Abstract

In a previous study, a metatranscriptomics survey of RNA viruses in several important lower vertebrate host groups revealed huge viral diversity, transforming the understanding of the evolution of vertebrate-associated RNA virus groups. However, the diversity of the DNA and retro-transcribing viruses in these host groups was left uncharacterized. Given that RNA sequencing is capable of revealing viruses undergoing active transcription and replication, we collected previously generated datasets associated with lower vertebrate hosts, and searched them for DNA and retro-transcribing viruses. Our results revealed the complete genome, or “core gene sets”, of 18 vertebrate-associated DNA and retro-transcribing viruses in cartilaginous fishes, ray-finned fishes, and amphibians, many of which had high abundance levels, and some of which showed systemic infections in multiple organs, suggesting active transcription or acute infection within the host. Furthermore, these new findings recharacterized the evolutionary history in the families Hepadnaviridae, Papillomaviridae, and Alloherpesviridae, confirming long-term virus–host codivergence relationships for these virus groups. Collectively, our results revealed reliable and sufficient information within metatranscriptomics sequencing to characterize not only RNA viruses, but also DNA and retro-transcribing viruses, and therefore established a key methodology that will help us to understand the composition and evolution of the total “infectome” within a diverse range of vertebrate hosts.

Highlights

  • The development of metagenomics and next-generation sequencing technologies has revolutionized the way in which we discover and characterize viruses

  • We identified a single species of alloherpesvirus from two metatranscriptomics libraries associated with Chinese tiger frogs (Hoplobatrachus rugulosus)—HWWF and HWWGP—to which we temporarily assigned the species name ranid herpesvirus 4 (RHV4)

  • Ray-finned fishes and amphibians, we identified, based on metatranscriptomics data and transcriptomics data, a total of five complete genomes and seven partial genomes of hepadnaviruses that were highly divergent from the existing members of the hepadnavirus family previously detected in other vertebrate hosts (Supplementary Table S1)

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Summary

Introduction

The development of metagenomics and next-generation sequencing technologies has revolutionized the way in which we discover and characterize viruses. These methods provide an unbiased view of the virome within a host, expand our knowledge of viral diversity, and fill in the “gaps” between many higher virus taxa [1,2,3,4]. Among various metagenomic methods used for virus discovery, metatranscriptomics (i.e., total RNA sequencing) represents a simple but efficient approach that transforms our view of the genomic diversity of RNA viruses in a wide range of hosts [5,6,7], and expands our knowledge of the diversity of DNA viruses [8,9,10,11]. Metatranscriptomics can reveal genomic information from viruses that are often known for chronic and latent infections, such as herpesviruses and papillomaviruses [10,11], which highlights the capacity of RNA sequencing for the discovery of viruses other than those with RNA genomes

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