Genomic Epidemiology of Salmonid Alphavirus in Norwegian Aquaculture Reveals Recent Subtype-2 Transmission Dynamics and Novel Subtype-3 Lineages

Viral disease poses a major barrier to sustainable aquaculture, with outbreaks causing large economic losses and growing concerns for fish welfare. Genomic epidemiology can support disease control by providing rapid inferences on viral evolution and disease transmission. In this study, genomic epide...

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Published in:Viruses
Main Authors: Daniel J. Macqueen, Oliver Eve, Manu Kumar Gundappa, Rose Ruiz Daniels, Michael D. Gallagher, Svein Alexandersen, Marius Karlsen
Format: Article in Journal/Newspaper
Language:English
Published: MDPI AG 2021
Subjects:
Online Access:https://doi.org/10.3390/v13122549
https://doaj.org/article/f957c8d09f7449578d1ec803c216422d
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spelling ftdoajarticles:oai:doaj.org/article:f957c8d09f7449578d1ec803c216422d 2023-05-15T15:32:58+02:00 Genomic Epidemiology of Salmonid Alphavirus in Norwegian Aquaculture Reveals Recent Subtype-2 Transmission Dynamics and Novel Subtype-3 Lineages Daniel J. Macqueen Oliver Eve Manu Kumar Gundappa Rose Ruiz Daniels Michael D. Gallagher Svein Alexandersen Marius Karlsen 2021-12-01T00:00:00Z https://doi.org/10.3390/v13122549 https://doaj.org/article/f957c8d09f7449578d1ec803c216422d EN eng MDPI AG https://www.mdpi.com/1999-4915/13/12/2549 https://doaj.org/toc/1999-4915 doi:10.3390/v13122549 1999-4915 https://doaj.org/article/f957c8d09f7449578d1ec803c216422d Viruses, Vol 13, Iss 2549, p 2549 (2021) genomic epidemiology genomic surveillance viral genomics aquaculture salmonid alphavirus pancreas disease Microbiology QR1-502 article 2021 ftdoajarticles https://doi.org/10.3390/v13122549 2022-12-31T12:43:57Z Viral disease poses a major barrier to sustainable aquaculture, with outbreaks causing large economic losses and growing concerns for fish welfare. Genomic epidemiology can support disease control by providing rapid inferences on viral evolution and disease transmission. In this study, genomic epidemiology was used to investigate salmonid alphavirus (SAV), the causative agent of pancreas disease (PD) in Atlantic salmon. Our aim was to reconstruct SAV subtype-2 (SAV2) diversity and transmission dynamics in recent Norwegian aquaculture, including the origin of SAV2 in regions where this subtype is not tolerated under current legislation. Using nanopore sequencing, we captured ~90% of the SAV2 genome for n = 68 field isolates from 10 aquaculture production regions sampled between 2018 and 2020. Using time-calibrated phylogenetics, we infer that, following its introduction to Norway around 2010, SAV2 split into two clades (SAV2a and 2b) around 2013. While co-present at the same sites near the boundary of Møre og Romsdal and Trøndelag, SAV2a and 2b were generally detected in non-overlapping locations at more Southern and Northern latitudes, respectively. We provide evidence for recent SAV2 transmission over large distances, revealing a strong connection between Møre og Romsdal and SAV2 detected in 2019/20 in Rogaland. We also demonstrate separate introductions of SAV2a and 2b outside the SAV2 zone in Sognefjorden (Vestland), connected to samples from Møre og Romsdal and Trøndelag, respectively, and a likely 100 km Northward transmission of SAV2b within Trøndelag. Finally, we recovered genomes of SAV2a and SAV3 co-infecting single fish in Rogaland, involving novel SAV3 lineages that diverged from previously characterized strains >25 years ago. Overall, this study demonstrates useful applications of genomic epidemiology for tracking viral disease spread in aquaculture. Article in Journal/Newspaper Atlantic salmon Directory of Open Access Journals: DOAJ Articles Norway Sav’ ENVELOPE(156.400,156.400,68.817,68.817) Viruses 13 12 2549
institution Open Polar
collection Directory of Open Access Journals: DOAJ Articles
op_collection_id ftdoajarticles
language English
topic genomic epidemiology
genomic surveillance
viral genomics
aquaculture
salmonid alphavirus
pancreas disease
Microbiology
QR1-502
spellingShingle genomic epidemiology
genomic surveillance
viral genomics
aquaculture
salmonid alphavirus
pancreas disease
Microbiology
QR1-502
Daniel J. Macqueen
Oliver Eve
Manu Kumar Gundappa
Rose Ruiz Daniels
Michael D. Gallagher
Svein Alexandersen
Marius Karlsen
Genomic Epidemiology of Salmonid Alphavirus in Norwegian Aquaculture Reveals Recent Subtype-2 Transmission Dynamics and Novel Subtype-3 Lineages
topic_facet genomic epidemiology
genomic surveillance
viral genomics
aquaculture
salmonid alphavirus
pancreas disease
Microbiology
QR1-502
description Viral disease poses a major barrier to sustainable aquaculture, with outbreaks causing large economic losses and growing concerns for fish welfare. Genomic epidemiology can support disease control by providing rapid inferences on viral evolution and disease transmission. In this study, genomic epidemiology was used to investigate salmonid alphavirus (SAV), the causative agent of pancreas disease (PD) in Atlantic salmon. Our aim was to reconstruct SAV subtype-2 (SAV2) diversity and transmission dynamics in recent Norwegian aquaculture, including the origin of SAV2 in regions where this subtype is not tolerated under current legislation. Using nanopore sequencing, we captured ~90% of the SAV2 genome for n = 68 field isolates from 10 aquaculture production regions sampled between 2018 and 2020. Using time-calibrated phylogenetics, we infer that, following its introduction to Norway around 2010, SAV2 split into two clades (SAV2a and 2b) around 2013. While co-present at the same sites near the boundary of Møre og Romsdal and Trøndelag, SAV2a and 2b were generally detected in non-overlapping locations at more Southern and Northern latitudes, respectively. We provide evidence for recent SAV2 transmission over large distances, revealing a strong connection between Møre og Romsdal and SAV2 detected in 2019/20 in Rogaland. We also demonstrate separate introductions of SAV2a and 2b outside the SAV2 zone in Sognefjorden (Vestland), connected to samples from Møre og Romsdal and Trøndelag, respectively, and a likely 100 km Northward transmission of SAV2b within Trøndelag. Finally, we recovered genomes of SAV2a and SAV3 co-infecting single fish in Rogaland, involving novel SAV3 lineages that diverged from previously characterized strains >25 years ago. Overall, this study demonstrates useful applications of genomic epidemiology for tracking viral disease spread in aquaculture.
format Article in Journal/Newspaper
author Daniel J. Macqueen
Oliver Eve
Manu Kumar Gundappa
Rose Ruiz Daniels
Michael D. Gallagher
Svein Alexandersen
Marius Karlsen
author_facet Daniel J. Macqueen
Oliver Eve
Manu Kumar Gundappa
Rose Ruiz Daniels
Michael D. Gallagher
Svein Alexandersen
Marius Karlsen
author_sort Daniel J. Macqueen
title Genomic Epidemiology of Salmonid Alphavirus in Norwegian Aquaculture Reveals Recent Subtype-2 Transmission Dynamics and Novel Subtype-3 Lineages
title_short Genomic Epidemiology of Salmonid Alphavirus in Norwegian Aquaculture Reveals Recent Subtype-2 Transmission Dynamics and Novel Subtype-3 Lineages
title_full Genomic Epidemiology of Salmonid Alphavirus in Norwegian Aquaculture Reveals Recent Subtype-2 Transmission Dynamics and Novel Subtype-3 Lineages
title_fullStr Genomic Epidemiology of Salmonid Alphavirus in Norwegian Aquaculture Reveals Recent Subtype-2 Transmission Dynamics and Novel Subtype-3 Lineages
title_full_unstemmed Genomic Epidemiology of Salmonid Alphavirus in Norwegian Aquaculture Reveals Recent Subtype-2 Transmission Dynamics and Novel Subtype-3 Lineages
title_sort genomic epidemiology of salmonid alphavirus in norwegian aquaculture reveals recent subtype-2 transmission dynamics and novel subtype-3 lineages
publisher MDPI AG
publishDate 2021
url https://doi.org/10.3390/v13122549
https://doaj.org/article/f957c8d09f7449578d1ec803c216422d
long_lat ENVELOPE(156.400,156.400,68.817,68.817)
geographic Norway
Sav’
geographic_facet Norway
Sav’
genre Atlantic salmon
genre_facet Atlantic salmon
op_source Viruses, Vol 13, Iss 2549, p 2549 (2021)
op_relation https://www.mdpi.com/1999-4915/13/12/2549
https://doaj.org/toc/1999-4915
doi:10.3390/v13122549
1999-4915
https://doaj.org/article/f957c8d09f7449578d1ec803c216422d
op_doi https://doi.org/10.3390/v13122549
container_title Viruses
container_volume 13
container_issue 12
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