RNA-seq of HaHV-1-infected abalones reveals a common transcriptional signature of Malacoherpesviruses

Abstract

Haliotid herpesvirus-1 (HaHV-1) is the viral agent causative of abalone viral ganglioneuritis, a disease that has severely affected gastropod aquaculture. Although limited, the sequence similarity between HaHV-1 and Ostreid herpesvirus-1 supported the assignment of both viruses to Malacoherpesviridae, a Herpesvirales family distantly related with other viruses. In this study, we reported the first transcriptional data of HaHV-1, obtained from an experimental infection of Haliotis diversicolor supertexta. We also sequenced the genome draft of the Chinese HaHV-1 variant isolated in 2003 (HaHV-1-CN2003) by PacBio technology. Analysis of 13 million reads obtained from 3 RNA samples at 60 hours post injection (hpi) allowed the prediction of 51 new ORFs for a total of 117 viral genes and the identification of 207 variations from the reference genome, consisting in 135 Single Nucleotide Polymorphisms (SNPs) and 72 Insertions or Deletions (InDels). The pairing of genomic and transcriptomic data supported the identification of 60 additional SNPs, representing viral transcriptional variability and preferentially grouped in hotspots. The expression analysis of HaHV-1 ORFs revealed one putative secreted protein, two putative capsid proteins and a possible viral capsid protease as the most expressed genes and demonstrated highly synchronized viral expression patterns of the 3 infected animals at 60 hpi. Quantitative reverse transcription data of 37 viral genes supported the burst of viral transcription at 30 and 60 hpi during the 72 hours of the infection experiment, and allowed the distinction between early and late viral genes.

Dual Transcriptomic Analysis Reveals a Delayed Antiviral Response of Haliotis diversicolor supertexta against Haliotid Herpesvirus-1

“…Most of the HaHV-1 ORFs exhibited somewhat stable expression trends among the tested time points (64 genes) or a preferential expression at 60 hpi (45 genes). These results are in agreement with the expression profiles that we recently published based on 37 selected HaHV-1 ORFs [38]. Although in-vivo analysis prevents the possibility to have synchronous viral infections due to the variability within cells and animals, this analysis identified viral genes preferentially induced in the early infection and can be used for future comparisons with similar viruses.…”

“…To produce an expression profile of the HaHV-1 genes, the clean reads were mapped on the HaHV-1 genome (GenBank No. KU096999) with the recently improved annotation [38], applying 0.8 for both length and similarity mapping parameters (CLC Genomics, v.11, Qiagen, Hilden, Germany). The total number of mapped reads was used as a proxy of the HaHV-1 expression value for each of the annotated genes and compared between the 3 experimental groups.…”

A-to-I editing of Malacoherpesviridae RNAs supports the antiviral role of ADAR1 in mollusks

“…Virus name, variant acronym, reference paper and availability of DNA- and RNA-seq data are reported. The cases with paired RNA/DNA HT-data are underlinedVirus nameVariant IDReferenceHT-DNA dataHT-RNA dataOsHV-1Reference 2005(Davison et al, 2005) [10]NNFrance μvar(Burioli et al, 2017) [24]naNIreland μvar(Burioli et al, 2017) [24]naN Italy μvar (Abbadi et al, 2018) [77]YYOsHV-1-SB(Xia et al, 2015) [104]NYAVNV(Ren et al, 2013) [105]NNAbHV-1Victoria(Savin et al, 2010) [106]NNTaiwanKU09699.1NN AbHV-1-CN2003 (Bai et al, 2019) [78]YYY: sequencing carried out with HTS instruments and data available; N: non-HTS datasets (genomes obtained with Sanger technology or not used for RNA-seq experiments); na: HTS data not available…”

Immune Control of Herpesvirus Infection in Molluscs

“…However, subsequent sequencing analysis revealed that OsHV-1 was only distantly related to other vertebrate herpesviruses and therefore represented a novel class of this virus family [ 21 ]. Malacoherpesviridae currently contains only two herpesvirus species [ 23 , 24 ]: Ostreid herpesvirus (OsHV-1) and Haliotid herpesvirus (HaHV-1) that mainly infect oysters and abalone, respectively. HaHV-1 was first discovered during a mass mortality event in Haliotis diversicolor supertexta in Tawain in 2003, with a subsequent outbreak of a similar virus seen in Australia in 2005 in both the black and green lip abalone ( Haliotis rubra and Haliotis laevigata , respectively) [ 14 , 15 ].…”

“…OsHV-1 and its associated variants were first linked to events of mass mortality in the Pacific Oyster ( Crassostrea gigas ) in France from 1993 to 2008, but since then have also been associated with disease in other countries including Australia [ 12 , 16 , 33 , 37 ]. HaHV-1 on the other hand was first recorded in 2003 in Taiwan and later in 2005 in Australia [ 23 , 26 ], where both outbreaks were associated with an acute onset of disease and high mortality [ 15 , 26 ].…”