Abstract
The family of double-stranded DNA (dsDNA) Malacoherpesviridae includes viruses able to infect marine mollusks and detrimental for worldwide aquaculture production. Due to fast-occurring mortality and a lack of permissive cell lines, the available data on the few known Malacoherpesviridae provide only partial support for the study of molecular virus features, life cycle, and evolutionary history. Following thorough data mining of bivalve and gastropod RNA-seq experiments, we used more than five million Malacoherpesviridae reads to improve the annotation of viral genomes and to characterize viral InDels, nucleotide stretches, and SNPs. Both genome and protein domain analyses confirmed the evolutionary diversification and gene uniqueness of known Malacoherpesviridae. However, the presence of Malacoherpesviridae-like sequences integrated within genomes of phylogenetically distant invertebrates indicates broad diffusion of these viruses and indicates the need for confirmatory investigations. The manifest co-occurrence of OsHV-1 genotype variants in single RNA-seq samples of Crassostrea gigas provide further support for the Malacoherpesviridae diversification. In addition to simple sequence motifs inter-punctuating viral ORFs, recombination-inducing sequences were found to be enriched in the OsHV-1 and AbHV1-AUS genomes. Finally, the highly correlated expression of most viral ORFs in multiple oyster samples is consistent with the burst of viral proteins during the lytic phase.
Highlights
The virus family of double-stranded DNA Malacoherpesviridae refers to only those Herpesvirales which affect mollusks, with the Haliotid herpesvirus, and bivalve Ostreid herpesvirus1 being highly similar virus variants and the only family members described so far (Davison et al, 2005; Savin et al, 2010)
This bias allows for the discovery of new viruses in almost every virome study, as recently reported for six new bivalve-associated RNA viruses (Rosani and Gerdol, 2016) and for RNA viruses associated with invertebrates (Shi et al, 2016)
We focused on the family of Malacoherpesviridae, a case study considering their enigmatic evolutionary origin and limited transcriptional/genomic data
Summary
The virus family of double-stranded DNA (dsDNA) Malacoherpesviridae refers to only those Herpesvirales which affect mollusks, with the Haliotid herpesvirus, and bivalve Ostreid herpesvirus being highly similar virus variants and the only family members described so far (Davison et al, 2005; Savin et al, 2010). Malacoherpesviridae are distantly related to other Herpesvirales families, namely alpha-, beta-, gamma-, and allo-herpesviridae (Davison et al, 2009; Iranzo et al, 2016). The considerable genome size of Herpesvirales (125–290 kb) supports complex transcriptional landscapes, including several coding (ORFs) and non-coding RNAs (ncRNAs) such as microRNAs (miRNAs). Modulation of latent vs lytic phases guarantees long-term survival and efficient propagation of Herpesvirales, viral genomes are exposed to mutational pressure during their latency state into the cell nucleus (Brown, 2014). In alpha- and gamma-herpesvirales, different recombination-initiating motifs can activate host genome integrity pathways like homologous recombination-dependent DNA repair (HR), a virus-protective strategy proposed as being crucial for Herpesvirales biology (Brown, 2017; Piekna-Przybylska et al, 2017).
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