Genomes of Anguillid Herpesvirus 1 Strains Reveal Evolutionary Disparities and Low Genetic Diversity in the Genus Cyprinivirus

Abstract

Anguillid herpesvirus 1 (AngHV-1) is a pathogen of eels and a member of the genus Cyprinivirus in the family Alloherpesviridae. We have compared the biological and genomic features of different AngHV-1 strains, focusing on their growth kinetics in vitro and genetic content, diversity, and recombination. Comparisons based on three core genes conserved among alloherpesviruses revealed that AngHV-1 exhibits a slower rate of change and less positive selection than other cypriniviruses. We propose that this may be linked to major differences in host species and corresponding epidemiological circumstances. Efforts to derive evolutionary rate estimates for cypriniviruses under various theoretical models were ultimately unrewarding. We highlight the potential value of future collaborative efforts towards generating short-term evolutionary rate estimates based on known sequence sampling dates. Finally, we revealed that there is significantly less genetic diversity in core gene sequences within cyprinivirus species clades compared to species in the family Herpesviridae. This suggests that cyprinivirus species may have undergone much more vigorous purifying selection post species clade divergence. We discuss whether this may be linked to biological and anthropogenic factors or to sampling bias, and we propose that the comparison of short-term evolutionary rates between species may provide further insights into these differences.

Virus-induced interference as a means for accelerating fitness-based selection of cyprinid herpesvirus 3 single-nucleotide variantsin vitroandin vivo

“…Our recent evidence supporting a general low degree of diversity among cyprinivirus species clades compared to species clades within the family Herpesviridae suggests that a high degree of purifying selection has occurred after species clade divergence (Donohoe et al, 2021). We speculated that this difference could be linked, at least in part, to fundamental differences in biology between members of the two distantly related virus families.…”

“…Compared to the family Herpesviridae there are relatively few studies regarding evolution within the family Alloherpesviridae (Aoki et al, 2007;Davison et al, 2013;Waltzek et al, 2009Waltzek et al, , 2005. Recently, we investigated the diversity of core gene sequences within species clades of the genus Cyprinivirus (referred to as cypriniviruses and comprising alloherpesviruses infecting cyprinids and eels) (Donohoe et al, 2021). This revealed significantly less genetic diversity within cyprinivirus species clades than within species in the family Herpesviridae, which may be linked, at least in part, to different environmental pressures.…”

Susceptibility and Permissivity of Zebrafish (Danio rerio) Larvae to Cypriniviruses

“…The AngHV-1 Luc-copGFP and the CyHV-2 Luc-copGFP recombinant strains both encode the same reporter genes consisting of the Luc2 cassette and a copepod ( Pontellina plumata ) GFP (copGFP) cassette linked by a T2A sequence, driven by a eukaryotic translation elongation factor 1 alpha (EF-1α) promoter. To generate these recombinants, the dual Luc2/copGFP cassette was inserted in the region between ORF32 and ORF33 in the AngHV-1 UK parental strain genome (GenBank accession MW580855.1) [ 40 ] (Delrez et al, unpublished data) and in the intergenic region between ORF64 and ORF66 in CyHV-2 YC-01 parental strain genome (GenBank accession no. MN593216.1) (He et al, unpublished data) using homologous recombination in eucaryotic cells, as described previously [ 50 ].…”

“…In addition to CyHV-3, the genus Cyprinivirus contains two other economically important viruses: anguillid herpesvirus 1 (AngHV-1) and cyprinid herpesvirus 2 (CyHV-2) [ 40 ]. AngHV-1 infects the European eel ( Anguilla anguilla ), Japanese eel ( Anguilla japonica ), and American eel ( Anguilla rostrata ) [ 41 ]; CyHV-2 also infects goldfish ( Carassius auratus ) and the closely related Prussian carp ( Carassius gibelio ) and crucian carp ( Carassius carassius ) [ 42 ].…”

A complete check-up of European eel after eight years of restocking in an upland river: Trends in growth, lipid content, sex ratio and health status

“…The high-energy requirement for spawning migration and the dysfunction of the swim bladder have an adverse effect on individuals with reduced lipid stores due to infection (Marohn et al, 2013). The AngHV-1 infection causes the following symptoms: lethargy; swimming near the surface; swimming in a circular motion; mottled skin; inflammation; haemorrhaging in the fins; throat, operculum, head, lower jaw, pectoral fin, tail and skin lesions; and necrosis within the kidney, gills and liver (Haenen et al, 2012;Armitage et al, 2014;McConville et al, 2018;Donohoe et al, 2021). Armitage et al (2014) reported dead eels measuring 50-90 cm (17-26 years old) due to AngHV-1 infection in two English still-water fisheries, but experimental infections did not produce eel mortality (see also Kobayashi and Miyazaki, 1996;Hangalapura et al, 2007).…”