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Virulence Changes to Harveyi Clade Bacteria Infected with Bacteriophage from Vibrio owensii

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Abstract

Vibrio owensii is one of the most virulent vibrios known being able to kill crustacean larvae at 102 CFU ml−1. This study describes virulence changes to naïve strains of Vibrio harveyi and Vibrio campbellii when infected with the bacteriophage VOB from a closely related species V. owensii 47666-1. The bacteriophage from V. owensii was induced into lytic phase by using mitomycin C at 100 ng ml−1. One strain of V. harveyi and two strains of V. campbellii from 29 tested containing no prophage were susceptible to lysogenic conversion with VOB. Virulence changes induced in Harveyi clade bacteria included the up-regulation of protein secretion, statistically significant increased haemolysin and chitinase production and increased mortality to nauplii of Penaeus monodon. No change in siderophore production was observed. Bacteriophage VOB is likely to be responsible for some of the virulence factors expressed by V. owensii. As this bacteriophage is able to infect strains of V. harveyi and V. campbellii this phage may contribute to increased virulence of other vibrios in aquaculture and in the natural environment.

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References

  1. Biosca E, Amaro C. Siderophores and related outer membrane proteins in Vibrio spp. which are potential pathogens of fish and shellfish. J Fish Dis. 1991;14:249–63.

    Article  CAS  Google Scholar 

  2. Cano-Gomez A, Goulden E, Owens L, Høj L. Vibrio owensii sp. nov. isolated from cultured crustaceans in Australia. FEMS Microbiol Lett. 2010;302:175–81.

    Article  PubMed  CAS  Google Scholar 

  3. Cano-Gomez A, Hoj L, Owens L, Andreakis N. Multilocus Sequence Analysis (MLSA) provides basis for fast and reliable identification of Vibrio harveyi-related species and confirms previous misidentifications of Australian aquaculture pathogens. Syst Environ Microbiol. 2011;34:561–5.

    Article  CAS  Google Scholar 

  4. Chimetto LA, Cleenwerck I, Alves N, Silva BS, Brocchi M, Willems A, De Vos P, Thompson FL. Vibrio communis sp. nov., isolated from the marine animals Mussismilia hispida, Phyllogorgia dilatata, Palythoa caribaeorum, Palythoa variabilis and Litopenaeus vannamei. Int J Syst Evolut Microbiol. 2011;61:362–8.

    Article  CAS  Google Scholar 

  5. Gooday G. The ecology of chitin degradation. Adv Microbial Ecol. 1990;11:387–430.

    Article  CAS  Google Scholar 

  6. Harris LJ. An investigation into the virulence of strains of Vibrio harveyi pathogenic to larvae of the tiger prawn, Penaeus monodon. Honours thesis, Microbiology and Immunology. James Cook University of North Queensland, Townsville, Australia. 1993.

  7. Harris LJ, Owens L. Production of exotoxins by two luminous Vibrio harveyi strains known to be primary pathogens of Penaeus monodon larvae. Dis Aquat Org. 1999;38:11–22.

    Article  CAS  Google Scholar 

  8. Hoffmann M, Monday SR, Fischer M, Brown EW. Genetic and phylogenetic evidence for misidentification of Vibrio species within the Harveyi clade. Lett Appl Microbiol. 2011;54:160–5.

    Article  PubMed  Google Scholar 

  9. Liu PC, Lee KK, Yii KC, Kou GH, Chen SN. Isolation of Vibrio harveyi from diseased kuruma prawns Penaeus japonicus. Curr Microbiol. 1996;33:129–32.

    Article  PubMed  CAS  Google Scholar 

  10. Liu PC, Lee KK, Tu CC. Chen S N. Purification and characterization of a cysteine protease produced by pathogenic luminous Vibrio harveyi. Curr Microbiol. 1997;35:32–9.

    Article  PubMed  CAS  Google Scholar 

  11. Liu PC, Lee KK. Cysteine protease is a major exotoxin of pathogenic luminous Vibrio harveyi in the tiger prawn, Penaeus monodon. Lett Appl Microbiol. 1999;28:428–30.

    Article  PubMed  CAS  Google Scholar 

  12. McCall JO, Sizemore RK. Description of a bacteriocinogenic plasmid in Beneckea harveyi. Appl Environ Microbiol. 1979;38:974–9.

    PubMed  CAS  Google Scholar 

  13. Muir P. Factors affecting the survival of penaeid prawns in culture with particular reference to the larval stages. PhD thesis, James Cook University of North Queensland, Townsville, Australia. 1979.

  14. Munro J, Oakey HJ, Bromage E, Owens L. Experimental bacteriophage-mediated virulence in strains of Vibrio harveyi. Dis Aquat Org. 2003;54:187–94.

    Article  PubMed  Google Scholar 

  15. Oakey HJ. The mode of action and risk assessment of bacteriophage associated with virulent strains of the marine pathogen, Vibrio harveyi, Aqua CRC Education and Training Industry Programs. 2000.

  16. Oakey HJ, Owens L. A new bacteriophage, VHML, isolated from a toxin-producing strain of Vibrio harveyi in tropical Australia. J Appl Microbiol. 2000;89:702–9.

    Article  PubMed  CAS  Google Scholar 

  17. Owens L, Austin D, Austin B. Effect of strain origin on siderophore production in Vibrio harveyi isolates. Dis Aquat Org. 1996;27:157–60.

    Article  Google Scholar 

  18. Paul JH, Sullivan MB, Segall AM, Rohwer F. Marine phage genomics. Comp Biochem Physiol B. 2002;133:463–76.

    Article  PubMed  Google Scholar 

  19. Payne M, Oakey HJ, Owens L. The ability of two different Vibrio spp. bacteriophages to cross-infect Vibrio harveyi, Vibrio cholerae & Vibrio mimicus. J Appl Microbiol. 2004;97:663–72.

    Article  PubMed  CAS  Google Scholar 

  20. Pizzutto M, Hirst R. Classification of isolates of Vibrio harveyi virulent to Penaeus monodon larvae by protein profile analysis and M13 DNA fingerprinting. Dis Aquat Org. 1995;21:61–8.

    Article  Google Scholar 

  21. Ruangpan L, Danayadol Y, Direkbusarakom S, Siurairatana S, Flegel T. Bacteriophage implicated in mortality of cultivated Penaeus monodon exhibiting tea-brown gill syndrome (TBGS). In shrimp biotechnology seminar. Bangkok: NSTDA; 1998.

    Google Scholar 

  22. Schwyn B, Neilands J. Universal chemical assay for the detection and determination of siderophores. Anal Biochem. 1987;160:47–56.

    Article  PubMed  CAS  Google Scholar 

  23. Soto-Rodriguez SA, Roque A, Lizarraga-Partida ML, Guerra-Flores AL, Gomez-Gill B. Virulence of luminous vibrios to Artemia franciscana nauplii. Dis Aquat Org. 2003;53:231–40.

    Article  PubMed  CAS  Google Scholar 

  24. Sudheesh P, Xu H-S. Pathogenicity of Vibrio parahaemolyticus in tiger prawn Penaeus monodon Fabricius: possible role of extracellular proteases. Aquaculture. 2001;196:37–46.

    Article  CAS  Google Scholar 

  25. Svitil AL, Chadhain S, Moore J, Kirchman DL. Chitin degradation proteins produced by the marine bacterium Vibrio harveyi growing on different forms of chitin. Appl Environ Microbiol. 1997;63:408–13.

    PubMed  CAS  Google Scholar 

  26. Tarsi R, Pruzzo C. Role of surface proteins in Vibrio cholerae attachment to chitin. Appl Environ Microbiol. 1999;65:1348–51.

    PubMed  CAS  Google Scholar 

  27. Toranzo A, Barja J, Colwel R, Hetrick F, Crosa J. Haemagglutinating, haemolytic and cytotoxic activities of Vibrio anguillarium and related vibrios isolated from striped bass on the Atlantic Coast. FEMS Microbiol Lett. 1983;18:257–62.

    Article  Google Scholar 

  28. Weinbauer MG, Suttle CA. Potential significance of lysogeny to bacteriophage production and bacterial mortality in coastal waters of the Gulf of Mexico. Appl Environ Microbiol. 1996;62:4374–80.

    PubMed  CAS  Google Scholar 

  29. Yoshizawa S, Wada M, Kita-Tsukamoto K, Ikemoto E, Yokota A, Kogure K. Vibrio azureus sp. nov., a luminous marine bacterium isolated from seawater. Int J Syst Evol Microbiol. 2009;59:1645–9.

    Article  PubMed  CAS  Google Scholar 

  30. Yoshizawa S, Wada M, Yokota A, Kogure K. Vibrio sagamiensis sp. nov., luminous marine bacteria isolated from sea water. J Gen Appl Microbiol. 2010;56:499–507.

    Article  PubMed  CAS  Google Scholar 

  31. Yoshizawa S, Tsuruya Y, Fukui Y, Sawabe T, Yokota A, Kogure K, Higgins M, Carson J, Thompson FL. Vibrio jasicida sp. nov., a member of the Harveyi clade, from marine animals (packhorse lobster, abalone, and Atlantic salmon). Int J Syst Evol Microbiol. 2012;59:1645–9.

    Article  Google Scholar 

  32. Zhang XH, Austin B. Pathogenicity of Vibrio harveyi to salmonids. J Fish Dis. 2000;23:93–102.

    Article  Google Scholar 

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Acknowledgments

Dr Jane Oakey participated in all aspects of this research but does not wish to be a co-author on this publication.

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Author notes

  1. Nancy Busico-Salcedo

    Present address: College of Veterinary Medicine, University of Southern Mindanao, Kabacan, Cotabato, Philippines

Authors and Affiliations

  1. Microbiology and Immunology, School of Veterinary and Biomedical Sciences, James Cook University, Townsville, QLD, 4811, Australia

    Nancy Busico-Salcedo & Leigh Owens

  2. Centre for Sustainable Tropical Fisheries and Aquaculture, School of Veterinary and Biomedical Sciences, James Cook University, Townsville, QLD, 4811, Australia

    Leigh Owens

Authors
  1. Nancy Busico-Salcedo
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  2. Leigh Owens
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Correspondence to Leigh Owens.

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Busico-Salcedo, N., Owens, L. Virulence Changes to Harveyi Clade Bacteria Infected with Bacteriophage from Vibrio owensii . Indian J. Virol. 24, 180–187 (2013). https://doi.org/10.1007/s13337-013-0136-1

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  • DOI: https://doi.org/10.1007/s13337-013-0136-1

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