Cross-species transmission and differential fate of an endogenous retrovirus in three mammal lineages

Abstract

Endogenous retroviruses (ERVs) arise from retroviruses chromosomally integrated in the host germline. ERVs are common in vertebrate genomes and provide a valuable fossil record of past retroviral infections to investigate the biology and evolution of retroviruses over a deep time scale, including cross-species transmission events. Here we took advantage of a catalog of ERVs we recently produced for the bat Myotis lucifugus to seek evidence for infiltration of these retroviruses in other mammalian species (>100) currently represented in the genome sequence database. We provide multiple lines of evidence for the cross-ordinal transmission of a gammaretrovirus endogenized independently in the lineages of vespertilionid bats, felid cats and pangolin~13-25 million years ago. Following its initial introduction, the ERV amplified extensively in parallel in both bat and cat lineages, generating hundreds of species-specific insertions throughout evolution. However, despite being derived from the same viral species, phylogenetic and selection analyses suggest that the ERV experienced different amplification dynamics in the two mammalian lineages. In the cat lineage, the ERV appears to have expanded primarily by retrotransposition of a single proviral progenitor that lost infectious capacity shortly after endogenization. In the bat lineage, the ERV followed a more complex path of germline invasion characterized by both retrotransposition and multiple infection events. The results also suggest that some of the bat ERVs have maintained infectious capacity for extended period of time and may be still infectious today. This study provides one of the most rigorously documented cases of cross-ordinal transmission of a mammalian retrovirus. It also illustrates how the same retrovirus species has transitioned multiple times from an infectious pathogen to a genomic parasite (i.e. retrotransposon), yet experiencing different invasion dynamics in different mammalian hosts. Author SummaryThe cross-species transmission of viruses poses a continuous threat to public health. Bats are increasingly recognized as a major reservoir for zoonotic RNA viruses, including Data Availability Statement: All relevant data are within the paper and its Supporting Information files. Funding:The work is supported by grant R01-GM077582 from National Institutes of Health (http:// www.nih.gov/). XZ is also supported by University of Utah graduate research fellowship (https:// gradschool.utah.edu/). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.Competing Interests: The authors have declared that no competing interests exist.rabies, Ebola, and possibly MERS, but little is known about their capacity to harbor and transmit retroviruses. Here we investigated past incidents of cross-species transmission involving bat retroviruses, by screening for the presence of endogenous retroviruses (ERVs) previously identified in the genome of the little brown bat in more than 100 diverse ...

Discovery of an endogenous Deltaretrovirus in the genome of long-fingered bats (Chiroptera: Miniopteridae)

“…S4). This observation provides compelling evidence that multiple gene conversion events, a phenomenon that has previously been described in ERVs (19,20), have occurred between the 5′ and 3′ LTRs of individual proviruses. This fact is precluding the LTR-based approach of age estimation.…”

Widespread Occurrence and Diverse Origins of Polintoviruses Influence Lineage-specific Genome Dynamics in Stony Corals

“…The varying degree of expansion of these elements in different stony coral genomes and possible horizontal transfer between genus makes them a key player in the genome evolution of stony corals. Transfer of transposable elements across closely related lineages is not uncommon 63 . Consistent with our observations, an analysis from a very recent study by Jeong et al (2023) 64 found the horizontal transfer of polintoviruses across different nematode strains within the same species, and even inter-phylum transfer of these elements.…”