Ecological fitness and virulence features of Vibrio parahaemolyticus in estuarine environments

Lovell, Charles R.

doi:10.1007/s00253-017-8096-9

Cited by 45 publications

(33 citation statements)

References 132 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Vibrio parahaemolyticus is a Gram-negative halophilic bacterium that is mostly disseminated in marine and estuarine surroundings ( Broberg et al, 2011 ; Lovell, 2017 ). Virulent V. parahaemolyticus strains usually cause human acute gastroenteritis after consumption of raw or poorly cooked seafood ( Broberg et al, 2011 ).…”

Section: Introductionmentioning

confidence: 99%

Transcriptional Regulation of the Type VI Secretion System 1 Genes by Quorum Sensing and ToxR in Vibrio parahaemolyticus

et al. 2017

View full text Add to dashboard Cite

Vibrio parahaemolyticus, the leading cause of seafood-associated gastroenteritis, harbors two separate T6SSs on chromosomes 1 and 2, i.e., T6SS1 (VP1386-1420) and T6SS2 (VPA1025-1046). T6SS1 contains at least 7 putative operons: VP1386-1387, VP1388-1390, VP1392-1391, VP1393-1406, VP1400-1406, VP1409-1407, and VP1410-1420. V. parahaemolyticus AphA and OpaR are the two master regulators of quorum sensing (QS) system that are highly expressed at low cell density and high cell density, respectively. ToxR is a membrane-bound virulence regulatory protein conserved across the Vibrio family. In the present work, we show that ToxR coordinates with AphA and OpaR to repress T6SS1 expression in V. parahaemolyticus. OpaR binds to the promoters of VP1388-1390, VP1400-1406, and VP1409-1407 to repress their transcription, but it appears to negatively regulate VP1393-1406 transcription in an indirect manner. By contrast, AphA negatively regulated the above four T6SS1 operons in an indirect manner. In addition, ToxR binds to the promoters of VP1400-1406 and VP1409-1407 to inhibit their transcription, but it presents an indirect interaction with VP1388-1390 and VP1393-1406 promoters. Notably, the expression of ToxR also manifested in a QS-dependent manner and the highest expression occurred at LCD. Meanwhile, the highest expression of T6SS1 occurred at an OD600 value of 0.6 to 0.8 due to the tight regulation of ToxR and QS, suggesting T6SS1 functions only during the mid-logarithmic growth phase. These observations provide significant insight into the molecular mechanism of T6SS1 gene regulation by QS and ToxR in V. parahaemolyticus.

show abstract

Section: Introductionmentioning

confidence: 99%

Transcriptional Regulation of the Type VI Secretion System 1 Genes by Quorum Sensing and ToxR in Vibrio parahaemolyticus

et al. 2017

View full text Add to dashboard Cite

show abstract

“…There has been some consideration of the roles of human virulence determinants in ecological fitness, but the natural context of pathogenic V. parahaemolyticus evolution is still unknown (40)(41)(42). Whereas tdh and T3SS2␣ each may promote growth when bacteria are under predation, isolates that carry trh-containing islands (which likely also have T3SS2␤) do not derive similar benefits from their islands (43).…”

Section: Discussionmentioning

confidence: 99%

Parallel Evolution of Two Clades of an Atlantic-Endemic Pathogenic Lineage of Vibrio parahaemolyticus by Independent Acquisition of Related Pathogenicity Islands

González-Escalona

Drees

et al. 2017

Appl Environ Microbiol

View full text Add to dashboard Cite

Shellfish-transmitted Vibrio parahaemolyticus infections have recently increased from locations with historically low disease incidence, such as the Northeast United States. This change coincided with a bacterial population shift toward human-pathogenic variants occurring in part through the introduction of several Pacific native lineages (ST36, ST43, and ST636) to nearshore areas off the Atlantic coast of the Northeast United States. Concomitantly, ST631 emerged as a major endemic pathogen. Phylogenetic trees of clinical and environmental isolates indicated that two clades diverged from a common ST631 ancestor, and in each of these clades, a human-pathogenic variant evolved independently through acquisition of distinct Vibrio pathogenicity islands (VPaI). These VPaI differ from each other and bear little resemblance to hemolysin-containing VPaI from isolates of the pandemic clonal complex. Clade I ST631 isolates either harbored no hemolysins or contained a chromosome I-inserted island we call VPaIβ that encodes a type 3 secretion system (T3SS2β) typical of Trh hemolysin producers. The more clinically prevalent and clonal ST631 clade II had an island we call VPaIγ that encodes both tdh and trh and that was inserted in chromosome II. VPaIγ was derived from VPaIβ but with some additional acquired elements in common with VPaI carried by pandemic isolates, exemplifying the mosaic nature of pathogenicity islands. Genomics comparisons and amplicon assays identified VPaIγ-type islands containing tdh inserted adjacent to the ure cluster in the three introduced Pacific and most other emergent lineages that collectively cause 67% of infections in the Northeast United States as of 2016. IMPORTANCE The availability of three different hemolysin genotypes in the ST631 lineage provided a unique opportunity to employ genome comparisons to further our understanding of the processes underlying pathogen evolution. The fact that two different pathogenic clades arose in parallel from the same potentially benign lineage by independent VPaI acquisition is surprising considering the historically low prevalence of community members harboring VPaI in waters along the Northeast U.S. coast that could serve as the source of this material. This illustrates a possible predisposition of some lineages to not only acquire foreign DNA but also become human pathogens. Whereas the underlying cause for the expansion of V. parahaemolyticus lineages harboring VPaIγ along the U.S. Atlantic coast and spread of this element to multiple lineages that underlies disease emergence is not known, this work underscores the need to define the environment factors that favor bacteria harboring VPaI in locations of emergent disease.

show abstract

“…The chitinase gene had a 99% blast identity score to the chitinase gene found in the V. vulnificus YJ016 strain; however, the chitinase gene in YJ016 is located on the first chromosome and WR-2-BW’s chitinase gene is located in the second chromosome. Chitinous exoskeletal materials of invertebrates can be a source of carbon and nitrogen for bacteria; vibrios in particular have a well-known association with marine copepods (Kaneko and Colwell 1975 ; Lovell 2017 ). V. cholerae has a well-studied association with copepods, which commonly serve as a vector of cholera infections in Bangladesh water systems (Tamplin et al 1990 ).…”

Section: Discussionmentioning

confidence: 99%

“…The mortality rate of V. vulnificus when it invades the bloodstream (sepsis) increases to 60%. Pathogenesis of both species is complex, and while some virulence factor genes have been implicated, the mechanisms underlying V. vulnificus and V. parahaemolyticus virulence are not well understood (Broberg et al 2011 ; Lovell 2017 ; Klein and Lovell 2016 ).…”

Section: Introductionmentioning

confidence: 99%

Occurrence and significance of pathogenicity and fitness islands in environmental vibrios

2018

Self Cite

View full text Add to dashboard Cite

Pathogenicity islands (PAIs) are large genomic regions that contain virulence genes, which aid pathogens in establishing infections. While PAIs in clinical strains (strains isolated from a human infection) are well-studied, less is known about the occurrence of PAIs in strains isolated from the environment. In this study we describe three PAIs found in environmental Vibrio vulnificus and Vibrio parahaemolyticus strains, as well as a genomic fitness island found in a Vibrio diabolicus strain. All four islands had markedly different GC profiles than the rest of the genome, indicating that all of these islands were acquired via lateral gene transfer. Genes on the PAIs and fitness island were characterized. The PAI found in V. parahaemolyticus contained the tdh gene, a collagenase gene, and genes involved in the type 3 secretion system II (T3SS2). A V. vulnificus environmental strain contained two PAIs, a small 25 kbp PAI and a larger 143 kbp PAI. Both PAIs contained virulence genes. Toxin–antitoxin (TA) genes were found in all three species: on the V. diabolicus fitness island, and on the V. parahaemolyticus and V. vulnificus PAIs.

show abstract

Ecological fitness and virulence features of Vibrio parahaemolyticus in estuarine environments

Cited by 45 publications

References 132 publications

Transcriptional Regulation of the Type VI Secretion System 1 Genes by Quorum Sensing and ToxR in Vibrio parahaemolyticus

Transcriptional Regulation of the Type VI Secretion System 1 Genes by Quorum Sensing and ToxR in Vibrio parahaemolyticus

Parallel Evolution of Two Clades of an Atlantic-Endemic Pathogenic Lineage of Vibrio parahaemolyticus by Independent Acquisition of Related Pathogenicity Islands

Occurrence and significance of pathogenicity and fitness islands in environmental vibrios

Contact Info

Product

Resources

About