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Osmoadaptation among Vibrio species and unique genomic features and physiological responses of Vibrio parahaemolyticus.

ABSTRACT: Vibrio parahaemolyticus is a moderately halophilic bacterium found in estuarine and marine coastal ecosystems worldwide. Although the ability of V. parahaemolyticus to grow and proliferate in fluctuating saline environments is well known, the underlying molecular mechanisms of osmoadaptation are unknown. We performed an in silico analysis of V. parahaemolyticus strain RIMD2210633 for genes homologous to osmotic stress response genes in other bacteria. We uncovered two putative compatible solute synthesis systems (encoded by ectABC and betABI) and six putative compatible solute transporters (encoded by four bcct loci and two proVWX loci). An ectoine synthesis system clustered with a betaine/carnitine/choline transporter and a ProU transporter (encoded by homologues of proVWX from Escherichia coli), and a betaine synthesis system clustered with a ProU transporter (encoded by homologues of proVXW from Pseudomonas syringae). This is at least double the number present in V. cholerae, V. fischeri, or V. vulnificus. Six additional Vibrio species contain both ectABC and betABI, i.e., V. alginolyticus 12G01, V. angustum, V. harveyi BAA-1116, V. splendidus LGP32, Vibrio sp. strain MED222, and Vibrio sp. strain Ex25. V. harveyi HY01 and V. splendidus 12B01 only encoded the betaine system. In addition, V. alginolyticus had a compendium of systems identical to that found in V. parahaemolyticus. Comparative physiological analysis of RIMD2210633 with V. vulnificus YJ016, V. cholerae N16961, and V. fischeri ES114 grown at different salinities and temperatures demonstrated that V. parahaemolyticus had a growth advantage under all of the conditions examined. We demonstrate, by one-dimensional nuclear magnetic resonance analysis, that V. parahaemolyticus is capable of de novo synthesis of ectoine at high salinity whereas a Delta ectB knockout strain is not. We constructed a single-knockout mutation in proU1, but no growth defect was noted, indicating transporter system redundancy. We complemented E. coli MKH13, a compatible solute transporter-negative strain, with bcct2 and demonstrated uptake of betaine at high salt concentrations.

SUBMITTER: Naughton LM

PROVIDER: S-EPMC2681680 | biostudies-literature | 2009 May

REPOSITORIES: biostudies-literature

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Osmoadaptation among Vibrio species and unique genomic features and physiological responses of Vibrio parahaemolyticus.

Naughton Lynn M LM Blumerman Seth L SL Carlberg Megan M Boyd E Fidelma EF

Applied and environmental microbiology 20090313 9

Vibrio parahaemolyticus is a moderately halophilic bacterium found in estuarine and marine coastal ecosystems worldwide. Although the ability of V. parahaemolyticus to grow and proliferate in fluctuating saline environments is well known, the underlying molecular mechanisms of osmoadaptation are unknown. We performed an in silico analysis of V. parahaemolyticus strain RIMD2210633 for genes homologous to osmotic stress response genes in other bacteria. We uncovered two putative compatible solute ...[more]

PMID: 19286794

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Project description:Vibrio parahaemolyticus is a bacterial pathogen that can cause illness after the consumption or handling of contaminated seafood. The primary virulence factors associated with V. parahaemolyticus illness are thermostable direct hemolysin (TDH) and Tdh-related hemolysin (TRH). However, clinical strains lacking tdh and trh have recently been isolated, and these clinical isolates are poorly understood. To help understand the emergence of clinical tdh- and trh-negative isolates, a genomic approach was used to comprehensively compare 4 clinical tdh- and trh-negative isolates with 16 environmental tdh- and trh-negative isolates and 34 clinical isolates positive for tdh or trh, or both, with the objective of identifying genomic features that are unique to clinical tdh- and trh-negative isolates. The prevalence of pathogenicity islands (PAIs) common to clinical isolates was thoroughly examined in each of the clinical tdh- and trh-negative isolates. The tdh PAI was not present in any clinical or environmental tdh- and trh-negative isolates. The trh PAI was not present in any environmental isolates; however, in clinical tdh- and trh-negative isolate 10-4238, the majority of the trh PAI including a partial trh1 gene was present, which resulted in reclassification of this isolate as a tdh-negative and trh-positive isolate. In the other clinical tdh- and trh-negative isolates, neither the trh gene nor the trh PAI was present. We identified 862 genes in clinical tdh- and trh-negative isolates but not in environmental tdh- and trh-negative isolates. Many of these genes are highly homologous to genes found in common enteric bacteria and included genes encoding a number of chemotaxis proteins and a novel putative type VI secretion system (T6SS) effector and immunity protein (T6SS1). The availability of genome sequences from clinical V. parahaemolyticus tdh- and trh-negative isolates and the comparative analysis may help provide an understanding of how this pathotype is able to survive in vivo during clinical illness.

Project description:Vibrio parahaemolyticus is a bacterial pathogen that becomes lethal to Penaeus shrimps when acquiring the pVA1-type plasmid carrying the PirABvp genes, causing acute hepatopancreatic necrosis disease (AHPND). This disease causes significant losses across the world, with outbreaks reported in Southeast Asia, Mexico, and South America. Virulence level and mortality differences have been reported in isolates from different locations, and whether this phenomenon is caused by plasmid-related elements or genomic-related elements from the bacteria remains unclear. Here, nine genomes of South American AHPND-causing V. parahaemolyticus (VPAHPND) isolates were assembled and analyzed using a comparative genomics approach at (i) whole-genome, (ii) secretion system, and (iii) plasmid level, and then included for a phylogenomic analysis with another 86 strains. Two main results were obtained from our analyses. First, all isolates contained pVA1-type plasmids harboring the toxin coding genes, and with high similarity with the prototypical sequence of Mexican-like origin, while phylogenomic analysis showed some level of heterogeneity with discrete clusters and wide diversity compared to other available genomes. Second, although a high genomic similarity was observed, variation in virulence genes and clusters was observed, which might be relevant in the expression of the disease. Overall, our results suggest that South American pathogenic isolates are derived from various genetic lineages which appear to have acquired the plasmid through horizontal gene transfer. Furthermore, pathogenicity seems to be a multifactorial trait where the degree of virulence could be altered by the presence or variations of several virulence factors. IMPORTANCE AHPND have caused losses of over $2.6 billion to the aquaculture industry around the world due to its high mortality rate in shrimp farming. The most common etiological agent is V. parahaemolyticus strains possessing the pVA1-type plasmid carrying the PirABvp toxin. Nevertheless, complete understanding of the role of genetic elements and their impact in the virulence of this pathogen remains unclear. In this work, we analyzed nine South American AHPND-causing V. parahaemolyticus isolates at a genomic level, and assessed their evolutionary relationship with other 86 strains. We found that all our isolates were highly similar and possessed the Mexican-type plasmid, but their genomic content did not cluster with other Mexican strains, but instead were spread across all isolates. These results suggest that South American VPAHPND have different genetic backgrounds, and probably proceed from diverse geographical locations, and acquire the pVA1-type plasmid via horizontal gene transfer at different times.

Project description:BackgroundVibrio parahaemolyticus is a common cause of foodborne disease. Beginning in 1996, a more virulent strain having serotype O3:K6 caused major outbreaks in India and other parts of the world, resulting in the emergence of a pandemic. Other serovariants of this strain emerged during its dissemination and together with the original O3:K6 were termed strains of the pandemic clone. Two genomes, one of this virulent strain and one pre-pandemic strain have been sequenced. We sequenced four additional genomes of V. parahaemolyticus in this study that were isolated from different geographical regions and time points. Comparative genomic analyses of six strains of V. parahaemolyticus isolated from Asia and Peru were performed in order to advance knowledge concerning the evolution of V. parahaemolyticus; specifically, the genetic changes contributing to serotype conversion and virulence. Two pre-pandemic strains and three pandemic strains, isolated from different geographical regions, were serotype O3:K6 and either toxin profiles (tdh+, trh-) or (tdh-, trh+). The sixth pandemic strain sequenced in this study was serotype O4:K68.ResultsGenomic analyses revealed that the trh+ and tdh+ strains had different types of pathogenicity islands and mobile elements as well as major structural differences between the tdh pathogenicity islands of the pre-pandemic and pandemic strains. In addition, the results of single nucleotide polymorphism (SNP) analysis showed that 94% of the SNPs between O3:K6 and O4:K68 pandemic isolates were within a 141 kb region surrounding the O- and K-antigen-encoding gene clusters. The "core" genes of V. parahaemolyticus were also compared to those of V. cholerae and V. vulnificus, in order to delineate differences between these three pathogenic species. Approximately one-half (49-59%) of each species' core genes were conserved in all three species, and 14-24% of the core genes were species-specific and in different functional categories.ConclusionsOur data support the idea that the pandemic strains are closely related and that recent South American outbreaks of foodborne disease caused by V. parahaemolyticus are closely linked to outbreaks in India. Serotype conversion from O3:K6 to O4:K68 was likely due to a recombination event involving a region much larger than the O-antigen- and K-antigen-encoding gene clusters. Major differences between pathogenicity islands and mobile elements are also likely driving the evolution of V. parahaemolyticus. In addition, our analyses categorized genes that may be useful in differentiating pathogenic Vibrios at the species level.

Project description:Vibrio parahaemolyticus is a Gram-negative marine bacterium. A limited population of the organisms causes acute gastroenteritis in humans. Almost all of the clinical V. parahaemolyticus isolates exhibit a beta-type hemolysis on Wagatsuma agar, known as the Kanagawa phenomenon (KP). KP is induced by the thermostable direct hemolysin (TDH) produced by the organism, and has been considered a crucial marker to distinguish pathogenic strains from non-pathogenic ones. Since 1996, so-called âpandemic clonesâ, the majority of which belong to serotype O3:K6, have caused worldwide outbreaks of gastroenteritis. In this study, we used a DNA microarray constructed based on the genome sequence of a pandemic V. parahaemolyticus strain RIMD2210633 to examin the genomic composition of 22 strains of V. parahaemolyticus, including both pathogenic (pandemic as well as non-pandemic) and non-pathogenic strains. Over 85% of the RIMD2210633 genes were conserved in all the strains tested. Many of variably present genes formed gene clusters on the genome of RIMD2210633 and were probably acquired through lateral gene transfer. At least 70 genes over 10 loci were specifically present in the pandemic strains when compared with any of the non-pandemic strains, suggesting that the difference between pandemic and non-pandemic strains is not due to a simple genetic event. Only the genes in the 80-kb pathogenicity island (Vp-PAI) on chromosome II, including two tdh genes and a set of genes for the Type III secretion system, were detected only in the KP-positive pathogenic strains. These results strongly suggest that acquisition of this Vp-PAI was crucial for the emergence of V. parahaemolyticus strains that are pathogenic for humans. Keywords: comparative genomic hybridization, CGH Total 66 test samples were analyzed. Genomic DNA from each test strain and a reference strain (RIMD2210633) were labeled with Cy3 and Cy5, respectively, and were cohybridized on a single array. Labeling and hybridization were performed three times independently.

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Osmoadaptation among Vibrio species and unique genomic features and physiological responses of Vibrio parahaemolyticus.

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Osmoadaptation among Vibrio species and unique genomic features and physiological responses of Vibrio parahaemolyticus.

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