1887

Abstract

Renibacterium salmoninarum is the causative agent of bacterial kidney disease (BKD), which is a commercially important disease of farmed salmonids. Typing by conventional methods provides limited information on the evolution and spread of this pathogen, as there is a low level of standing variation within the R. salmoninarum population. Here, we apply whole-genome sequencing to 42 R. salmoninarum isolates from Chile, primarily from salmon farms, in order to understand the epidemiology of BKD in this country. The patterns of genomic variation are consistent with multiple introductions to Chile, followed by rapid dissemination over a 30 year period. The estimated dates of introduction broadly coincide with major events in the development of the Chilean aquaculture industry. We find evidence for significant barriers to transmission of BKD in the Chilean salmon production chain that may also be explained by previously undescribed signals of host tropism in R. salmoninarum. Understanding the genomic epidemiology of BKD can inform disease intervention and improve sustainability of the economically important salmon industry. This article contains data hosted by Microreact.

  • This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Loading

Article metrics loading...

/content/journal/mgen/10.1099/mgen.0.000201
2018-07-24
2024-03-29
Loading full text...

Full text loading...

/deliver/fulltext/mgen/4/9/mgen000201.html?itemId=/content/journal/mgen/10.1099/mgen.0.000201&mimeType=html&fmt=ahah

References

  1. FAO The State of World Fisheries and Aquaculture 2016. Rome: Food and Agriculture Organization of the United Nations; 2016
    [Google Scholar]
  2. Alvial A, Kibenge F, Forster J, Burgos JM, Ibarra R et al. The Recovery of the Chilean Salmon Industry: the ISA Crisis and its Consequences and Lessons Puerto Montt: Global Aquaculture Alliance; 2012 p. 85
    [Google Scholar]
  3. Sanders JE, Barros MJ. Evidence by the fluorescent antibody test for the occurrence of Renibacterium salmoninarum among salmonid fish in Chile. J Wildl Dis 1986; 22:255–257 [View Article][PubMed]
    [Google Scholar]
  4. SERNAPESCA. Informe Sobre Uso de Antimicrobianos en la Salmonicultura Nacional 2015 Valparaíso:: Departamento de Salud Animal;; 2015.
    [Google Scholar]
  5. Barnes AC, Delamare-Deboutteville J, Gudkovs N, Brosnahan C, Morrison R et al. Whole genome analysis of Yersinia ruckeri isolated over 27 years in Australia and New Zealand reveals geographical endemism over multiple lineages and recent evolution under host selection. Microb Genom 2016; 2:e000095 [View Article][PubMed]
    [Google Scholar]
  6. Bayliss SC, Verner-Jeffreys DW, Bartie KL, Aanensen DM, Sheppard SK et al. The promise of whole genome pathogen sequencing for the molecular epidemiology of emerging aquaculture pathogens. Front Microbiol 2017; 8:121 [View Article][PubMed]
    [Google Scholar]
  7. Brynildsrud O, Feil EJ, Bohlin J, Castillo-Ramirez S, Colquhoun D et al. Microevolution of Renibacterium salmoninarum: evidence for intercontinental dissemination associated with fish movements. ISME J 2014; 8:746–756 [View Article][PubMed]
    [Google Scholar]
  8. Bethke J, Quezada J, Poblete-Morales M, Irgang R, Yáñez A et al. Biochemical, serological, and genetic characterisation of Renibacterium salmoninarum isolates recovered from salmonids in Chile. Bull Eur Assoc Fish Pathol 2017; 37:169–180
    [Google Scholar]
  9. SUBPESCA Resolución Exenta No. 1741. Establece Clasificación de Enfermedades de Alto Riesgo Valparaíso: Subsecretaría de Pesca y Acuicultura; 2013
    [Google Scholar]
  10. SUBPESCA Reglamento de Medidas de Protección, Control y Erradicación de Enfermedades de Alto Riesgo para las Especies Hidrobiológicas, (Última Modificación D.S. No 216-2016) (F.D.O. 05-08-2017). Valparaíso: Subsecretaría de Pesca y Acuicultura; 2001
    [Google Scholar]
  11. SERNAPESCA Aprueba Programa Sanitario General de Manejo de la Reproducción de Peces (PSGR) Valparaíso: Servicio Nacional de Pesca y Acuicultura; 2013
    [Google Scholar]
  12. Evelyn TPT. An improved growth medium for the kidney disease bacterium and some notes on using the medium. Bull Off Int Epizoot 1977; 87:511–513
    [Google Scholar]
  13. Ponstingl H, Ning Z. SMALT-a new mapper for DNA sequencing reads. F1000 Posters 2010
    [Google Scholar]
  14. McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K et al. The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res 2010; 20:1297–1303 [View Article][PubMed]
    [Google Scholar]
  15. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics 2009; 25:2078–2079 [View Article][PubMed]
    [Google Scholar]
  16. Connor TR, Loman NJ, Thompson S, Smith A, Southgate J et al. CLIMB (the Cloud Infrastructure for Microbial Bioinformatics): an online resource for the medical microbiology community. Microb Genom 2016; 2:e000086 [View Article][PubMed]
    [Google Scholar]
  17. Kurtz S, Phillippy A, Delcher AL, Smoot M, Shumway M et al. Versatile and open software for comparing large genomes. Genome Biol 2004; 5:R12 [View Article][PubMed]
    [Google Scholar]
  18. Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 2014; 30:1312–1313 [View Article][PubMed]
    [Google Scholar]
  19. Jombart T, Kendall M, Almagro-Garcia J, Colijn C. treespace: statistical exploration of landscapes of phylogenetic trees. Mol Ecol Resour 2017; 17:1385–1392 [View Article][PubMed]
    [Google Scholar]
  20. Page AJ, Taylor B, Delaney AJ, Soares J, Seemann T et al. SNP-sites: rapid efficient extraction of SNPs from multi-FASTA alignments. Microb Genom 2016; 2:e000056 [View Article][PubMed]
    [Google Scholar]
  21. Croucher NJ, Page AJ, Connor TR, Delaney AJ, Keane JA et al. Rapid phylogenetic analysis of large samples of recombinant bacterial whole genome sequences using Gubbins. Nucleic Acids Res 2015; 43:e15 [View Article][PubMed]
    [Google Scholar]
  22. Didelot X, Wilson DJ. ClonalFrameML: efficient inference of recombination in whole bacterial genomes. PLoS Comput Biol 2015; 11:e1004041 [View Article][PubMed]
    [Google Scholar]
  23. Yu G, Smith DK, Zhu H, Guan Y, Lam TT-Y. ggtree: an r package for visualization and annotation of phylogenetic trees with their covariates and other associated data. Methods Ecol Evol 2017; 8:28–36 [View Article]
    [Google Scholar]
  24. Wickham H. Ggplot2: Elegant Graphics for Data Analysis, 2nd ed. New York: Springer; 2009
    [Google Scholar]
  25. Rambaut A, Lam TT, Max Carvalho L, Pybus OG. Exploring the temporal structure of heterochronous sequences using TempEst (formerly Path-O-Gen). Virus Evol 2016; 2:vew007 [View Article][PubMed]
    [Google Scholar]
  26. Bouckaert R, Heled J, Kühnert D, Vaughan T, Wu CH et al. BEAST 2: a software platform for Bayesian evolutionary analysis. PLoS Comput Biol 2014; 10:e1003537 [View Article][PubMed]
    [Google Scholar]
  27. Drummond AJ, Ho SY, Phillips MJ, Rambaut A. Relaxed phylogenetics and dating with confidence. PLoS Biol 2006; 4:e88 [View Article][PubMed]
    [Google Scholar]
  28. Argimón S, Abudahab K, Goater RJ, Fedosejev A, Bhai J et al. Microreact: visualizing and sharing data for genomic epidemiology and phylogeography. Microb Genom 2016; 2:e000093 [View Article][PubMed]
    [Google Scholar]
  29. Duchêne S, Holt KE, Weill FX, Le Hello S, Hawkey J et al. Genome-scale rates of evolutionary change in bacteria. Microb Genom 2016; 2:e000094 [View Article][PubMed]
    [Google Scholar]
  30. van Belkum A, Scherer S, van Alphen L, Verbrugh H. Short-sequence DNA repeats in prokaryotic genomes. Microbiol Mol Biol Rev 1998; 62:275–293[PubMed]
    [Google Scholar]
  31. United Nations A Case Study of the Salmon Industry in Chile New York and Geneva: United Nations. United Nations Conference on Trade and Development; 2006
    [Google Scholar]
  32. SUBPESCA Informe Sectorial Diciembre 2017 Valparaíso: Subsecretaría de Pesca y Acuicultura; 2018
    [Google Scholar]
  33. Godoy MG, Aedo A, Kibenge MJ, Groman DB, Yason CV et al. First detection, isolation and molecular characterization of infectious salmon anaemia virus associated with clinical disease in farmed Atlantic salmon (Salmo salar) in Chile. BMC Vet Res 2008; 4:28 [View Article][PubMed]
    [Google Scholar]
  34. Vike S, Nylund S, Nylund A. ISA virus in Chile: evidence of vertical transmission. Arch Virol 2009; 154:1–8 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/mgen/10.1099/mgen.0.000201
Loading
/content/journal/mgen/10.1099/mgen.0.000201
Loading

Data & Media loading...

Supplements

Supplementary File 1

PDF
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