Identification of diverse full-length endogenous betaretroviruses in megabats and microbats

Abstract

BackgroundBetaretroviruses infect a wide range of species including primates, rodents, ruminants, and marsupials. They exist in both endogenous and exogenous forms and are implicated in animal diseases such as lung cancer in sheep, and in human disease, with members of the human endogenous retrovirus-K (HERV-K) group of endogenous betaretroviruses (βERVs) associated with human cancers and autoimmune diseases. To improve our understanding of betaretroviruses in an evolutionarily distinct host species, we characterized βERVs present in the genomes and transcriptomes of mega- and microbats, which are an important reservoir of emerging viruses.ResultsA diverse range of full-length βERVs were discovered in mega- and microbat genomes and transcriptomes including the first identified intact endogenous retrovirus in a bat. Our analysis revealed that the genus Betaretrovirus can be divided into eight distinct sub-groups with evidence of cross-species transmission. Betaretroviruses are revealed to be a complex retrovirus group, within which one sub-group has evolved from complex to simple genomic organization through the acquisition of an env gene from the genus Gammaretrovirus. Molecular dating suggests that bats have contended with betaretroviral infections for over 30 million years.ConclusionsOur study reveals that a diverse range of betaretroviruses have circulated in bats for most of their evolutionary history, and cluster with extant betaretroviruses of divergent mammalian lineages suggesting that their distribution may be largely unrestricted by host species barriers. The presence of βERVs with the ability to transcribe active viral elements in a major animal reservoir for viral pathogens has potential implications for public health.

Endogenous viruses: Connecting recent and ancient viral evolution

“…Boreoeutherians, marsupials, and birds (Arnaud et al, 2008;Baba et al, 2011;Baillie and Wilkins, 2001;Baillie et al, 2004;Bolisetty et al, 2012;Ericsson et al, 2001;Gifford et al, 2005;Hayward et al, 2013;Herniou et al, 1998;Lavie et al, 2004;Mayer et al, 2013;; Van der Kuyl, 2011) VI/RT-RNA virus Retroviridae (Gammaretroviruses)…”

A Novel Recombinant Retrovirus in the Genomes of Modern Birds Combines Features of Avian and Mammalian Retroviruses

“…First, it is the only known class II/gammaretroviral recombinant in an avian genome. Other such recombinants have been described in mammals, including the exogenous and endogenous primate type D betaretroviruses (e.g., MPMV) (12, 29, 34), a recently described bat ERV (35), and endogenous intracisternal A particles (IAPs), which have recombined with gammaretroviral env, in the genomes of the shrew and guinea pig (36). The only previously characterized class II/gammaretroviral recombinants found outside mammals are two related ERVs of pythons (PyERV) (37).…”

A Novel Endogenous Betaretrovirus in the Common Vampire Bat (Desmodus rotundus) Suggests Multiple Independent Infection and Cross-Species Transmission Events

“…Recently described retroviruses in chiropterans are diverse, some potentially representing the oldest viral lineages in mammalian taxa (2)(3)(4)(5). However, retroviral characterization has been restricted to bat species distributed in Eurasia, Africa, and Australia (2,4,5).…”

“…Little is known about retroviruses in bats from the neotropics, and nothing is known about those in vampire bats. Endogenous retroviruses (ERVs) are present in the genomes of all vertebrates examined (2)(3)(4)(5)(6)(7)(8)(9)(10)(11)(12)(13). As different species may share ERV sequences, it is assumed that, in many cases, an exogenous retrovirus infected the common ancestor of multiple species and became fixed in the genome prior to species divergence (14)(15)(16).…”