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

Viruses. 2019 May 22;11(5):465. doi: 10.3390/v11050465.

Abstract

Heart and skeletal muscle inflammation (HSMI) in farmed Atlantic salmon (Salmo salar) was first diagnosed in Norway in 1999. The disease is caused by Piscine orthoreovirus-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.

Keywords: HSMI; PRV-1; Piscine orthoreovirus; reassortment; viral evolution; virulence.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Animals
  • Evolution, Molecular*
  • Fish Diseases / virology*
  • Genome, Viral*
  • High-Throughput Nucleotide Sequencing
  • Muscle, Skeletal / pathology
  • Muscle, Skeletal / virology
  • Myocardium
  • Norway
  • Open Reading Frames
  • Orthoreovirus / genetics*
  • Phylogeny
  • Reassortant Viruses
  • Reoviridae Infections / veterinary*
  • Salmo salar / genetics*
  • Salmo salar / virology*
  • Virulence

Supplementary concepts

  • Piscine orthoreovirus