Pan-genome survey of the fish pathogen Yersinia ruckeri links accessory- and amplified genes to virulence

Andreas Riborg; Snorre Gulla; Eve Zeyl Fiskebeck; David Ryder; David W Verner-Jeffreys; Duncan J Colquhoun; Timothy J Welch

doi:10.1371/journal.pone.0285257

Pan-genome survey of the fish pathogen Yersinia ruckeri links accessory- and amplified genes to virulence

PLoS One. 2023 May 11;18(5):e0285257. doi: 10.1371/journal.pone.0285257. eCollection 2023.

Authors

Andreas Riborg^{1

2}, Snorre Gulla¹, Eve Zeyl Fiskebeck¹, David Ryder³, David W Verner-Jeffreys³, Duncan J Colquhoun^{1

4}, Timothy J Welch⁵

Affiliations

¹ Norwegian Veterinary Institute, Ås, Norway.
² Vaxxinova Norway AS, Bergen, Norway.
³ Centre for Environment, Fisheries and Aquaculture Science (CEFAS), Weymouth, Dorset, United Kingdom.
⁴ University of Bergen, Bergen, Norway.
⁵ National Centre for Cool and Coldwater Aquaculture, USDA-ARS, Leetown, WV, United States of America.

Abstract

While both virulent and putatively avirulent Yersinia ruckeri strains exist in aquaculture environments, the relationship between the distribution of virulence-associated factors and de facto pathogenicity in fish remains poorly understood. Pan-genome analysis of 18 complete genomes, representing established virulent and putatively avirulent lineages of Y. ruckeri, revealed the presence of a number of accessory genetic determinants. Further investigation of 68 draft genome assemblies revealed that the distribution of certain putative virulence factors correlated well with virulence and host-specificity. The inverse-autotransporter invasin locus yrIlm was, however, the only gene present in all virulent strains, while absent in lineages regarded as avirulent. Strains known to be associated with significant mortalities in salmonid aquaculture display a combination of serotype O1-LPS and yrIlm, with the well-documented highly virulent lineages, represented by MLVA clonal complexes 1 and 2, displaying duplication of the yrIlm locus. Duplication of the yrIlm locus was further found to have evolved over time in clonal complex 1, where some modern, highly virulent isolates display up to three copies.

Copyright: This is an open access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Animals
Fish Diseases*
Oncorhynchus mykiss*
Serogroup
Virulence / genetics
Yersinia Infections*
Yersinia ruckeri / genetics

Grants and funding

AR was funded by Norwegian Research Council grant 297312 (https://www.forskningsradet.no/en/), Vaxxinova Norway AS (https://en.vaxxinova.no) and Aquagen AS (https://www.aquagen.no/en). DJC, SG and EZF were funded by Norwegian Seafood Research Fund grant 901505 (https://www.fhf.no). TW was funded by USDA CRIS project number 8082-32000-007-000-D (https://www.nifa.usda.gov/cris). DR and DVJ were funded by the BBSRC (https://www.ukri.org/councils/bbsrc/) / NERC (https://www.ukri.org/councils/nerc/) on the sustainable aquaculture call (BB/M026388/1), and Cefas (https://www.cefas.co.uk) and Defra (https://www.gov.uk/government/organisations/department-for-environment-food-rural-affairs/services-information) contract FB002. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.