Evolution of the <i>Piscine orthoreovirus</i> Genome Linked to Emergence of Heart and Skeletal Muscle Inflammation in Farmed Atlantic Salmon (<i>Salmo salar</i>)

Heart and skeletal muscle inflammation (HSMI) in farmed Atlantic salmon (<i>Salmo salar)</i> was first diagnosed in Norway in 1999. The disease is caused by <i>Piscine orthoreovirus</i>-1 (PRV-1). The virus is prevalent in farmed Atlantic salmon, but not always associated wit...

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Main Authors: Kannimuthu Dhamotharan, Torstein Tengs, Øystein Wessel, Stine Braaen, Ingvild B. Nyman, Elisabeth F. Hansen, Debes H. Christiansen, Maria K. Dahle, Espen Rimstad, Turhan Markussen
Format: Article
Language:English
Published: MDPI AG 2019-05-01
Series:Viruses
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Online Access:https://www.mdpi.com/1999-4915/11/5/465
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author Kannimuthu Dhamotharan
Torstein Tengs
Øystein Wessel
Stine Braaen
Ingvild B. Nyman
Elisabeth F. Hansen
Debes H. Christiansen
Maria K. Dahle
Espen Rimstad
Turhan Markussen
author_facet Kannimuthu Dhamotharan
Torstein Tengs
Øystein Wessel
Stine Braaen
Ingvild B. Nyman
Elisabeth F. Hansen
Debes H. Christiansen
Maria K. Dahle
Espen Rimstad
Turhan Markussen
author_sort Kannimuthu Dhamotharan
collection DOAJ
description Heart and skeletal muscle inflammation (HSMI) in farmed Atlantic salmon (<i>Salmo salar)</i> was first diagnosed in Norway in 1999. The disease is caused by <i>Piscine orthoreovirus</i>-1 (PRV-1). The virus is prevalent in farmed Atlantic salmon, but not always associated with disease. Phylogeny and sequence analyses of 31 PRV-1 genomes collected over a 30-year period from fish with or without HSMI, grouped the viral sequences into two main monophylogenetic clusters, one associated with HSMI and the other with low virulent PRV-1 isolates. A PRV-1 strain from Norway sampled in 1988, a decade before the emergence of HSMI, grouped with the low virulent HSMI cluster. The two distinct monophylogenetic clusters were particularly evident for segments S1 and M2. Only a limited number of amino acids were unique to the association with HSMI, and they all located to S1 and M2 encoded proteins. The observed co-evolution of the S1-M2 pair coincided in time with the emergence of HSMI in Norway, and may have evolved through accumulation of mutations and/or segment reassortment. Sequences of S1-M2 suggest selection of the HSMI associated pair, and that this segment pair has remained almost unchanged in Norwegian salmon aquaculture since 1997. PRV-1 strains from the North American Pacific Coast and Faroe Islands have not undergone this evolution, and are more closely related to the PRV-1 precursor strains not associated with clinical HSMI.
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spelling doaj.art-0575ecd2602b4584b09c0864ea93897c2022-12-21T19:55:17ZengMDPI AGViruses1999-49152019-05-0111546510.3390/v11050465v11050465Evolution of the <i>Piscine orthoreovirus</i> Genome Linked to Emergence of Heart and Skeletal Muscle Inflammation in Farmed Atlantic Salmon (<i>Salmo salar</i>)Kannimuthu Dhamotharan0Torstein Tengs1Øystein Wessel2Stine Braaen3Ingvild B. Nyman4Elisabeth F. Hansen5Debes H. Christiansen6Maria K. Dahle7Espen Rimstad8Turhan Markussen9Faculty of Veterinary Medicine, Norwegian University of Life Sciences, 0454 Oslo, NorwayFaculty of Chemistry, Biotechnology and Food Science, Norwegian University of Life Sciences, 1433 Ås, NorwayFaculty of Veterinary Medicine, Norwegian University of Life Sciences, 0454 Oslo, NorwayFaculty of Veterinary Medicine, Norwegian University of Life Sciences, 0454 Oslo, NorwayFaculty of Veterinary Medicine, Norwegian University of Life Sciences, 0454 Oslo, NorwayFaculty of Veterinary Medicine, Norwegian University of Life Sciences, 0454 Oslo, NorwayFaroese Food and Veterinary Authority, National Reference Laboratory for Fish Diseases, FO-110 Tórshavn, Faroe IslandsDepartment of Immunology, Norwegian Veterinary Institute, 0454 Oslo, NorwayFaculty of Veterinary Medicine, Norwegian University of Life Sciences, 0454 Oslo, NorwayFaculty of Veterinary Medicine, Norwegian University of Life Sciences, 0454 Oslo, NorwayHeart and skeletal muscle inflammation (HSMI) in farmed Atlantic salmon (<i>Salmo salar)</i> was first diagnosed in Norway in 1999. The disease is caused by <i>Piscine orthoreovirus</i>-1 (PRV-1). The virus is prevalent in farmed Atlantic salmon, but not always associated with disease. Phylogeny and sequence analyses of 31 PRV-1 genomes collected over a 30-year period from fish with or without HSMI, grouped the viral sequences into two main monophylogenetic clusters, one associated with HSMI and the other with low virulent PRV-1 isolates. A PRV-1 strain from Norway sampled in 1988, a decade before the emergence of HSMI, grouped with the low virulent HSMI cluster. The two distinct monophylogenetic clusters were particularly evident for segments S1 and M2. Only a limited number of amino acids were unique to the association with HSMI, and they all located to S1 and M2 encoded proteins. The observed co-evolution of the S1-M2 pair coincided in time with the emergence of HSMI in Norway, and may have evolved through accumulation of mutations and/or segment reassortment. Sequences of S1-M2 suggest selection of the HSMI associated pair, and that this segment pair has remained almost unchanged in Norwegian salmon aquaculture since 1997. PRV-1 strains from the North American Pacific Coast and Faroe Islands have not undergone this evolution, and are more closely related to the PRV-1 precursor strains not associated with clinical HSMI.https://www.mdpi.com/1999-4915/11/5/465PRV-1<i>Piscine orthoreovirus</i>HSMIvirulencereassortmentviral evolution
spellingShingle Kannimuthu Dhamotharan
Torstein Tengs
Øystein Wessel
Stine Braaen
Ingvild B. Nyman
Elisabeth F. Hansen
Debes H. Christiansen
Maria K. Dahle
Espen Rimstad
Turhan Markussen
Evolution of the <i>Piscine orthoreovirus</i> Genome Linked to Emergence of Heart and Skeletal Muscle Inflammation in Farmed Atlantic Salmon (<i>Salmo salar</i>)
Viruses
PRV-1
<i>Piscine orthoreovirus</i>
HSMI
virulence
reassortment
viral evolution
title Evolution of the <i>Piscine orthoreovirus</i> Genome Linked to Emergence of Heart and Skeletal Muscle Inflammation in Farmed Atlantic Salmon (<i>Salmo salar</i>)
title_full Evolution of the <i>Piscine orthoreovirus</i> Genome Linked to Emergence of Heart and Skeletal Muscle Inflammation in Farmed Atlantic Salmon (<i>Salmo salar</i>)
title_fullStr Evolution of the <i>Piscine orthoreovirus</i> Genome Linked to Emergence of Heart and Skeletal Muscle Inflammation in Farmed Atlantic Salmon (<i>Salmo salar</i>)
title_full_unstemmed Evolution of the <i>Piscine orthoreovirus</i> Genome Linked to Emergence of Heart and Skeletal Muscle Inflammation in Farmed Atlantic Salmon (<i>Salmo salar</i>)
title_short Evolution of the <i>Piscine orthoreovirus</i> Genome Linked to Emergence of Heart and Skeletal Muscle Inflammation in Farmed Atlantic Salmon (<i>Salmo salar</i>)
title_sort evolution of the i piscine orthoreovirus i genome linked to emergence of heart and skeletal muscle inflammation in farmed atlantic salmon i salmo salar i
topic PRV-1
<i>Piscine orthoreovirus</i>
HSMI
virulence
reassortment
viral evolution
url https://www.mdpi.com/1999-4915/11/5/465
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