1887

Abstract

Bacteria from the family have been implicated in mass mortalities of farmed Pacific oysters () in multiple countries, leading to substantial impairment of growth in the sector. In Ireland there has been concern that have been involved in serious summer outbreaks. There is evidence that is increasingly becoming the main pathogen of concern for the Pacific oyster industry in Ireland. While bacteria belonging to the clade are also detected frequently in mortality episodes, their role in the outbreaks of summer mortality is not well understood. To identify and characterize strains involved in these outbreaks, 43 isolates were recovered from Pacific oyster summer mass mortality episodes in Ireland from 2008 to 2015 and these were whole-genome sequenced. Among these, 25 were found to be (implicated in disease) and 18 were members of the species complex (role in disease undetermined). Two distinct clades of – clade A and clade B – were found that had previously been described as circulating within French oyster culture. The high degree of similarity between the Irish and French isolates points to translocation of the pathogen between Europe’s two major oyster-producing countries, probably via trade in spat and other age classes. isolates were more diverse, but the data reveal a single clone of this species that has spread across oyster farms in Ireland. This underscores that could be transmitted readily across oyster farms. The presence of clades A and B in not only France but also Ireland adds weight to growing concern that this pathogen is spreading and impacting Pacific oyster production within Europe.

Funding
This study was supported by the:
  • Marine Institute
    • Principle Award Recipient: NotApplicable
  • Department for Environment, Food and Rural Affairs, UK Government
    • Principle Award Recipient: DavidW. Verner-Jeffreys
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.
Loading

Article metrics loading...

/content/journal/mgen/10.1099/mgen.0.001078
2023-08-04
2024-05-01
Loading full text...

Full text loading...

/deliver/fulltext/mgen/9/8/mgen001078.html?itemId=/content/journal/mgen/10.1099/mgen.0.001078&mimeType=html&fmt=ahah

References

  1. Botta R, Asche F, Borsum JS, Camp EV. A review of global oyster aquaculture production and consumption. Marine Policy 2020; 117:103952 [View Article]
    [Google Scholar]
  2. Jennings S, Stentiford GD, Leocadio AM, Jeffery KR, Metcalfe JD et al. Aquatic food security: insights into challenges and solutions from an analysis of interactions between fisheries, aquaculture, food safety, human health, fish and human welfare, economy and environment. Fish Fish 2016; 17:893–938 [View Article]
    [Google Scholar]
  3. Barbosa Solomieu V, Renault T, Travers M-A. Mass mortality in bivalves and the intricate case of the Pacific oyster, Crassostrea gigas. J Invertebr Pathol 2015; 131:2–10 [View Article] [PubMed]
    [Google Scholar]
  4. Salvi D, Mariottini P. Revision shock in Pacific oysters taxonomy: the genus Magallana (formerly Crassostrea in part) is well-founded and necessary. Zool J Linn Soc 2021; 192:43–58 [View Article]
    [Google Scholar]
  5. Food and Agriculture Organization of the United Nations FAO Yearbook. fishery and aquaculture statistics 2019/FAO Annuaire. Statistiques des Pêches et de L’Aquaculture 2019/FAO Anuario. Estadísticas de Pesca Y Acuicultura 2019. Food Agriculture Org 2021
    [Google Scholar]
  6. Girard S, Pérez Agúndez JA. The effects of the oyster mortality crisis on the economics of the shellfish farming sector: preliminary review and prospects from a case study in Marennes-Oleron Bay (France). Mar Policy 2014; 48:142–151 [View Article]
    [Google Scholar]
  7. EFSA Panel on Animal Health and welfare (AHAW) Scientific opinion on the increased mortality events in Pacific oysters, Crassostrea gigas. EFSA J 2010; 8:1894 [View Article]
    [Google Scholar]
  8. Wendling CC, Wegner KM. Relative contribution of reproductive investment, thermal stress and Vibrio infection to summer mortality phenomena in Pacific oysters. Aquaculture 2013; 412–413:88–96 [View Article]
    [Google Scholar]
  9. Lemire A, Goudenège D, Versigny T, Petton B, Calteau A et al. Populations, not clones, are the unit of vibrio pathogenesis in naturally infected oysters. ISME J 2015; 9:1523–1531 [View Article] [PubMed]
    [Google Scholar]
  10. Segarra A, Pépin JF, Arzul I, Morga B, Faury N et al. Detection and description of a particular Ostreid herpesvirus 1 genotype associated with massive mortality outbreaks of Pacific oysters, Crassostrea gigas, in France in 2008. Virus Res 2010; 153:92–99 [View Article] [PubMed]
    [Google Scholar]
  11. European Union Reference Laboratory 2014 Annual meeting of the National reference Laboratories for Mollusc diseases; 2014; 22
  12. Collins E, McCleary S, Morrissey T, Geary M, Connor CO et al. Sporulating Haplosporidium nelsoni in Crassostrea gigas in a production Bay in Ireland. Bulletin of the EAFP 2018; 38:4–11
    [Google Scholar]
  13. McCleary S, Henshilwood K. Novel quantitative TaqMan® MGB real-time PCR for sensitive detection of Vibrio aestuarianus in Crassostrea gigas. Dis Aquat Organ 2015; 114:239–248 [View Article] [PubMed]
    [Google Scholar]
  14. Lane DJ, Pace B, Olsen GJ, Stahl DA, Sogin ML et al. Rapid determination of 16S ribosomal RNA sequences for phylogenetic analyses. Proc Natl Acad Sci 1985; 82:6955–6959 [View Article]
    [Google Scholar]
  15. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 2014; 30:2114–2120 [View Article] [PubMed]
    [Google Scholar]
  16. Andrews S. FastQC: A Quality Control Tool for High Throughput Sequence Data Cambridge, United Kingdom: Babraham Bioinformatics, Babraham Institute; 2010
    [Google Scholar]
  17. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 2012; 19:455–477 [View Article] [PubMed]
    [Google Scholar]
  18. Magoč T, Salzberg SL. FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 2011; 27:2957–2963 [View Article] [PubMed]
    [Google Scholar]
  19. 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]
  20. Li H, Durbin R. Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 2009; 25:1754–1760 [View Article]
    [Google Scholar]
  21. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014; 30:2068–2069 [View Article] [PubMed]
    [Google Scholar]
  22. Gurevich A, Saveliev V, Vyahhi N, Tesler G. QUAST: quality assessment tool for genome assemblies. Bioinformatics 2013; 29:1072–1075 [View Article] [PubMed]
    [Google Scholar]
  23. Goudenège D, Travers MA, Lemire A, Petton B, Haffner P et al. A single regulatory gene is sufficient to alter Vibrio aestuarianus pathogenicity in oysters. Environ Microbiol 2015; 17:4189–4199 [View Article] [PubMed]
    [Google Scholar]
  24. Pruitt KD, Tatusova T, Maglott DR. NCBI reference sequences (RefSeq): a curated non-redundant sequence database of genomes, transcripts and proteins. Nucleic Acids Res 2007; 35:D61–5 [View Article] [PubMed]
    [Google Scholar]
  25. Bayliss SC, Thorpe HA, Coyle NM, Sheppard SK, Feil EJ. PIRATE: a fast and scalable pangenomics toolbox for clustering diverged orthologues in bacteria. Gigascience 2019; 8:giz119 [View Article] [PubMed]
    [Google Scholar]
  26. Hadfield J, Croucher NJ, Goater RJ, Abudahab K, Aanensen DM et al. Phandango: an interactive viewer for bacterial population genomics. Bioinformatics 2017 [View Article]
    [Google Scholar]
  27. Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 2013; 30:772–780 [View Article] [PubMed]
    [Google Scholar]
  28. R Core Team R: A language and environment for statistical computing; 2013
  29. Kozlov AM, Darriba D, Flouri T, Morel B, Stamatakis A. RAxML-NG: a fast, scalable and user-friendly tool for maximum likelihood phylogenetic inference. Bioinformatics 2019; 35:4453–4455 [View Article] [PubMed]
    [Google Scholar]
  30. Crandall KA, Lagergren J. Rapid neighbour-joining. In Algorithms in Bioinformatics Berlin, Heidelberg: Springer; 2008 pp 113–122 [View Article]
    [Google Scholar]
  31. Rambaut A. FigTree; 2016
  32. Argimón S, Abudahab K, Goater RJE, 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]
  33. Ranjith KM, Brinda K, Arjun U, Hegde NG, Nath R. Double phase transition in the triangular antiferromagnet Ba3CoTa2O9. J Phys Condens Matter 2017; 29:115804 [View Article] [PubMed]
    [Google Scholar]
  34. Zhou Y, Liang Y, Lynch KH, Dennis JJ, Wishart DS. PHAST: a fast phage search tool. Nucleic Acids Res 2011; 39:W347–52 [View Article] [PubMed]
    [Google Scholar]
  35. 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]
  36. Liu M, Hao G, Li Z, Zhou Y, Garcia-Sillas R et al. CitAB two-component system-regulated citrate utilization contributes to Vibrio cholerae competitiveness with the gut microbiota. Infect Immun 2019; 87:e00746-18 [View Article] [PubMed]
    [Google Scholar]
  37. Davies BW, Bogard RW, Young TS, Mekalanos JJ. Coordinated regulation of accessory genetic elements produces cyclic di-nucleotides for V. cholerae virulence. Cell 2012; 149:358–370 [View Article] [PubMed]
    [Google Scholar]
  38. Pérez-Cataluña A, Lucena T, Tarazona E, Arahal DR, Macián MC et al. An MLSA approach for the taxonomic update of the Splendidus clade, a lineage containing several fish and shellfish pathogenic Vibrio spp. Syst Appl Microbiol 2016; 39:361–369 [View Article] [PubMed]
    [Google Scholar]
  39. Omata T, Gohta S, Takahashi Y, Harano Y, Maeda S. Involvement of a CbbR homolog in low CO2-induced activation of the bicarbonate transporter operon in cyanobacteria. J Bacteriol 2001; 183:1891–1898 [View Article] [PubMed]
    [Google Scholar]
  40. Grudniak AM, Markowska K, Wolska KI. Interactions of Escherichia coli molecular chaperone HtpG with DnaA replication initiator DNA. Cell Stress Chaperones 2015; 20:951–957 [View Article] [PubMed]
    [Google Scholar]
  41. Chao L, Rakshe S, Leff M, Spormann AM. PdeB, a cyclic Di-GMP-specific phosphodiesterase that regulates Shewanella oneidensis MR-1 motility and biofilm formation. J Bacteriol 2013; 195:3827–3833 [View Article] [PubMed]
    [Google Scholar]
  42. European Union Reference Laboratory Annual Meeting and Seventh Combined Technical Workshop of the National Reference Laboratories for Mollusc Diseases. Ifremer 2016
    [Google Scholar]
  43. European Union Reference Laboratory Report of the 2020 Annual Meeting of National Reference Laboratories for Mollusc Diseases (IFREMER). Ifremer; 2020
  44. Roux FL, Wegner KM, Baker-Austin C, Vezzulli L, Osorio CR et al. The emergence of Vibrio pathogens in Europe: ecology, evolution, and pathogenesis (Paris, 11–12th March 2015). Front Microbiol 2015; 6: [View Article]
    [Google Scholar]
  45. Mesnil A, Jacquot M, Garcia C, Tourbiez D, Canier L et al. Emergence and clonal expansion of Vibrio aestuarianus lineages pathogenic for oysters in Europe. Mol Ecol 2023; 32:2869–2883 [View Article] [PubMed]
    [Google Scholar]
  46. 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]
  47. Koskiniemi S, Sun S, Berg OG, Andersson DI. Selection-driven gene loss in bacteria. PLoS Genet 2012; 8:e1002787 [View Article] [PubMed]
    [Google Scholar]
  48. Le Roux F, Zouine M, Chakroun N, Binesse J, Saulnier D et al. Genome sequence of Vibrio splendidus: an abundant planctonic marine species with a large genotypic diversity. Environ Microbiol 2009; 11:1959–1970 [View Article] [PubMed]
    [Google Scholar]
  49. Gay M, Renault T, Pons A-M, Le Roux F. Two vibrio splendidus related strains collaborate to kill Crassostrea gigas: taxonomy and host alterations. Dis Aquat Organ 2004; 62:65–74 [View Article] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/mgen/10.1099/mgen.0.001078
Loading
/content/journal/mgen/10.1099/mgen.0.001078
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Supplementary material 2

EXCEL
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