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: Macqueen, Daniel J, Eve, Oliver, Gundappa, Manu Kumar, Daniels, Rose Ruiz, Gallagher, Michael D, Alexandersen, Svein, Karlsen, Marius
Other Authors: Biotechnology and Biological Sciences Research Council, The Norwegian Seafood Research Fund, Roslin Institute, Bionano Genomics, PHARMAQ, orcid:0000-0001-8050-7722, orcid:0000-0003-4328-2178
Format: Article in Journal/Newspaper
Language:English
Published: MDPI AG 2021
Subjects:
Online Access:http://hdl.handle.net/1893/35888
https://doi.org/10.3390/v13122549
http://dspace.stir.ac.uk/retrieve/930efc2a-ed74-4693-927d-ebc078679290/viruses-13-02549.pdf
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spelling ftunivstirling:oai:dspace.stir.ac.uk:1893/35888 2024-04-28T08:13:47+00:00 Genomic Epidemiology of Salmonid Alphavirus in Norwegian Aquaculture Reveals Recent Subtype-2 Transmission Dynamics and Novel Subtype-3 Lineages Macqueen, Daniel J Eve, Oliver Gundappa, Manu Kumar Daniels, Rose Ruiz Gallagher, Michael D Alexandersen, Svein Karlsen, Marius Biotechnology and Biological Sciences Research Council The Norwegian Seafood Research Fund Roslin Institute Bionano Genomics PHARMAQ orcid:0000-0001-8050-7722 orcid:0000-0003-4328-2178 2021 application/pdf http://hdl.handle.net/1893/35888 https://doi.org/10.3390/v13122549 http://dspace.stir.ac.uk/retrieve/930efc2a-ed74-4693-927d-ebc078679290/viruses-13-02549.pdf en eng MDPI AG Macqueen DJ, Eve O, Gundappa MK, Daniels RR, Gallagher MD, Alexandersen S & Karlsen M (2021) Genomic Epidemiology of Salmonid Alphavirus in Norwegian Aquaculture Reveals Recent Subtype-2 Transmission Dynamics and Novel Subtype-3 Lineages. Viruses , 13 (12), Art. No.: 2549. https://doi.org/10.3390/v13122549 2549 http://hdl.handle.net/1893/35888 doi:10.3390/v13122549 34960818 WOS:000737476700001 2-s2.0-85121623089 1988741 http://dspace.stir.ac.uk/retrieve/930efc2a-ed74-4693-927d-ebc078679290/viruses-13-02549.pdf © 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/). http://creativecommons.org/licenses/by/4.0/ genomic epidemiology genomic surveillance viral genomics aquaculture salmonid alphavirus pancreas disease Journal Article VoR - Version of Record 2021 ftunivstirling https://doi.org/10.3390/v13122549 2024-04-03T14:08:14Z 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 University of Stirling: Stirling Digital Research Repository Viruses 13 12 2549
institution Open Polar
collection University of Stirling: Stirling Digital Research Repository
op_collection_id ftunivstirling
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
Macqueen, Daniel J
Eve, Oliver
Gundappa, Manu Kumar
Daniels, Rose Ruiz
Gallagher, Michael D
Alexandersen, Svein
Karlsen, Marius
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.
author2 Biotechnology and Biological Sciences Research Council
The Norwegian Seafood Research Fund
Roslin Institute
Bionano Genomics
PHARMAQ
orcid:0000-0001-8050-7722
orcid:0000-0003-4328-2178
format Article in Journal/Newspaper
author Macqueen, Daniel J
Eve, Oliver
Gundappa, Manu Kumar
Daniels, Rose Ruiz
Gallagher, Michael D
Alexandersen, Svein
Karlsen, Marius
author_facet Macqueen, Daniel J
Eve, Oliver
Gundappa, Manu Kumar
Daniels, Rose Ruiz
Gallagher, Michael D
Alexandersen, Svein
Karlsen, Marius
author_sort Macqueen, Daniel J
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 http://hdl.handle.net/1893/35888
https://doi.org/10.3390/v13122549
http://dspace.stir.ac.uk/retrieve/930efc2a-ed74-4693-927d-ebc078679290/viruses-13-02549.pdf
genre Atlantic salmon
genre_facet Atlantic salmon
op_relation Macqueen DJ, Eve O, Gundappa MK, Daniels RR, Gallagher MD, Alexandersen S & Karlsen M (2021) Genomic Epidemiology of Salmonid Alphavirus in Norwegian Aquaculture Reveals Recent Subtype-2 Transmission Dynamics and Novel Subtype-3 Lineages. Viruses , 13 (12), Art. No.: 2549. https://doi.org/10.3390/v13122549
2549
http://hdl.handle.net/1893/35888
doi:10.3390/v13122549
34960818
WOS:000737476700001
2-s2.0-85121623089
1988741
http://dspace.stir.ac.uk/retrieve/930efc2a-ed74-4693-927d-ebc078679290/viruses-13-02549.pdf
op_rights © 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
http://creativecommons.org/licenses/by/4.0/
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container_title Viruses
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