Four genomic islands that mark post-1995 pandemic Vibrio parahaemolyticus isolates

Hurley, Catherine C; Quirke, Anne Marie; Reen, F. Jerry; Boyd, E. Fidelma

doi:10.1186/1471-2164-7-104

Cited by 96 publications

(110 citation statements)

References 47 publications

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“…T3SS1 was present in each of the clinical and environmental isolates in this investigation. The tdh PAI (also known as VPAI-7) is composed of 87 coding sequences (in V. parahaemolyticus RIMD2210633) and includes tdhA, tdhS, and the T3SS2␣ genes (38). In our current work, due to multiple ho- mologous areas in the tdh PAI and trh PAI areas, the use of de novo assembly led to this large PAI being split between multiple contigs.…”

Section: Resultsmentioning

confidence: 99%

“…By examining the complete genome of V. parahaemolyticus RIMD2210633, Hurley et al (2006) identified seven genomic islands which occur in pathogenic V. parahaemolyticus isolates (38). VPAI-1, VPAI-4, VPAI-5, and VPAI-6 appeared to represent DNA acquired by pandemic V. parahaemolyticus isolates (38).…”

Section: Fig 2 General Genomic Features Of Clinical V Parahaemolyticmentioning

confidence: 99%

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Genomic Features of Environmental and Clinical Vibrio parahaemolyticus Isolates Lacking Recognized Virulence Factors Are Dissimilar

Ronholm

Petronella

Leung

et al. 2016

Appl Environ Microbiol

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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 tdhand 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. Vibrio parahaemolyticus is a Gram-negative, halophilic bacterium that is ubiquitous in marine and estuarine environments and is often found colonizing shellfish or shrimp. While most strains are nonpathogenic, many have acquired virulence factors that result in illness when individuals are exposed to V. parahaemolyticus strains carrying these virulence factors (1). V. parahaemolyticus is recognized to be a leading cause of foodborne illness worldwide and is transmitted via the handling and consumption of raw or undercooked contaminated seafood (1). Infections occur both sporadically and in very large outbreaks. The most common manifestation of V. parahaemolyticus infection is acute, watery diarrhea accompanied by abdominal pain and nausea, although symptoms can also be severe and include a dysenterylike illness or septicemia (2). Since most cases of illness caused by V. parahaemolyticus are self-limiting, rates of infection are probably underestimated due to underreporting.Clinical V. parahaemolyticus isolates generally have at...

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Section: Resultsmentioning

confidence: 99%

Section: Fig 2 General Genomic Features Of Clinical V Parahaemolyticmentioning

confidence: 99%

Genomic Features of Environmental and Clinical Vibrio parahaemolyticus Isolates Lacking Recognized Virulence Factors Are Dissimilar

Ronholm

Petronella

Leung

et al. 2016

Appl Environ Microbiol

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“…Pathogenicity islands, which possess a wide range of virulent genes, are widespread among bacteria but are the least examined class of MIGEs (7)(8)(9)(10)(11)(12)(13)(14)(15)(16)(17). Excision of PAIs from the bacterial chromosome is thought to be the first step in the transfer and spread of these elements.…”

Section: Discussionmentioning

confidence: 99%

“…Commensal bacteria can be converted into deadly pathogens through HGT of MIGEs that contain virulence factors, or a pathogen may become more virulent with the acquisition of additional virulence factors (1,(4)(5)(6). PAIs were first described for uropathogenic Escherichia coli (UPEC) and have since been described for many pathogenic bacteria (7)(8)(9)(10)(11)(12)(13)(14)(15)(16)(17). PAIs range in size from 10 to 200 kb and have a guanine and cytosine (GC) content that differs from that of the core bacterial chromosome.…”

mentioning

confidence: 99%

Pathogenicity Island Cross Talk Mediated by Recombination Directionality Factors Facilitates Excision from the Chromosome

2016

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Pathogenicity islands (PAIs) are mobile integrated genetic elements (MIGEs) that contain a diverse range of virulence factors and are essential in the evolution of pathogenic bacteria. PAIs are widespread among bacteria and integrate into the host genome, commonly at a tRNA locus, via integrase-mediated site-specific recombination. The excision of PAIs is the first step in the horizontal transfer of these elements and is not well understood. In this study, we examined the role of recombination directionality factors (RDFs) and their relationship with integrases in the excision of two PAIs essential for Vibrio cholerae host colonization: Vibrio pathogenicity island 1 (VPI-1) and VPI-2. VPI-1 does not contain an RDF, which allowed us to answer the question of whether RDFs are an absolute requirement for excision. We found that an RDF was required for efficient excision of VPI-2 but not VPI-1 and that RDFs can induce excision of both islands. Expression data revealed that the RDFs act as transcriptional repressors to both VPI-1-and VPI-2-encoded integrases. We demonstrated that the RDFs Vibrio excision factor A (VefA) and VefB bind at the attachment sites (overlapping the int promoter region) of VPI-1 and VPI-2, thus supporting this mode of integrase repression. In addition, V. cholerae RDFs are promiscuous due to their dual functions of promoting excision of both VPI-1 and VPI-2 and acting as negative transcriptional regulators of the integrases. This is the first demonstration of cross talk between PAIs mediated via RDFs which reveals the complex interactions that occur between separately acquired MIGEs. IMPORTANCEDeciphering the mechanisms of pathogenicity island excision is necessary for understanding the evolution and spread of these elements to their nonpathogenic counterparts. Such mechanistic insight would assist in predicting the mobility of uncharacterized genetic elements. This study identified extensive RDF-mediated cross talk between two nonhomologous VPIs and demonstrated the dual functionality of RDF proteins: (i) inducing PAI excision and (ii) acting as transcriptional regulators. Findings from this study may be implicated in determining the mobilome contribution of other bacteria with multiple MIGEs. Mobile integrative genetic elements (MIGEs) are the vectors of horizontal gene transfer (HGT) among bacteria via the mechanisms of transformation, transduction, and conjugation (1-3). Members of MIGEs include transposons, integrons, bacteriophages, plasmids, and integrative conjugative elements (ICEs)/ conjugative transposons and genomic/pathogenicity islands (GEIs/PAIs). Commensal bacteria can be converted into deadly pathogens through HGT of MIGEs that contain virulence factors, or a pathogen may become more virulent with the acquisition of additional virulence factors (1, 4-6). PAIs were first described for uropathogenic Escherichia coli (UPEC) and have since been described for many pathogenic bacteria (7-17). PAIs range in size from 10 to 200 kb and have a guanine and cytosine (GC) content ...

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“…T3SS-1 is the major contributor to lethality in the intraperitoneal mouse model, and it also plays a minor role in virulence in the infant rabbit model (23). The T3SS-2 gene cluster is flanked by a copy of the tdh gene (tdhA and tdhS) within an 80-kb pathogenicity island named VPaI-7, a region found only in clinical isolates (16,(24)(25)(26). T3SS-2 plays only a minor role in cytotoxicity but is the major contributing factor toward enterotoxicity (17,22,23,27).…”

mentioning

confidence: 99%

Loss of Sigma Factor RpoN Increases Intestinal Colonization of Vibrio parahaemolyticus in an Adult Mouse Model

2014

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bVibrio parahaemolyticus is the leading cause of bacterial seafood-borne gastroenteritis worldwide, yet little is known about how this pathogen colonizes the human intestine. The alternative sigma factor RpoN/sigma-54 is a global regulator that controls flagellar synthesis, as well as a wide range of nonflagellar genes. We constructed an in-frame deletion mutation in rpoN (VP2670) in V. parahaemolyticus RIMD2210633, a clinical serogroup O3:K6 isolate, and examined the effects in vivo using a streptomycintreated mouse model of colonization. We confirmed that deletion of rpoN rendered V. parahaemolyticus nonmotile, and it caused reduced biofilm formation and an apparent defect in glutamine synthetase production. In in vivo competition assays between the rpoN mutant and a wild-type RIMD2210633 strain marked with the ␤-galactosidase gene lacZ (WBWlacZ), the mutant colonized significantly more proficiently. Intestinal persistence competition assays also demonstrated that the rpoN mutant had enhanced fitness and outcompeted WBWlacZ. Mutants defective in the polar flagellum biosynthesis FliAP sigma factor also outcompeted WBWlacZ but not to the same level as the rpoN mutant, which suggested that lack of motility is not the sole cause of the fitness effect. In an in vitro growth competition assay in mouse intestinal mucus, the rpoN mutant also outcompeted the wild type and exhibited faster doubling times when grown in mucus and on individual components of mucus. Genes in the pathways for the catabolism of mucus sugars also had significantly higher expression levels in a ⌬rpoN mutant than in the wild type. These data suggest that in V. parahaemolyticus, RpoN plays an important role in carbon utilization regulation, which may significantly affect host colonization. Vibrio parahaemolyticus is a Gram-negative bacterium ubiquitous in the marine and estuarine environments worldwide (1-4). Vibrio parahaemolyticus is also the leading cause of seafoodassociated bacterial gastroenteritis in the United States and Asia (5, 6), which usually stems from the consumption of raw or undercooked shellfish (7,8). Typically, infection by this organism leads to nausea, vomiting, fever, and a diarrhea distinct from that of the related Vibrio cholerae. Less commonly, infection by V. parahaemolyticus can cause wound infection and septicemia, leading to mortality in immunocompromised individuals (9-12).Much effort has gone into understanding the mechanisms that contribute to V. parahaemolyticus pathogenesis, with a particular focus on virulence factors produced by this bacterium. Strains that caused disease often possessed either the thermostable direct hemolysin (TDH) or the TDH-related hemolysin (TRH), while nonpathogenic strains typically lacked these two markers (13-15). Additionally, sequence analysis of RIMD2210633, an O3:K6 isolate (TDH ϩ TRH Ϫ ), revealed the presence of two type 3 secretion systems (T3SS), one on each chromosome (T3SS-1 and T3SS-2) (16, 17). T3SS-1 is common to both clinical and nonclinical strains of V. parahaemolyticu...

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Four genomic islands that mark post-1995 pandemic Vibrio parahaemolyticus isolates

Cited by 96 publications

References 47 publications

Genomic Features of Environmental and Clinical Vibrio parahaemolyticus Isolates Lacking Recognized Virulence Factors Are Dissimilar

Genomic Features of Environmental and Clinical Vibrio parahaemolyticus Isolates Lacking Recognized Virulence Factors Are Dissimilar

Pathogenicity Island Cross Talk Mediated by Recombination Directionality Factors Facilitates Excision from the Chromosome

Loss of Sigma Factor RpoN Increases Intestinal Colonization of Vibrio parahaemolyticus in an Adult Mouse Model

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