1887

Abstract

Most Vibrio parahaemolyticus isolates found in marine environments are non-pathogenic; however, certain lineages have acquired genomic pathogenicity islands (PAIs) that enable these isolates to cause human illness. The V. parahaemolyticus PAI contains one or both of two toxins: thermostable direct haemolysin (TDH) or TDH-related haemolysin (TRH) and type III secretion system 2 (T3SS2). Recently, a few V. parahaemolyticus isolates that do not have this PAI were obtained from clinical samples, and there has been interest in determining whether these isolates possess novel virulence factors. In this investigation, we have selected four V. parahaemolyticus isolates: a canonical pathogenic strain containing TDH, TRH and T3SS2; two strains from clinical cases which do not contain a PAI; and an environmental isolate which also does not contain a PAI. For each isolate, we analyzed differential gene expression after crude bile exposure. Several enteric bacterial pathogens are known to use bile as a signal to enhance virulence gene expression. We have shown that in the tdh-positive trh-positive pathotype gene virulence gene expression was not up-regulated in response to crude bile, strongly indicating that the current dogma of virulence gene regulation in V. parahaemolyticus needs to be revisited and separately investigated for each pathotype. In addition, we have created a list of genes of interest that were up-regulated in the non-canonical pathotypes which may contribute to virulence in these isolates.

Loading

Article metrics loading...

/content/journal/mgen/10.1099/mgen.0.000182
2018-05-29
2019-10-16
Loading full text...

Full text loading...

/deliver/fulltext/mgen/4/6/mgen000182.html?itemId=/content/journal/mgen/10.1099/mgen.0.000182&mimeType=html&fmt=ahah

References

  1. Ceccarelli D, Hasan NA, Huq A, Colwell RR. Distribution and dynamics of epidemic and pandemic Vibrio parahaemolyticus virulence factors. Front Cell Infect Microbiol 2013;3:97 [CrossRef][PubMed]
    [Google Scholar]
  2. Joseph SW, Colwell RR, Kaper JB. Vibrio parahaemolyticus and related halophilic Vibrios. Crit Rev Microbiol 1982;10:77–124 [CrossRef][PubMed]
    [Google Scholar]
  3. Nishibuchi M, Fasano A, Russell RG, Kaper JB. Enterotoxigenicity of Vibrio parahaemolyticus with and without genes encoding thermostable direct hemolysin. Infect Immun 1992;60:3539–3545[PubMed]
    [Google Scholar]
  4. Honda T, Ni Y, Miwatani T, Adachi T, Kim J. The thermostable direct hemolysin of Vibrio parahaemolyticus is a pore-forming toxin. Can J Microbiol 1992;38:1175–1180 [CrossRef][PubMed]
    [Google Scholar]
  5. Broberg CA, Calder TJ, Orth K. Vibrio parahaemolyticus cell biology and pathogenicity determinants. Microbes Infect 2011;13:992–1001 [CrossRef][PubMed]
    [Google Scholar]
  6. Hiyoshi H, Kodama T, Iida T, Honda T. Contribution of Vibrio parahaemolyticus virulence factors to cytotoxicity, enterotoxicity, and lethality in mice. Infect Immun 2010;78:1772–1780 [CrossRef][PubMed]
    [Google Scholar]
  7. Matsuda S, Kodama T, Okada N, Okayama K, Honda T et al. Association of Vibrio parahaemolyticus thermostable direct hemolysin with lipid rafts is essential for cytotoxicity but not hemolytic activity. Infect Immun 2010;78:603–610 [CrossRef][PubMed]
    [Google Scholar]
  8. Makino K, Oshima K, Kurokawa K, Yokoyama K, Uda T et al. Genome sequence of Vibrio parahaemolyticus: a pathogenic mechanism distinct from that of V. cholerae. Lancet 2003;361:743–749 [CrossRef][PubMed]
    [Google Scholar]
  9. Izutsu K, Kurokawa K, Tashiro K, Kuhara S, Hayashi T et al. Comparative genomic analysis using microarray demonstrates a strong correlation between the presence of the 80-kilobase pathogenicity island and pathogenicity in Kanagawa phenomenon-positive Vibrio parahaemolyticus strains. Infect Immun 2008;76:1016–1023 [CrossRef][PubMed]
    [Google Scholar]
  10. Sugiyama T, Iida T, Izutsu K, Park KS, Honda T. Precise region and the character of the pathogenicity island in clinical Vibrio parahaemolyticus strains. J Bacteriol 2008;190:1835–1837 [CrossRef][PubMed]
    [Google Scholar]
  11. Okada N, Iida T, Park KS, Goto N, Yasunaga T et al. Identification and characterization of a novel type III secretion system in trh-positive Vibrio parahaemolyticus strain TH3996 reveal genetic lineage and diversity of pathogenic machinery beyond the species level. Infect Immun 2009;77:904–913 [CrossRef][PubMed]
    [Google Scholar]
  12. Ham H, Orth K. The role of type III secretion system 2 in Vibrio parahaemolyticus pathogenicity. J Microbiol 2012;50:719–725 [CrossRef][PubMed]
    [Google Scholar]
  13. Yu Y, Yang H, Li J, Zhang P, Wu B et al. Putative type VI secretion systems of Vibrio parahaemolyticus contribute to adhesion to cultured cell monolayers. Arch Microbiol 2012;194:827–835 [CrossRef][PubMed]
    [Google Scholar]
  14. Salomon D, Kinch LN, Trudgian DC, Guo X, Klimko JA et al. Marker for type VI secretion system effectors. Proc Natl Acad Sci USA 2014;111:9271–9276 [CrossRef][PubMed]
    [Google Scholar]
  15. Boyer F, Fichant G, Berthod J, Vandenbrouck Y, Attree I. Dissecting the bacterial type VI secretion system by a genome wide in silico analysis: what can be learned from available microbial genomic resources?. BMC Genomics 2009;10:104 [CrossRef][PubMed]
    [Google Scholar]
  16. Ronholm J, Petronella N, Chew Leung C, Pightling AW, Banerjee SK. Genomic features of environmental and clinical Vibrio parahaemolyticus isolates lacking recognized virulence factors are dissimilar. Appl Environ Microbiol 2016;82:1102–1113 [CrossRef][PubMed]
    [Google Scholar]
  17. Lüdeke CH, Kong N, Weimer BC, Fischer M, Jones JL. Complete genome sequences of a clinical isolate and an environmental isolate of Vibrio parahaemolyticus. Genome Announc 2015;3:e00216-15 [CrossRef][PubMed]
    [Google Scholar]
  18. Meador CE, Parsons MM, Bopp CA, Gerner-Smidt P, Painter JA et al. Virulence gene- and pandemic group-specific marker profiling of clinical Vibrio parahaemolyticus isolates. J Clin Microbiol 2007;45:1133–1139 [CrossRef][PubMed]
    [Google Scholar]
  19. Bhoopong P, Palittapongarnpim P, Pomwised R, Kiatkittipong A, Kamruzzaman M et al. Variability of properties of Vibrio parahaemolyticus strains isolated from individual patients. J Clin Microbiol 2007;45:1544–1550 [CrossRef][PubMed]
    [Google Scholar]
  20. Jones JL, Lüdeke CH, Bowers JC, Garrett N, Fischer M et al. Biochemical, serological, and virulence characterization of clinical and oyster Vibrio parahaemolyticus isolates. J Clin Microbiol 2012;50:2343–2352 [CrossRef][PubMed]
    [Google Scholar]
  21. Banerjee SK, Kearney AK, Nadon CA, Peterson CL, Tyler K et al. Phenotypic and genotypic characterization of Canadian clinical isolates of Vibrio parahaemolyticus collected from 2000 to 2009. J Clin Microbiol 2014;52:1081–1088 [CrossRef][PubMed]
    [Google Scholar]
  22. Hazen TH, Lafon PC, Garrett NM, Lowe TM, Silberger DJ et al. Insights into the environmental reservoir of pathogenic Vibrio parahaemolyticus using comparative genomics. Front Microbiol 2015;6:1–14 [CrossRef][PubMed]
    [Google Scholar]
  23. Hung DT, Mekalanos JJ. Bile acids induce cholera toxin expression in Vibrio cholerae in a ToxT-independent manner. Proc Natl Acad Sci USA 2005;102:3028–3033 [CrossRef][PubMed]
    [Google Scholar]
  24. Edwards AD, Slater NK. Protection of live bacteria from bile acid toxicity using bile acid adsorbing resins. Vaccine 2009;27:3897–3903 [CrossRef][PubMed]
    [Google Scholar]
  25. Sistrunk JR, Nickerson KP, Chanin RB, Rasko DA, Faherty CS. Survival of the fittest: how bacterial pathogens utilize bile to enhance infection. Clin Microbiol Rev 2016;29:819–836 [CrossRef][PubMed]
    [Google Scholar]
  26. Hamer HM, de Preter V, Windey K, Verbeke K. Functional analysis of colonic bacterial metabolism: relevant to health?. Am J Physiol Gastrointest Liver Physiol 2012;302:G1–G9 [CrossRef]
    [Google Scholar]
  27. Osawa R, Yamai S. Production of thermostable direct hemolysin by Vibrio parahaemolyticus enhanced by conjugated bile acids. Appl Environ Microbiol 1996;62:3023–3025[PubMed]
    [Google Scholar]
  28. Pace JL, Chai TJ, Rossi HA, Jiang X. Effect of bile on Vibrio parahaemolyticus. Appl Environ Microbiol 1997;63:2372–2377[PubMed]
    [Google Scholar]
  29. Gotoh K, Kodama T, Hiyoshi H, Izutsu K, Park KS et al. Bile acid-induced virulence gene expression of Vibrio parahaemolyticus reveals a novel therapeutic potential for bile acid sequestrants. PLoS One 2010;5:e13365 [CrossRef][PubMed]
    [Google Scholar]
  30. Li P, Rivera-Cancel G, Kinch LN, Salomon D, Tomchick DR et al. Bile salt receptor complex activates a pathogenic type III secretion system. Elife 2016;5:1153 [CrossRef][PubMed]
    [Google Scholar]
  31. Livny J, Zhou X, Mandlik A, Hubbard T, Davis BM et al. Comparative RNA-Seq based dissection of the regulatory networks and environmental stimuli underlying Vibrio parahaemolyticus gene expression during infection. Nucleic Acids Res 2014;42:12212–12223 [CrossRef]
    [Google Scholar]
  32. Ronholm J, Petronella N, Kenwell R, Banerjee S. Draft whole-genome sequences of 14 Vibrio parahaemolyticus clinical isolates with an ambiguous K serogroup. Genome Announc 2015;3:e00217-15 [CrossRef][PubMed]
    [Google Scholar]
  33. Banerjee S, Petronella N, Chew Leung C, Farber J. Draft genome sequences of four Vibrio parahaemolyticus isolates from clinical cases in Canada. Genome Announc 2015;3:e01482-14 [CrossRef][PubMed]
    [Google Scholar]
  34. Trapnell C, Roberts A, Goff L, Pertea G, Kim D et al. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc 2012;7:562–578 [CrossRef][PubMed]
    [Google Scholar]
  35. Langmead B, Trapnell C, Pop M, Salzberg SL. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 2009;10:R25 [CrossRef][PubMed]
    [Google Scholar]
  36. Trapnell C, Pachter L, Salzberg SL. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 2009;25:1105–1111 [CrossRef][PubMed]
    [Google Scholar]
  37. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014;30:2068–2069 [CrossRef][PubMed]
    [Google Scholar]
  38. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G et al. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 2010;28:511–515 [CrossRef][PubMed]
    [Google Scholar]
  39. Haas BJ, Chin M, Nusbaum C, Birren BW, Livny J. How deep is deep enough for RNA-Seq profiling of bacterial transcriptomes?. BMC Genomics 2012;13:734 [CrossRef][PubMed]
    [Google Scholar]
  40. Gustavsson N, Diez A, Nyström T. The universal stress protein paralogues of Escherichia coli are co-ordinately regulated and co-operate in the defence against DNA damage. Mol Microbiol 2002;43:107–117 [CrossRef][PubMed]
    [Google Scholar]
  41. Nagakubo S, Nishino K, Hirata T, Yamaguchi A. The putative response regulator BaeR stimulates multidrug resistance of Escherichia coli via a novel multidrug exporter system, MdtABC. J Bacteriol 2002;184:4161–4167 [CrossRef][PubMed]
    [Google Scholar]
  42. Paul S, Alegre KO, Holdsworth SR, Rice M, Brown JA et al. A single-component multidrug transporter of the major facilitator superfamily is part of a network that protects Escherichia coli from bile salt stress. Mol Microbiol 2014;92:872–884 [CrossRef][PubMed]
    [Google Scholar]
  43. Bina JE, Mekalanos JJ. Vibrio cholerae tolC is required for bile resistance and colonization. Infect Immun 2001;69:4681–4685 [CrossRef][PubMed]
    [Google Scholar]
  44. Chatterjee A, Chaudhuri S, Saha G, Gupta S, Chowdhury R. Effect of bile on the cell surface permeability barrier and efflux system of Vibrio cholerae. J Bacteriol 2004;186:6809–6814 [CrossRef][PubMed]
    [Google Scholar]
  45. Bina JE, Provenzano D, Wang C, Bina XR, Mekalanos JJ. Characterization of the Vibrio cholerae vexAB and vexCD efflux systems. Arch Microbiol 2006;186:171–181 [CrossRef][PubMed]
    [Google Scholar]
  46. Herrera CM, Crofts AA, Henderson JC, Pingali SC, Davies BW et al. The Vibrio cholerae VprA-VprB two-component system controls virulence through endotoxin modification. MBio 2014;5:e02283-14 [CrossRef][PubMed]
    [Google Scholar]
  47. Lee S, Yeom JH, Seo S, Lee M, Kim S et al. Functional analysis of Vibrio vulnificus RND efflux pumps homologous to Vibrio cholerae VexAB and VexCD, and to Escherichia coli AcrAB. J Microbiol 2015;53:256–261 [CrossRef][PubMed]
    [Google Scholar]
  48. Matsuo T, Ogawa W, Tsuchiya T, Kuroda T. Overexpression of vmeTUV encoding a multidrug efflux transporter of Vibrio parahaemolyticus causes bile acid resistance. Gene 2014;541:19–25 [CrossRef][PubMed]
    [Google Scholar]
  49. de Jesus MC, Urban AA, Marasigan ME, Barnett Foster DE. Acid and bile-salt stress of enteropathogenic Escherichia coli enhances adhesion to epithelial cells and alters glycolipid receptor binding specificity. J Infect Dis 2005;192:1430–1440 [CrossRef][PubMed]
    [Google Scholar]
  50. Goforth JB, Walter NE, Karatan E. Effects of polyamines on Vibrio cholerae virulence properties. PLoS One 2013;8:e60765 [CrossRef][PubMed]
    [Google Scholar]
  51. Vuilleumier S. Bacterial glutathione S-transferases: what are they good for?. J Bacteriol 1997;179:1431–1441 [CrossRef][PubMed]
    [Google Scholar]
  52. Delepelaire P. Type I secretion in Gram-negative bacteria. Biochim Biophys Acta 2004;1694:149–161 [CrossRef][PubMed]
    [Google Scholar]
  53. Zgurskaya HI. Multicomponent drug efflux complexes: architecture and mechanism of assembly. Future Microbiol 2009;4:919–932 [CrossRef][PubMed]
    [Google Scholar]
  54. Rosenberg EY, Bertenthal D, Nilles ML, Bertrand KP, Nikaido H. Bile salts and fatty acids induce the expression of Escherichia coli AcrAB multidrug efflux pump through their interaction with Rob regulatory protein. Mol Microbiol 2003;48:1609–1619 [CrossRef][PubMed]
    [Google Scholar]
  55. Yamanaka H, Kobayashi H, Takahashi E, Okamoto K. MacAB is involved in the secretion of Escherichia coli heat-stable enterotoxin II. J Bacteriol 2008;190:7693–7698 [CrossRef][PubMed]
    [Google Scholar]
  56. Bina JE, Mekalanos JJ. Vibrio cholerae tolC is required for bile resistance and colonization. Infect Immun 2001;69:4681–4685 [CrossRef][PubMed]
    [Google Scholar]
  57. Hasegawa H, Gharaibeh DN, Lind EJ, Häse CC. Virulence of metalloproteases produced by Vibrio species on Pacific oyster Crassostrea gigas larvae. Dis Aquat Organ 2009;85:123–131 [CrossRef][PubMed]
    [Google Scholar]
  58. Lally ET, Hill RB, Kieba IR, Korostoff J. The interaction between RTX toxins and target cells. Trends Microbiol 1999;7:356–361 [CrossRef][PubMed]
    [Google Scholar]
  59. Quiñones-Ramírez EI, Natividad-Bonifacio I, Fernández FJ, Vázquez-Salinas C. Vibrio vulnificus: understanding this pathogenic bacterium. Reviews in Medical Microbiology 2010;21:21–27 [CrossRef]
    [Google Scholar]
  60. Salomon D, Gonzalez H, Updegraff BL, Orth K. Vibrio parahaemolyticus type VI secretion system 1 is activated in marine conditions to target bacteria, and is differentially regulated from system 2. PLoS One 2013;8:e61086 [CrossRef][PubMed]
    [Google Scholar]
  61. Livny J, Zhou X, Mandlik A, Hubbard T, Davis BM et al. Comparative RNA-Seq based dissection of the regulatory networks and environmental stimuli underlying Vibrio parahaemolyticus gene expression during infection. Nucleic Acids Res 2014;42:12212–12223 [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/mgen/10.1099/mgen.0.000182
Loading
/content/journal/mgen/10.1099/mgen.0.000182
Loading

Data & Media loading...

Supplements

Supplementary File 1

Supplementary File 2

PDF

Most Cited This Month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error