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: Text
Language:English
Published: Multidisciplinary Digital Publishing Institute 2021
Subjects:
Online Access:https://doi.org/10.3390/v13122549
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spelling ftmdpi:oai:mdpi.com:/1999-4915/13/12/2549/ 2023-08-20T04:05:21+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 agris 2021-12-20 application/pdf https://doi.org/10.3390/v13122549 EN eng Multidisciplinary Digital Publishing Institute Animal Viruses https://dx.doi.org/10.3390/v13122549 https://creativecommons.org/licenses/by/4.0/ Viruses; Volume 13; Issue 12; Pages: 2549 genomic epidemiology genomic surveillance viral genomics aquaculture salmonid alphavirus pancreas disease Text 2021 ftmdpi https://doi.org/10.3390/v13122549 2023-08-01T03:36:06Z 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. Text Atlantic salmon MDPI Open Access Publishing Norway Sav’ ENVELOPE(156.400,156.400,68.817,68.817) Viruses 13 12 2549
institution Open Polar
collection MDPI Open Access Publishing
op_collection_id ftmdpi
language English
topic genomic epidemiology
genomic surveillance
viral genomics
aquaculture
salmonid alphavirus
pancreas disease
spellingShingle genomic epidemiology
genomic surveillance
viral genomics
aquaculture
salmonid alphavirus
pancreas disease
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
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 Text
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 Multidisciplinary Digital Publishing Institute
publishDate 2021
url https://doi.org/10.3390/v13122549
op_coverage agris
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; Volume 13; Issue 12; Pages: 2549
op_relation Animal Viruses
https://dx.doi.org/10.3390/v13122549
op_rights https://creativecommons.org/licenses/by/4.0/
op_doi https://doi.org/10.3390/v13122549
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