Analysis of Piscine orthoreovirus genotype 1 genomes collected over a 32-year period (1988–2020) suggests a fitness peak in salmon hosts with minimal evidence for temporal divergence

Abstract Piscine orthoreovirus genotype-1 (PRV-1) is a double-stranded non-enveloped RNA virus that has two subtypes (PRV-1a and PRV-1b) with members of PRV-1b considered to be more virulent than members of PRV-1a. PRV-1 is commonly found in wild and farmed salmonids of the Northeast Pacific (PRV-1a only), North Atlantic and Chilean waters (PRV-1a and PRV-1b). We are interested in understanding the original source of PRV-1, the timing of its introduction, and the role that salmon farming has in the spread and maintenance of PRV-1 in the Northeast Pacific, as well as in other regions. To this end, we generated 179 concatenated coding genome sequences of PRV-1a from archived/historical, as well as contemporary clinical and environmental samples, collected primarily in the Northeast Pacific. These concatenated genomes, along with 152 concatenated genomes generated using sequences from GenBank, were used to generate Northeast Pacific (n = 302 genomes) and Global (n = 331 genomes) datasets. In both datasets, we found that evidence for a temporal signal is restricted to a single clade from the Northeast Pacific, so conducting divergence time estimations for the entire Northeast Pacific and Global datasets was not undertaken. However, partial PRV-1 sequences obtained from histology samples collected in 1977 show that PRV-1a has been in the Northeast Pacific for at least 47 years, and we propose based on the probability of detection, that it was likely widely distributed at that time. With the exception of a recently introduced genetic variant, WCAN_BC17_AS_2017, PRV-1a variants from the Northeast Pacific form 3 well-supported clades at the genome level. All clades contain sequences from farmed and wild salmon, although one PRV-1 clade was only detected in farmed/wild Pacific salmon and not in farmed Atlantic Salmon. This observation, along with the occurrence of identical PRV-1a genetic variants in wild and farmed fish, provides evidence for transfer between these groups in the Northeast Pacific. Our analysis of the Global dataset identified additional PRV-1 genetic structure in the North Atlantic and Chilean waters and the requirement for additional PRV-1 genomic sequencing from these areas to better understand these relationships. The high level of Global PRV-1 genetic homogeneity at the genome level and the prediction that both PRV-1a and PRV-1b are under strong negative/purifying selection, suggests that PRV-1 is at or near a fitness peak in most host populations. The majority of differences between PRV-1 genetic variants are synonymous mutations. Understanding the extent to which synonymous mutations determine the phenotypes of PRV-1 could help to explain why some genetically similar variants differ in their pathogenicity and virulence.

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