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Abstract
A recent study reported the discovery of an endogenous reptilian foamy virus (FV), termed ERV-Spuma-Spu, found in the genome of tuatara. Here, we report two novel reptilian foamy viruses also identified as endogenous FVs (EFVs) in the genomes of panther gecko (ERV-Spuma-Ppi) and Schlegel’s Japanese gecko (ERV-Spuma-Gja). Their presence indicates that FVs are capable of infecting reptiles in addition to mammals, amphibians, and fish. Numerous copies of full length ERV-Spuma-Spu elements were found in the tuatara genome littered with in-frame stop codons and transposable elements, suggesting that they are indeed endogenous and are not functional. ERV-Spuma-Ppi and ERV-Spuma-Gja, on the other hand, consist solely of a foamy virus-like env gene. Examination of host flanking sequences revealed that they are orthologous, and despite being more than 96 million years old, their env reading frames are fully coding competent with evidence for strong purifying selection to maintain expression and for them likely being transcriptionally active. These make them the oldest EFVs discovered thus far and the first documented EFVs that may have been co-opted for potential cellular functions. Phylogenetic analyses revealed a complex virus–host co-evolutionary history and cross-species transmission routes of ancient FVs.
Highlights
Foamy viruses (FV; the Spumaretrovirinae subfamily) are a unique subgroup of retroviruses comprising an independent lineage basal to all other exogenous retroviruses [1].foamy virus (FV) surveillance and the discovery of their endogenous retrovirus (ERV) counterparts revealed that the host range of FVs covers a wide range of vertebrates, including mammals [2,3], amphibians [4], lobe-finned fish [5], bony fish [4,6], and cartilaginous fish [4,7], considerably wider than those of other retrovirus groups
Towards the 3’ end of the env gene could be identified in all mammalian FVs but were absent from CoeEFV and ERV-Spuma-Spu
A concatenated nucleotide alignment of pol and env sequences of ERV-Spuma-Spu elements together with those of mammalian, amphibian, and lobe-finned fish FVs and endogenous FVs (EFVs) was checked for potential recombination events by Recombination Detection Program 4 (RDP4) [12]; gag sequences were not included, as they could not be aligned among these viruses
Summary
Foamy viruses (FV; the Spumaretrovirinae subfamily) are a unique subgroup of retroviruses (family Retroviridae) comprising an independent lineage basal to all other exogenous retroviruses [1]. A recent study reported the discovery of the first reptilian endogenous FV (EFV) in the tuatara genome, namely ERV-Spuma-Spu [8]. Evolutionary analyses together with other currently available FV and EFV sequences suggest that these reptile EFVs do not form a monophyletic clade and that they are significantly younger than their hosts. This in turn suggests that, in contrast to what was previously suggested, their ancestors likely originated from cross-species transmissions, where one gave rise to ERV-Spuma-Spu and the other gave rise to the two gecko EFVs. Our results improve our understanding of how FVs evolved and interacted with their hosts in the distant past
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