of Vibrio vulnificus, which causes serious wound infection and septicemia in humans, was isolated fortuitously from a clinical strain YJ016. This mutant was defective in cytotoxicity, migration on soft agar and virulence in the mouse. The purpose of this study was to map the mutation in this attenuated mutant and further explore how the gene thus identified is involved in virulence.MethodsThe whole genome sequence of mutant NY303 determined by next-generation sequencing was compared with that of strain YJ016 to map the mutations. By isolating and characterizing the specific gene-knockout mutants, the gene associated with the phenotype of mutant NY303 was identified. This gene encodes a global regulator, Lrp. A mutant, YH01, deficient in Lrp was isolated and examined in vitro, in vivo and ex vivo to find the affected virulence mechanisms. The target genes of Lrp were further identified by comparing the transcriptomes, which were determined by RNA-seq, of strain YJ016 and mutant YH01. The promoters bound by Lrp were identified by genome footprinting-sequencing, and those related with virulence were further examined by electrophoretic mobility shift assay.ResultsA mutation in lrp was shown to be associated with the reduced cytotoxicity, chemotaxis and virulence of mutant NY303. Mutant YH01 exhibited a phenotype resembling that of mutant NY303, and was defective in colonization in the mouse and growth in mouse serum, but not the antiphagocytosis ability. 596 and 95 genes were down- and up-regulated, respectively, in mutant YH01. Many of the genes involved in secretion of the MARTX cytotoxin, chemotaxis and iron-acquisition were down-regulated in mutant YH01. The lrp gene, which was shown to be negatively autoregulated, and 7 down-regulated virulence-associated genes were bound by Lrp in their promoters. A 14-bp consensus sequence, mkCrTTkwAyTsTG, putatively recognized by Lrp was identified in the promoters of these genes.ConclusionsLrp is a global regulator involved in regulation of cytotoxicity, chemotaxis and iron-acquisition in V. vulnificus. Down-regulation of many of the genes associated with these properties may be responsible, at least partly, for loss of virulence in mutant NY303.

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Transcriptome sequencing reveals the virulence and environmental genetic programs of Vibrio vulnificus exposed to host and estuarine conditions.

Publications

Transcriptome sequencing reveals the virulence and environmental genetic programs of Vibrio vulnificus exposed to host and estuarine conditions.

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