Abstract

Horizontal gene transfer from retroviruses to mammals is well documented and extensive, but is rare between unrelated viruses with distinct genome types. Three herpesviruses encode a gene with similarity to a retroviral superantigen gene (sag) of the unrelated mouse mammary tumour virus (MMTV). We uncover ancient retroviral sags in over 20 mammals to reconstruct their shared history with herpesviral sags, revealing that the acquisition is a convergent evolutionary event. A retrovirus circulating in South American primates over 10 million years ago was the source of sag in two monkey herpesviruses, and a different retrovirus was the source of sag in a Peruvian rodent herpesvirus. We further show through a timescaled phylogenetic analysis that a cross-species transmission of monkey herpesviruses occurred after the acquisition of sag. These results reveal that a diverse range of ancient sag-containing retroviruses independently donated sag twice from two separate lineages that are distinct from MMTV.

Highlights

  • Horizontal gene transfer from retroviruses to mammals is well documented and extensive, but is rare between unrelated viruses with distinct genome types

  • The trees show that at least two horizontal gene transfer (HGT) events occurred from different retroviral lineages that are both distinct from mammary tumour virus (MMTV), and we provide estimates for the timing of these events

  • While ORF12 is absent in Ateline Herpesvirus 3 (AtHV3), sequence similarity to Saimirine Herpesvirus 2 (SaHV2) at that locus is maintained, indicating that it was a shared gene in their ancestor that later degraded in AtHV3 (Fig. 1)

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Summary

Introduction

Horizontal gene transfer from retroviruses to mammals is well documented and extensive, but is rare between unrelated viruses with distinct genome types. We further show through a timescaled phylogenetic analysis that a cross-species transmission of monkey herpesviruses occurred after the acquisition of sag These results reveal that a diverse range of ancient sag-containing retroviruses independently donated sag twice from two separate lineages that are distinct from MMTV. Viruses of every genome type and replication strategy are known to occasionally integrate into the germline genome of their host and can thereafter be inherited along with the host gene repertoire[17,18,19] These endogenous retroviruses (ERVs) can eventually reach population fixation, and drift at the host neutral evolutionary rate. We aimed to characterize the relationship between endogenous retroviral sags, MMTV sag and herpesvirus sags, as well as the pattern of selective pressures involved in their respective evolutionary histories To tackle these goals, we collected ancient retroviral data by mining ERVs from mammalian genomes. We use these ERVs to reconstruct the history of this unique virulence gene, by synthesizing evidence from phylogenetics and bioinformatic techniques under an evolutionary framework

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