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Abstract

Yersinia ruckeri is a salmonid pathogen with widespread distribution in cool-temperate waters including Australia and New Zealand, two isolated environments with recently developed salmonid farming industries. Phylogenetic comparison of 58 isolates from Australia, New Zealand, USA, Chile, Finland and China based on non-recombinant core genome SNPs revealed multiple deep-branching lineages, with a most recent common ancestor estimated at 18 500 years BP (12 355–24 757 95% HPD) and evidence of Australasian endemism. Evolution within the Tasmanian Atlantic salmon serotype O1b lineage has been slow, with 63 SNPs describing the variance over 27 years. Isolates from the prevailing lineage are poorly/non-motile compared to a lineage pre-vaccination, introduced in 1997, which is highly motile but has not been isolated since from epizootics. A non-motile phenotype has arisen independently in Tasmania compared to Europe and USA through a frameshift in fliI, encoding the ATPase of the flagella cluster. We report for the first time lipopolysaccharide O-antigen serotype O2 isolates in Tasmania. This phenotype results from deletion of the O-antigen cluster and consequent loss of high-molecular-weight O-antigen. This phenomenon has occurred independently on three occasions on three continents (Australasia, North America and Asia) as O2 isolates from the USA, China and Tasmania share the O-antigen deletion but occupy distant lineages. Despite the European and North American origins of the Australasian salmonid stocks, the lineages of Y. ruckeri in Australia and New Zealand are distinct from those of the northern hemisphere, suggesting they are pre-existing ancient strains that have emerged and evolved with the introduction of susceptible hosts following European colonization.

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2016-11-30
2021-08-04
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References

  1. Alikhan N. F., Petty N. K., Ben Zakour N. L., Beatson S. A. 2011; BLAST Ring Image Generator (BRIG): simple prokaryote genome comparisons. BMC Genomics 12:402 [View Article][PubMed]
    [Google Scholar]
  2. Amann R. I., Ludwig W., Schleifer K. H. 1995; Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol Rev 59:143–169
    [Google Scholar]
  3. Anderson C. D., Knowles G., de Lisle G. W. 1994; A survey for Yersinia ruckeri and Aeromonas salmonicida in farmed and wild fish. Surveillance 21:39–40
    [Google Scholar]
  4. Atkinson S., Chang C. Y., Sockett R. E., Cámara M., Williams P. 2006; Quorum sensing in Yersinia enterocolitica controls swimming and swarming motility. J Bacteriol 188:1451–1461 [View Article][PubMed]
    [Google Scholar]
  5. Bankevich A., Nurk S., Antipov D., Gurevich A. A., Dvorkin M., Kulikov A. S., Lesin V. M., Nikolenko S. I., Pham S. et al. 2012; SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19:455–477 [View Article][PubMed]
    [Google Scholar]
  6. Barnes A. C. 2011; Enteric Redmouth Disease (ERM) (Yersinia ruckeri). In Fish Diseases and Disorders, Vol 3: Viral, Bacterial and Fungal Infections, 2nd edn. , pp. 484–511 Edited by Woo P. T. K, Bruno D. W. Wallingford, UK: CABI International; [CrossRef]
    [Google Scholar]
  7. Barros M. P., França C. T., Lins R. H., Santos M. D., Silva E. J., Oliveira M. B., Silveira-Filho V. M., Rezende A. M., Balbino V. Q., Leal-Balbino T. C. 2014; Dynamics of CRISPR loci in microevolutionary process of Yersinia pestis strains. PLoS One 9:e108353 [View Article][PubMed]
    [Google Scholar]
  8. Bastardo A., Bohle H., Ravelo C., Toranzo A. E., Romalde J. L. 2011; Serological and molecular heterogeneity among Yersinia ruckeri strains isolated from farmed Atlantic salmon Salmo salar in Chile. Dis Aquat Organ 93:207–214 [View Article][PubMed]
    [Google Scholar]
  9. Bastardo A., Ravelo C., Romalde J. L. 2012; Multilocus sequence typing reveals high genetic diversity and epidemic population structure for the fish pathogen Yersinia ruckeri . Environ Microbiol 14:1888–1897 [View Article][PubMed]
    [Google Scholar]
  10. Bastardo A., Ravelo C., Romalde J. L. 2015; Phylogeography of reveals effects of past evolutionary events on the current strain distribution and explains variations in the global transmission of enteric redmouth (ERM) disease. Front Microbiol 6:1198 [View Article][PubMed]
    [Google Scholar]
  11. Bouckaert R., Heled J., Kühnert D., Vaughan T., Wu C. H., Xie D., Suchard M. A., Rambaut A., Drummond A. J. 2014; beast 2: a software platform for bayesian evolutionary analysis. PLoS Comput Biol 10:e1003537 [View Article][PubMed]
    [Google Scholar]
  12. 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]
  13. Bullock G. L., Stuckey H. M., Shotts E. B. 1978; Early records of North American and Australian outbreaks of enteric redmouth disease. Fish Health News 6:96–97
    [Google Scholar]
  14. Busch R. A. 1978; Protective vaccines for mass immunization of trout. Salmonid 1:10–22
    [Google Scholar]
  15. Carson J., Wilson T. 2009 Yersiniosis in Fish. Australian New Zealand Standard Diagnostic Procedures Edited by Sub Committee on Aquatic Animal Health Laboratory Standards (SCAAHLS), Canberra Canberra, Australia: Commonwealth of Australia, Canberra;
    [Google Scholar]
  16. Carver T., Harris S. R., Berriman M., Parkhill J., McQuillan J. A. 2012; Artemis: an integrated platform for visualization and analysis of high-throughput sequence-based experimental data. Bioinformatics 28:464–469 [View Article][PubMed]
    [Google Scholar]
  17. Chen P. E., Cook C., Stewart A. C., Nagarajan N., Sommer D. D., Pop M., Thomason B., Thomason M. P., Lentz S. et al. 2010; Genomic characterization of the Yersinia genus. Genome Biol 11:R1 [View Article][PubMed]
    [Google Scholar]
  18. Coquet L., Cosette P., Quillet L., Petit F., Junter G. A., Jouenne T. 2002; Occurrence and phenotypic characterization of Yersinia ruckeri strains with biofilm-forming capacity in a rainbow trout farm. Appl Environ Microbiol 68:470–475 [View Article][PubMed]
    [Google Scholar]
  19. Craig L., Pique M. E., Tainer J. A. 2004; Type IV pilus structure and bacterial pathogenicity. Nat Rev Microbiol 2:363–378 [View Article][PubMed]
    [Google Scholar]
  20. Croucher N. J., Page A. J., Connor T. R., Delaney A. J., Keane J. A., Bentley S. D., Parkhill J., Harris S. R. 2015; Rapid phylogenetic analysis of large samples of recombinant bacterial whole genome sequences using Gubbins. Nucleic Acids Res 43:e15 [View Article][PubMed]
    [Google Scholar]
  21. Davies R. L. 1991; Clonal analysis of Yersinia ruckeri based on biotypes, serotypes and outer membrane protein-types. J Fish Dis 14:221–228 [View Article]
    [Google Scholar]
  22. Deshmukh S., Raida M. K., Dalsgaard I., Chettri J. K., Kania P. W., Buchmann K. 2012; Comparative protection of two different commercial vaccines against Yersinia ruckeri serotype O1 and biotype 2 in rainbow trout (Oncorhynchus mykiss). Vet Immunol Immunopathol 145:379–385 [View Article][PubMed]
    [Google Scholar]
  23. Forde B. M., Ben Zakour N. L., Stanton-Cook M., Phan M. D., Totsika M., Peters K. M., Chan K. G., Schembri M. A., Upton M., Beatson S. A. 2014; The complete genome sequence of Escherichia coli EC958: a high quality reference sequence for the globally disseminated multidrug resistant E. coli O25b:H4-ST131 clone. PLoS One 9:e104400 [View Article][PubMed]
    [Google Scholar]
  24. Fouz B., Zarza C., Amaro C. 2006; First description of non-motile Yersinia ruckeri serovar I strains causing disease in rainbow trout, Oncorhynchus mykiss (Walbaum), cultured in Spain. J Fish Dis 29:339–346 [View Article][PubMed]
    [Google Scholar]
  25. Furones M. D., Gilpin M. L., Munn C. B. 1993; Culture media for the differentiation of isolates of Yersinia ruckeri, based on detection of a virulence factor. J Appl Bacteriol 74:360–366 [View Article][PubMed]
    [Google Scholar]
  26. Gilmour D. 1996; Trout Fishery of Tasmania Volume One 1865-1910. Launceston, Tasmania, Australia: Don Gilmour, 261 Penquite Road, Launceston, Tasmania 7250, Australia.
  27. Glenn R. A., Taylor P. W., Pelton E. H., Gutenberger S. K., Ahrens M. A., Marchant L. M., Hanson K. C. 2015; Genetic Evidence of Vertical Transmission and Cycling of Yersinia ruckeri in Hatchery-Origin Fall Chinook Salmon Oncorhynchus tshawytscha. J Fish Wildl Manag 6:44–54 [View Article]
    [Google Scholar]
  28. Haiko J., Westerlund-Wikström B. 2013; The role of the bacterial flagellum in adhesion and virulence. Biology 2:1242–1267 [View Article][PubMed]
    [Google Scholar]
  29. Haworth J. 2010 Swimming Upstream: How Salmon Farming Developed in New Zealand, 1st edn. Christchurch, New Zealand: Wily Publications;
    [Google Scholar]
  30. Ispir U., Dorucu M. 2014; Efficacy of lipopolysaccharide antigen of Yersinia ruckeri in rainbow trout by intraperitoneal and bath immersion administration. Res Vet Sci 97:271–273 [View Article][PubMed]
    [Google Scholar]
  31. Jungalwalla P. 1991; The development of an integrated saltwater salmonid farming industry in Tasmania, Australia. In World Aquaculture World Aquaculture Society , pp. 65–73 Edited by Cook R. H., Pennell W. Los Angeles, USA: World Aquaculture Society;
    [Google Scholar]
  32. Kahn S. A., Beers P. T., Findlay V. L., Peebles I. R., Durham P. J., Wilson D. W., Gerrity S. E. 1999 Import Risk Analysis on Non-Viable Salmonids and Non-Salmonid Marine Fish Edited by Service A. Q. I. Canberra, Australia: Australian Govenment;
    [Google Scholar]
  33. Koskela K. A., Mattinen L., Kalin-Mänttäri L., Vergnaud G., Gorgé O., Nikkari S., Skurnik M. 2015; Generation of a CRISPR database for Yersinia pseudotuberculosis complex and role of CRISPR-based immunity in conjugation. Environ Microbiol 17:4306–4321 [View Article][PubMed]
    [Google Scholar]
  34. Leaché A. D., Banbury B. L., Felsenstein J., de Oca A. N., Stamatakis A. 2015; Short Tree, Long Tree, Right Tree, Wrong Tree: new acquisition bias corrections for Inferring SNP phylogenies. Syst Biol 64:1032–1047 [View Article][PubMed]
    [Google Scholar]
  35. Leskinen K., Blasdel B. G., Lavigne R., Skurnik M. 2016; RNA-Sequencing Reveals the Progression of Phage-Host Interactions between phiR1-37 and Yersinia enterocolitica. Viruses 8:111 [View Article][PubMed]
    [Google Scholar]
  36. Marraffini L. A. 2013; CRISPR-Cas immunity against phages: its effects on the evolution and survival of bacterial pathogens. PLoS Pathog 9:e1003765 [View Article][PubMed]
    [Google Scholar]
  37. McDowall R. M. 1994; The origins of New Zealand's Chinook Salmon, Oncorhynchus tshawytscha. Mar Fish Rev 56:1–7
    [Google Scholar]
  38. Milne I., Bayer M., Cardle L., Shaw P., Stephen G., Wright F., Marshall D. 2010; Tablet – next generation sequence assembly visualization. Bioinformatics 26:401–402 [View Article][PubMed]
    [Google Scholar]
  39. Milne I., Stephen G., Bayer M., Cock P. J., Pritchard L., Cardle L., Shaw P. D., Marshall D. 2013; Using tablet for visual exploration of second-generation sequencing data. Brief Bioinform 14:193–202 [View Article][PubMed]
    [Google Scholar]
  40. Minnich S. A., Rohde H. N. 2007; A rationale for repression and/or loss of motility by pathogenic Yersinia in the mammalian host. Adv Exp Med Biol 603:298–310 [View Article][PubMed]
    [Google Scholar]
  41. Navas E., Bohle H., Henríquez P., Grothusen H., Bustamante F., Bustos P., Mancilla M. 2014; Draft Genome Sequence of the Fish Pathogen Yersinia ruckeri Strain 37551, Serotype O1b, Isolated from Diseased, Vaccinated Atlantic Salmon (Salmo salar) in Chile. Genome Announc 2:e00858-14 [View Article][PubMed]
    [Google Scholar]
  42. Nelson M. C., LaPatra S. E., Welch T. J., Graf J. 2015; Complete Genome Sequence of Yersinia ruckeri Strain CSF007-82, Etiologic Agent of Red Mouth Disease in Salmonid Fish. Genome Announc 3:e0149101414 [View Article][PubMed]
    [Google Scholar]
  43. Page A. J., Cummins C. A., Hunt M., Wong V. K., Reuter S., Holden M. T., Fookes M., Falush D., Keane J. A., Parkhill J. 2015; Roary: rapid large-scale prokaryote pan genome analysis. Bioinformatics 31:3691–3693 [View Article][PubMed]
    [Google Scholar]
  44. Petkau A., Stuart-Edwards M., Stothard P., Van Domselaar G. 2010; Interactive microbial genome visualization with GView. Bioinformatics 26:3125–3126 [View Article][PubMed]
    [Google Scholar]
  45. Rambaut A., Lam T. T., Max Carvalho L., Pybus O. G. 2016; Exploring the temporal structure of heterochronous sequences using TempEst (formerly Path-O-Gen). Virus Evol 2:1 [View Article]
    [Google Scholar]
  46. Reuter S., Connor T. R., Barquist L., Walker D., Feltwell T., Harris S. R., Fookes M., Hall M. E., Petty N. K. et al. 2014; Parallel independent evolution of pathogenicity within the genus Yersinia . Proc Natl Acad Sci U S A 111:6768–6773 [View Article][PubMed]
    [Google Scholar]
  47. Rissman A. I., Mau B., Biehl B. S., Darling A. E., Glasner J. D., Perna N. T. 2009; Reordering contigs of draft genomes using the Mauve aligner. Bioinformatics 25:2071–2073 [View Article][PubMed]
    [Google Scholar]
  48. Romalde J. L., MagariÑos B., Barja J. L., Toranzo A. E. 1993; Antigenic and molecular characterization of yersinia ruckeri proposal for a new intraspecies classification. Syst Appl Microbiol 16:411–419 [View Article]
    [Google Scholar]
  49. Rosinski-Chupin I., Sauvage E., Mairey B., Mangenot S., Ma L., Da Cunha V., Rusniok C., Bouchier C., Barbe V., Glaser P. 2013; Reductive evolution in Streptococcus agalactiae and the emergence of a host adapted lineage. BMC Genomics 14:252 [View Article][PubMed]
    [Google Scholar]
  50. Sauter R. W., Williams C., Celnik B., Meyer E. A. 1985 Etiology of Early Lifestage Diseases, Final Report 1985, Report to Bonneville Power Administration, Contract No. 1984BI18186, Project 198404400, 53 Electronic Pages (BPA Report DOE/BP-18186-1)
    [Google Scholar]
  51. Schroll C., Barken K. B., Krogfelt K. A., Struve C. 2010; Role of type 1 and type 3 fimbriae in Klebsiella pneumoniae biofilm formation. BMC Microbiol 10:179 [View Article][PubMed]
    [Google Scholar]
  52. Scott D. S., Hewitson J., Fraser J. S. 1978; The origin of rainbow trout, Salmo gairdneri Richardson, in New Zealand. Calif Fish Game 64:200–209
    [Google Scholar]
  53. Seemann T. 2014; Prokka: rapid prokaryotic genome annotation. Bioinformatics 30:2068–2069 [View Article][PubMed]
    [Google Scholar]
  54. Stamatakis A. 2014; RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313 [View Article][PubMed]
    [Google Scholar]
  55. Sullivan M. J., Ben Zakour N. L., Forde B. M., Stanton-Cook M., Beatson S. A. 2016; Contiguity: contig adjacency graph construction and visualisation Available. https://github.com/BeatsonLab-MicrobialGenomics/Contiguity’ August 2016
  56. Tebbit G. L., Erickson J. D., Vande Water R. B. 1981; Development and use of Yersinia ruckeri bacterins to control enteric redmouth disease. In International Symposium on Fish Biologics: Serodiagnostics and Fish Vaccines , pp. 395–402 Edited by Hennessen W, Anderson D. P. Basel: Karger;
    [Google Scholar]
  57. Tinsley J. W., Austin D. A., Lyndon A. R., Austin B. 2011a; Novel non-motile phenotypes of Yersinia ruckeri suggest expansion of the current clonal complex theory. J Fish Dis 34:311–317 [View Article]
    [Google Scholar]
  58. Tinsley J. W., Lyndon A. R., Austin B. 2011b; Antigenic and cross-protection studies of biotype 1 and biotype 2 isolates of Yersinia ruckeri in rainbow trout, Oncorhynchus mykiss (Walbaum). J Appl Microbiol 111:8–16 [View Article]
    [Google Scholar]
  59. Toledo M. S., Troncoso M., Portell D. P., Figueroa G. 1993; Brote causado por Yersinia ruckeri en salmonidos en cultivo. Annals of Microbiology 1:59–62
    [Google Scholar]
  60. Treangen T. J., Ondov B. D., Koren S., Phillippy A. M. 2014; The harvest suite for rapid core-genome alignment and visualization of thousands of intraspecific microbial genomes. Genome Biol 15:524 [View Article][PubMed]
    [Google Scholar]
  61. Tsai C. M., Frasch C. E. 1982; A sensitive silver stain for detecting lipopolysaccharides in polyacrylamide gels. Anal Biochem 119:115–119 [View Article][PubMed]
    [Google Scholar]
  62. Walker J. 1988; Origins of the Tasmanian trout. An account of the Salmon Ponds and the first introduction of salmon and trout to Tasmania in 1864. Hobart, Tasmania, Australia: Inland Fisheries Commission, Tasmania, Australia.
  63. Wangkahart E., Scott C., Secombes C. J., Wang T. 2016; Re-examination of the rainbow trout (Oncorhynchus mykiss) immune response to flagellin: Yersinia ruckeri flagellin is a potent activator of acute phase proteins, anti-microbial peptides and pro-inflammatory cytokines in vitro. Dev Comp Immunol 57:75–87 [View Article][PubMed]
    [Google Scholar]
  64. Welch T. J., Verner-Jeffreys D. W., Dalsgaard I., Wiklund T., Evenhuis J. P., Cabrera J. A., Hinshaw J. M., Drennan J. D., LaPatra S. E. 2011; Independent emergence of Yersinia ruckeri biotype 2 in the United States and Europe. Appl Environ Microbiol 77:3493–3499 [View Article][PubMed]
    [Google Scholar]
  65. Welch T. J., LaPatra S. 2016; Yersinia ruckeri lipopolysaccharide is necessary and sufficient for eliciting a protective immune response in rainbow trout (Oncorhynchus mykiss, Walbaum). Fish Shellfish Immunol 49:420–426 [View Article][PubMed]
    [Google Scholar]
  66. Wheeler R. W., Davies R. L., Dalsgaard I., Garcia J., Welch T. J., Wagley S., Bateman K. S., Verner-Jeffreys D. W. 2009; Yersinia ruckeri biotype 2 isolates from mainland Europe and the UK likely represent different clonal groups. Dis Aquat Organ 84:25–33 [View Article][PubMed]
    [Google Scholar]
  67. Wilksch J. J., Yang J., Clements A., Gabbe J. L., Short K. R., Cao H., Cavaliere R., James C. E., Whitchurch C. B. et al. 2011; MrkH, a novel c-di-GMP-dependent transcriptional activator, controls Klebsiella pneumoniae biofilm formation by regulating type 3 fimbriae expression. PLoS Pathog 7:e1002204 [View Article][PubMed]
    [Google Scholar]
  68. Willumsen B. 1989; Birds and wild fish as potential vectors of Yersinia ruckeri . J Fish Dis 12:275–277 [View Article]
    [Google Scholar]
  69. Yi E. C., Hackett M. 2000; Rapid isolation method for lipopolysaccharide and lipid A from gram-negative bacteria. Analyst 125:651–656 [View Article][PubMed]
    [Google Scholar]
  70. Yim L., Sasias S., Martinez A., Betancor L., Estevez V., Scavone P., Bielli A., Sirok A., Chabalgoity J. A. 2014; Repression of flagella is a common trait in field isolates of Salmonella enterica serovar Dublin and is associated with invasive human infections. nfect Immun 82:1465–1476 [View Article]
    [Google Scholar]
  71. Zhou Y., Liang Y., Lynch K. H., Dennis J. J., Wishart D. S. 2011; PHAST: a fast phage search tool. Nucleic Acids Res 39:W347–352 [View Article][PubMed]
    [Google Scholar]
  72. Barnes, AC (2016) Yersinia ruckeri Genome sequencing and assembly http://www.ncbi.nlm.nih.gov/bioproject/PRJNA310959
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