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Volume 2, Issue 4

Identifying copy number variation of the dominant virulence factors msa and p22 within genomes of the fish pathogen Renibacterium salmoninarum Open Access

Abstract

Renibacterium salmoninarum is the causative agent of bacterial kidney disease, an important disease of farmed and wild salmonid fish worldwide. Despite the wide spatiotemporal distribution of this disease and habitat pressures ranging from the natural environment to aquaculture and rivers to marine environments, little variation has been observed in the R. salmoninarum genome. Here we use the coverage depth from genomic sequencing corroborated by real-time quantitative PCR to detect copy number variation (CNV) among the genes of R. salmoninarum. CNV was primarily limited to the known dominant virulence factors msa and p22. Among 68 isolates representing the UK, Norway and North America, the msa gene ranged from two to five identical copies and the p22 gene ranged from one to five copies. CNV for these two genes co-occurred, suggesting they may be functionally linked. Isolates carrying CNV were phylogenetically restricted and originated predominantly from sites in North America, rather than the UK or Norway. Although both phylogenetic relationship and geographical origin were found to correlate with CNV status, geographical origin was a much stronger predictor than phylogeny, suggesting a role for local selection pressures in the repeated emergence and maintenance of this trait.

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Keyword(s): copy number variation , gene duplication-amplification , major soluble antigen , p22 and renibacterium salmoninarum
© 2016 The Authors
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2016-04-29
2024-04-20
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References

  1. Abreu-Goodger C., Merino E. 2005; Ribex: a web server for locating riboswitches and other conserved bacterial regulatory elements. Nucleic Acids Res 33:W690–W692 [View Article][PubMed]
     [Google Scholar]
  2. Andersson D. I., Hughes D. 2009; Gene amplification and adaptive evolution in bacteria. Annu Rev Genet 43:167–195 [View Article][PubMed]
     [Google Scholar]
  3. Brown L. L., Iwama G. K., Evelyn T. P. T. 1996; The effect of early exposure of Coho salmon (Oncorhynchus kisutch) eggs to the p57 protein of Renibacterium salmoninarum on the development of immunity to the pathogen. Fish Shellfish Immunol 6:149–165
     [Google Scholar]
  4. Brynildsrud O., Feil E. J., Bohlin J., Castillo-Ramirez S., Colquhoun D., McCarthy U., Matejusova I. M., Rhodes L. D., Wiens G. D., Verner-Jeffreys D. W. 2014; Microevolution of Renibacterium salmoninarum: evidence for intercontinental dissemination associated with fish movements. ISME J 8:746–756 [View Article][PubMed]
     [Google Scholar]
  5. Brynildsrud O., Snipen L.-G., Bohlin J. 2015; CNOCpro: detection and quantification of CNVs in prokaryotic whole-genome sequencing data. Bioinforma Oxf Engl 31:1708–1715 [View Article]
     [Google Scholar]
  6. Coady A. M., Murray A. L., Elliott D. G., Rhodes L. D. 2006; Both msa genes in Renibacterium salmoninarum are needed for full virulence in bacterial kidney disease. Appl Environ Microbiol 72:2672–2678 [View Article][PubMed]
     [Google Scholar]
  7. Conant G. C., Wolfe K. H. 2008; Turning a hobby into a job: how duplicated genes find new functions. Nat Rev Genet 9:938–950 [View Article][PubMed]
     [Google Scholar]
  8. Diniz-Filho J. A., Soares T. N., Lima J. S., Dobrovolski R., Landeiro V. L., de Campos Telles M. P., Rangel T. F., Bini L. M. 2013; Mantel test in population genetics. Genet Mol Biol 36:475–485 [View Article][PubMed]
     [Google Scholar]
  9. Domenech P., Kolly G. S., Leon-Solis L., Fallow A., Reed M. B. 2010; Massive gene duplication event among clinical isolates of the Mycobacterium tuberculosis W/Beijing Family. J Bacteriol 192:4562–4570 [View Article][PubMed]
     [Google Scholar]
  10. Elliott K. T., Cuff L. E., Neidle E. L. 2013; Copy number change: evolving views on gene amplification. Future Microbiol 8:887–899 [View Article][PubMed]
     [Google Scholar]
  11. Evelyn T. P. T., Prosperi-Porta L., Ketcheson J. E. 1986; Experimental intra-ovum infection of salmonid eggs with Renibacterium salmoninarum and vertical transmission of the pathogen with such eggs despite their treatment with erythromycin. Dis Aquat Organ 1:197–202 [View Article]
     [Google Scholar]
  12. Fredriksen A., Bakken V. 1994; Identification of Renibacterium salmoninarum surface proteins by radioiodination. FEMS Microbiol Lett 121:297–301[PubMed]
     [Google Scholar]
  13. Frediksen Å., Enderesen C., Wergeland H. I. 1997; Immunosuppressive effect of a low molecular weight surface protein from Renibacterium salmoninarumon on lymphocytes from Atlantic salmon (Salmo salar L.). Fish Shellfish Immunol 7:273–282 [View Article]
     [Google Scholar]
  14. Fryer J. L., Lannan C. N. 1993; The history and current status of Renibacterium salmoninarum, the causative agent of bacterial kidney disease in Pacific salmon. Fish Res 17:15–33 [View Article]
     [Google Scholar]
  15. Kondrashov F. A., Rogozin I. B., Wolf Y. I., Koonin E. V. 2002; Selection in the evolution of gene duplications. Genome Biol 3:[PubMed]
     [Google Scholar]
  16. Kondrashov F. A. 2012; Gene duplication as a mechanism of genomic adaptation to a changing environment. Proc R Soc B Biol Sci 279:5048–5057 [View Article]
     [Google Scholar]
  17. Murray A. G., Munro L. A., Wallace I. S., Allan C. E. T., Peeler E. J., Thrush M. A. 2012; Epidemiology of Renibacterium salmoninarum in Scotland and the potential for compartmentalized management of salmon and trout farming areas. Aquaculture 324–325:1–13
     [Google Scholar]
  18. Naville M., Ghuillot-Gaudeffroy A., Marchais A., Gautheret D. 2011; ARNold: a web tool for the prediction of Rho-independent transcription terminators. RNA Biol 8:11–13[PubMed]
     [Google Scholar]
  19. O'Farrell C. L., Strom M. 1999; Differential expression of the virulence-associated protein p57 and characterization of its duplicated gene msa in virulent and attenuated strains of Renibacterium salmoninarum. Dis Aquat Organ 38:115–123 [View Article][PubMed]
     [Google Scholar]
  20. Pascho R. J., Elliott D. G., Achord S. 1993; Monitoring of the in-river migration of smolts from two groups of spring chinook salmon, Oncorhynchus tshawytscha (Walbaum), with different profiles of Renibacterium salmoninarum infection. Aquac Res 24:163–169 [View Article]
     [Google Scholar]
  21. Rhodes L. D., Coady A. M., Strom M. S. 2002; Expression of duplicate msa genes in the salmonid pathogen Renibacterium salmoninarum. Appl Environ Microbiol 68:5480–5487[PubMed]
     [Google Scholar]
  22. Rhodes L. D., Coady A. M., Deinhard R. K. 2004; Identification of a third msa gene in Renibacterium salmoninarum and the associated virulence phenotype. Appl Environ Microbiol 70:6488–6494 [View Article][PubMed]
     [Google Scholar]
  23. Rhodes L. D., Rice C. A., Greene C. M., Teel D. J., Nance S. L., Moran P., Durkin C. A., Gezhegne S. B. 2011; Nearshore ecosystem predictors of a bacterial infection in juvenile Chinook salmon. Mar Ecol Prog Ser 432:161–172 [View Article]
     [Google Scholar]
  24. Riehle M. M., Bennett A. F., Long A. D. 2001; Genetic architecture of thermal adaptation in Escherichia coli. Proc Natl Acad Sci U S A 98:525–530 [View Article][PubMed]
     [Google Scholar]
  25. Ronquist F., Huelsenbeck J. P. 2003; MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574[PubMed]
     [Google Scholar]
  26. Sandell T. A., Teel D. J., Fisher J., Beckman B., Jacobson K. C. 2015; Infections by Renibacterium salmoninarum and Nanophyetus salmincola Chapin are associated with reduced growth of juvenile Chinook salmon, Oncorhynchus tshawytscha (Walbaum), in the Northeast Pacific Ocean. J Fish Dis 38:365–378 [View Article][PubMed]
     [Google Scholar]
  27. Senson P. R., Stevenson R. M. 1999; Production of the 57 kDa major surface antigen by a non-agglutinating strain of the fish pathogen Renibacterium salmoninarum. Dis Aquat Organ 38:23–31 [View Article][PubMed]
     [Google Scholar]
  28. Stranger B. E., Forrest M. S., Dunning M., Ingle C. E., Beazley C., Thorne N., Redon R., Bird C. P., de Grassi A., other authors. 2007; Relative impact of nucleotide and copy number variation on gene expression phenotypes. Science 315:848–853 [View Article][PubMed]
     [Google Scholar]
  29. Turaga P., Wiens G., Kaattari S. 1987; Bacterial kidney disease: the potential role of soluble protein antigen(s). J Fish Biol 31:191–194 [View Article]
     [Google Scholar]
  30. Wiens G. D., Kaattari S. L. 1991; Monoclonal antibody characterization of a leukoagglutinin produced by Renibacterium salmoninarum. Infect Immun 59:631–637[PubMed]
     [Google Scholar]
  31. Wiens G. D., Chien M. S., Winton J. R., Kaattari S. L. 1999; Antigenic and functional characterization of p57 produced by Renibacterium salmoninarum. Dis Aquat Organ 37:43–52 [View Article][PubMed]
     [Google Scholar]
  32. Wiens G. D., Dale O. B. 2008; Renibacterium salmoninarum p57 antigenic variation is restricted in geographic distribution and correlated with genomic markers. Dis Aquat Organ 83:123–131 [View Article]
     [Google Scholar]
  33. Wiens G. D., Rockey D. D., Wu Z., Chang J., Levy R., Crane S., Chen D. S., Capri G. R., Burnett J. R., other authors. 2008; Genome sequence of the fish pathogen Renibacterium salmoninarum suggests reductive evolution away from an environmental Arthrobacter ancestor. J Bacteriol 190:6970–6982 [View Article][PubMed]
     [Google Scholar]
  34. Wood P. A., Kaattari S. L. 1996; Enhanced immunogenicity of Renibacterium salmoninarum in Chinook salmon after removal of the bacterial cell surface-associated 57 kDa protein. Dis Aquat Organ 25:71–79 [View Article]
     [Google Scholar]
  35. Brynildsrud, O., Feil, E. J., Bohlin, J., Castillo-Ramirez, S., Colquhoun, D., McCarthy, U., Matejusova, I. M., Rhodes, L. D. & Wiens, G. D. (2014). NCBI Sequence Read Archive. http://trace.ncbi.nlm.nih.gov/Traces/study/?acc=ERP003780.
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Identifying copy number variation of the dominant virulence factors msa and p22 within genomes of the fish pathogen Renibacterium salmoninarum
M Gen 2, e000055 (2016); https://doi.org/10.1099/mgen.0.000055
/content/journal/mgen/10.1099/mgen.0.000055
/content/journal/mgen/10.1099/mgen.0.000055
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