Advertisement

Archives of Microbiology

, Volume 190, Issue 2, pp 185–194 | Cite as

Genome analysis of the coral bleaching pathogen Vibrio shiloi

  • Leah Reshef
  • Eliora Ron
  • Eugene Rosenberg
Original Paper

Abstract

The past few decades have seen a world-wide increase in coral diseases, yet little is known about coral pathogens. In this study, techniques commonly used in pathogenomic research were applied to the coral pathogen Vibrio shiloi in order to identify genetic elements involved in its virulence. Suppressive subtractive hybridization was used to compare the gene content of V. shiloi to that of a closely related but non-pathogenic bacterium, Vibrio mediterranei, resulting in identification of several putative virulence factors and of three novel genomic islands. The entire genome of V. shiloi was further screened for genes related to previously characterized steps in infection: adhesion, superoxide dismutase production and toxin production. Exposure of pure cultures of V. shiloi to crushed coral tissues strongly affected the expression of seven genes encoding pili, zona occludins toxin (Zot) and a superoxide dismutase. Analysis of eight V. shiloi strains isolated in the last decade shows a shift of the natural population from strains carrying all three genomic islands to strains carrying none of them. This shift occurred following appearance of resistance in the coral Oculina patagonica to infection by V. shiloi. The relevance of these findings to the bleaching disease caused by V. shiloi is discussed.

Keywords

Vibrio Genomic Island Vibrio Species Suppressive Subtractive Hybridization Coral Pathogen 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

This work was supported by the GEF Coral Reef Targeted Research Program and the Israel Center for the Study of Emerging Diseases. The genome sequencing was supported by the Moore Foundation. We thank Uri Gophna for help with the bioinformatics.

References

  1. Banin E, Israely T, Fine M, Loya Y, Rosenberg E (2001) Role of endosymbiotic zooxanthellae and coral mucus in the adhesion of the coral-bleaching pathogen Vibrio shiloi to its host. FEMS Microbiol Lett 199:33–37PubMedCrossRefGoogle Scholar
  2. Banin E, Vassilakos D, Orr E, Martinez R, Rosenberg E (2003) Superoxide dismutase is a virulence factor produced by the coral bleaching pathogen Vibrio shiloi. Curr Microbiol 46:418–422PubMedCrossRefGoogle Scholar
  3. Brzuszkiewicz E, Bruggemann H, Liesegang H, Emmerth M, Oschlager T, Nagy G, Albermann K, Wagner C, Buchrieser C, Emody L, Gottschalk G, Hackert J, Dobrindt U (2006) How to become a uropathogen: comparative genomic analysis of extraintestinal pathogenic Escherichia coli strains. Proc Natl Acad Sci USA 103:12879–12884PubMedCrossRefGoogle Scholar
  4. Chen C, Chang W, Chang C, Tsai H, Liao T, Liu Y, Chen H, Shen A, Li J, Su T, Shao C, Lee C, Hor L, Tsai S (2003) Comparative genome analysis of Vibrio vulnificus, a marine pathogen. Genome Res 13:2577–2587PubMedCrossRefGoogle Scholar
  5. Chen T, Hosogi Y, Nishikawa K, Abbey K, Fleischmann RD, Walling J, Duncan MJ (2004) Comparative whole-genome analysis of virulent and avirulent strains of Porphyromonas gingivalis. J Bacteriol 186:5473–5479PubMedCrossRefGoogle Scholar
  6. Chiavelli D, Marsh J, Taylor R (2001) The mannose-sensitive hemagglutinin of Vibrio cholerae promotes adherence to zooplankton. Appl Environ Microbiol 67:3220–3225PubMedCrossRefGoogle Scholar
  7. Davis BM, Waldor MK (2003) Filamentous phage linked to virulence of Vibrio cholerae. Curr Opin Microbiol 6:35–42PubMedCrossRefGoogle Scholar
  8. Dobrindt U (2005) (Patho-) Genomics of Escherichia coli. Int J Med Microbiol 295:357–371PubMedCrossRefGoogle Scholar
  9. Hacker J et al (2004) Pathogenomics of mobile genetic elements of toxigenic bacteria. Int J Med Microbiol 293:453–461PubMedCrossRefGoogle Scholar
  10. Hsiao A, Liu Z, Joelsson A, Zhu J (2006) Vibrio cholerae virulence regulator-coordinated evasion of host immunity. Proc Natl Acad Sci USA 103:14542–14547PubMedCrossRefGoogle Scholar
  11. Kholodi G, Gorlenko ZH, Mindlin S, Hobman J, Nikifrov V (2002) Tn5041-like transposons: molecular diversity, evolutionary relationships and distribution of distinct variants in environmental bacteria. Microbiology 148:3569–3582Google Scholar
  12. Makino K, Oshima K, Kurokawa K, Yokoyama K, Uda T, Tagomori K, Iijima Y, Najima M, Nakano M, Yamashita A, Kubota Y, Kimura S, Yasunaga T, Honda T, Shinagawa H, Hattori M, Iida T (2003) Genome sequence of Vibrio parahaemolyticus: a pathogenic mechanism distinct from that of Vibrio cholerae. Lancet 361:743–749PubMedCrossRefGoogle Scholar
  13. Mokady D, Gophna U, Ron E (2005a) Extensive gene diversity in septicemic Escherichia coli strains. J Clin Microbiol 43:66–73PubMedCrossRefGoogle Scholar
  14. Mokady D, Gophna U, Ron E (2005b) Virulence factors of septicemic Escherichia coli strains. Int J Med Microbiol 295:455–462PubMedCrossRefGoogle Scholar
  15. Mydlarz LD, Jones LE, Harvell CD (2006) Innate immunity environmental drivers and disease ecology of marine and freshwater invertebrates. Annu Rev Ecol Evol Syst 37:251–288CrossRefGoogle Scholar
  16. Nasu H, Iida T, Sugahara T, Yamaichi Y, Park KS, Yokoyama K, Makino K, Shinagawa H, Honda T (2000) A filamentous phage associated with recent pandemic Vibrio parahaemolyticus O3: K6 strains. J Clin Microbiol 38(6):2156–2161PubMedGoogle Scholar
  17. Osborn AM, Bruce KD, Strike P, Ritchie DA (1997) Distribution, diversity and evolution of the bacterial mercury resistance (mer) operon. FEMS Microbiol Rev 19(4):239–262PubMedCrossRefGoogle Scholar
  18. Quirke AM, Reen FJ, Clasesson MJ, Boyd EF (2006) Genomic island identification in Vibrio vulnificus reveals significant genome plasticity in this human pathogen. Bioinformatics 22:905–910PubMedCrossRefGoogle Scholar
  19. Reshef L, Koren O, Loya Y, Zilber-Rosenberg I, Rosenberg E (2006) The coral probiotic hypothesis. Environ Microbiol 8:2068–2073PubMedCrossRefGoogle Scholar
  20. Rosenberg E, Falkovitz L (2004) The Vibrio shiloi/Oculina patagonica model system of coral bleaching. Annu Rev Microbiol 58:143–159PubMedCrossRefGoogle Scholar
  21. Rosenberg E, Koren O, Reshef L, Efrony R, Zilber-Rosenberg I (2007) The role of microorganisms in coral health, disease and evolution. Nat Rev Microbiol 5:355–362PubMedCrossRefGoogle Scholar
  22. Ruby EG, Urbanowski M, Campbell J, Dunn A, Faini M, Gunsalus R, Lostroh P, Lupp C, McCann J, Millikan D, Schaefer A, Stabb E, Stevens A, Visick K, Whistler C, Greenberg EP (2005) Complete genome sequence of Vibrio fischeri: a symbiotic bacterium with pathogenic congeners. Proc Natl Acad Sci USA 102:3004–3009PubMedCrossRefGoogle Scholar
  23. Thompson F, Hoste B, Thompson C, Huys G, Swings J (2001) The coral bleaching Vibrio shiloi Kushmaro et al. 2001 is a later synonym of Vibrio mediterranei Pujalte and Garay 1986. Syst Appl Microbiol 24:516–519PubMedCrossRefGoogle Scholar
  24. Toren A, Landau L, Kushmaro A, Loya Y, Rosenberg E (1998) Effect of temperature on adhesion of vibrio strain AK–1 to Oculina patagonica and on coral bleaching. Appl Environ Microbiol 64:1379–1384PubMedGoogle Scholar
  25. van Passel MWJ, Luyf ACM, van Kampen AHC, Bart A, van der Ende A (2005) delta p-Web, an online tool to assess composition similarity of individual nucleic acid sequences. Bioinformatics 21:3053–3055PubMedCrossRefGoogle Scholar
  26. Wang G, Olczak A, Walton J, Maier RJ (2005) Contribution of the Heliobacter pylori thiol peroxidase bacterioferritin comigratory protein to oxidative stress resistance and host colonization. Infect Immun 73:378–384PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  1. 1.Department of Molecular Microbiology and BiotechnologyTel Aviv UniversityTel AvivIsrael

Personalised recommendations