Abstract

BackgroundEndogenous viral elements play important roles in eukaryotic evolution by giving rise to genetic novelties. Herpesviruses are a large family of DNA viruses, most of which do not have the ability to endogenize into host genomes. Recently, we identified a novel type of endogenous herpesvirus, which we named “Teratorn”, from the medaka (Oryzias latipes) genome, in which the herpesvirus is fused with a piggyBac-like DNA transposon, forming a novel mobile element. Teratorn is a unique herpesvirus that retains its viral genes intact and has acquired the endogenized lifestyle by hijacking the transposon system. However, it is unclear how this novel element evolved in the teleost lineage and whether fusion of two mobile elements is a general phenomenon in vertebrates.ResultsHere we performed a comprehensive genomic survey searching for Teratorn-like viruses in publicly available genome data and found that they are widely distributed in teleosts, forming a clade within Alloherpesviridae. Importantly, at least half of the identified Teratorn-like viruses contain piggyBac-like transposase genes, suggesting the generality of the transposon-herpesvirus fusion in teleosts. Phylogenetic tree topologies between the piggyBac-like transposase gene and herpesvirus-like genes are nearly identical, supporting the idea of a long-term evolutionary relationship between them.ConclusionWe propose that piggyBac-like elements and Teratorn-like viruses have co-existed for a long time, and that fusion of the two mobile genetic elements occurred frequently in teleosts.

Highlights

  • Endogenous viral elements play important roles in eukaryotic evolution by giving rise to genetic novelties

  • For about half of these 22 species, we obtained multiple genomic loci by blast search of each herpesvirus-like gene, suggesting that Teratorn-like viruses are present in multiple copies in those species

  • Tblastn search using sequences of another distantly-related alloherpesvirus species, Cyprinid herpesvirus 3 (CyHV-3), did not yield any positive hits other than Teratorn-like viruses, suggesting that Teratorn-like viruses are the only herpesvirus integrated in teleost genomes

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Summary

Introduction

Endogenous viral elements play important roles in eukaryotic evolution by giving rise to genetic novelties. Teratorn is a unique herpesvirus that retains its viral genes intact and has acquired the endogenized lifestyle by hijacking the transposon system It is unclear how this novel element evolved in the teleost lineage and whether fusion of two mobile elements is a general phenomenon in vertebrates. Herpesviruses are double-stranded DNA viruses that infect a wide variety of animals, from vertebrates to invertebrates (e.g. molluscs) [3] They have relatively large genomes ranging from 124- to 295-kb in length [3, 4], and sometimes cause symptoms such as herpes zoster and lymphoma in mammals [5] and intestinal inflammation and epithelial necrosis in teleost fishes [3, 6, 7]. Most herpesvirus species reported to date establish episomal latency in the nucleus

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