Abstract

BackgroundRanaviruses (family Iridoviridae, nucleocytoplasmic large DNA viruses) have been reported as promiscuous pathogens of cold-blooded vertebrates. Rana grylio virus (RGV, a ranavirus), from diseased frog Rana grylio with a genome of 105.79 kb and Andrias davidianus ranavirus (ADRV), from diseased Chinese giant salamander (CGS) with a genome of 106.73 kb, contains 99% homologous genes.ResultsTo uncover the differences in virus replication and host responses under interspecies infection, we analyzed transcriptomes of CGS challenged with RGV and ADRV in different time points (1d, 7d) for the first time. A total of 128,533 unigenes were obtained from 820,858,128 clean reads. Transcriptome analysis revealed stronger gene expression of RGV than ADRV at 1 d post infection (dpi), which was supported by infection in vitro. RGV replicated faster and had higher titers than ADRV in cultured CGS cell line. RT-qPCR revealed the RGV genes including the immediate early gene (RGV-89R) had higher expression level than that of ADRV at 1 dpi. It further verified the acute infection of RGV in interspecies infection.The number of differentially expressed genes and enriched pathways from RGV were lower than that from ADRV, which reflected the variant host responses at transcriptional level. No obvious changes of key components in pathway “Antigen processing and presentation” were detected for RGV at 1 dpi. Contrarily, ADRV infection down-regulated the expression levels of MHC I and CD8. The divergent host immune responses revealed the differences between interspecies and natural infection, which may resulted in different fates of the two viruses. Altogether, these results revealed the differences in transcriptome responses among ranavirus interspecies infection of amphibian and new insights in DNA virus-host interactions in interspecies infection.ConclusionThe DNA virus (RGV) not only expressed self-genes and replicated quickly after entry into host under interspecies infection, but also avoided the over-activation of host responses. The strategy could gain time for the survival of interspecies pathogen, and may provide opportunity for its adaptive evolution and interspecies transmission.

Highlights

  • Ranaviruses have been reported as promiscuous pathogens of cold-blooded vertebrates

  • Differences in expression of virus genes between interspecies and natural infection A total of 820,858,128 cleaned reads were obtained from 15 transcriptome libraries covering Rana grylio virus (RGV)-1d, RGV-7d, Andrias davidianus ranavirus (ADRV)-1d and ADRV7d groups

  • A portion of the cleaned reads were successfully mapped to the RGV (NCBI accession number: JQ654586) and ADRV (KC865735) genome

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Summary

Introduction

Ranaviruses (family Iridoviridae, nucleocytoplasmic large DNA viruses) have been reported as promiscuous pathogens of cold-blooded vertebrates. As a genus of the family Iridoviridae, viruses in Ranavirus have icosahedral capsids and double-stranded, nucleocytoplasmic large DNA genomes [13, 14]. These viruses have been reported as promiscuous pathogens of cold-blooded vertebrates [15] and have been isolated from different aquaculture animals including fish [16,17,18], amphibians [19,20,21], and reptiles [22, 23]. It has been reported that frog virus 3 (FV3, a ranavirus) or FV3-like ranavirus could infect heterologous species [26, 27]

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