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Abstract
This study reports and characterises two novel distinct lineages of foamy viruses (FVs) in the forms of endogenous retroviruses (ERVs). Several closely related elements were found in the genome of oriental stork (Ciconia boyciana) and other was found in the genome of spine-bellied sea snake (Hydrophis hardwickii), designated ERV-Spuma.N-Cbo (where 'N' runs from one to thirteen) and ERV-Spuma.1-Hha, respectively. This discovery of avian and serpentine endogenous FVs adds snakes, and perhaps more crucially, birds to the list of currently known hosts of FVs, in addition to mammals, reptiles, amphibians, and fish. This indicates that FVs are, or at least were, capable of infecting all major lineages of vertebrates. Moreover, together with other FVs, phylogenetic analyses showed that both of them are most closely related to mammalian FVs. Further examination revealed that reptilian FVs form a deep paraphyletic group that is basal to mammalian and avian FVs, suggesting that there were multiple ancient FV cross-class transmissions among their hosts. Evolutionary timescales of various FV lineages were estimated in this study, in particular, the timescales of reptilian FVs and that of the clade of mammalian, avian, and serpentine FVs. This was accomplished by using the recently established time-dependent rate phenomenon models, inferred using mainly the knowledge of the co-speciation history between FVs and mammals. It was found that the estimated timescales matched very well with those of reptiles. Combined with the observed phylogenetic patterns, these results suggested that FVs likely co-speciated with ancient reptilian animals, but later jumped to a protomammal and/or a bird, which ultimately gave rise to mammalian and avian FVs. These results contribute to our understanding of FV emergence, specifically the emergence of mammalian and avian FVs, and provide new insights into how FVs co-evolved with their non-mammalian vertebrate hosts in the distant past.
Highlights
Foamy viruses (FVs) are complex retroviruses, belonging to the subfamily Spumaretrovirinae, family Retroviridae
Combined with the observed phylogenetic patterns, these results suggested that foamy viruses (FVs) likely co-speciated with ancient reptilian animals, but later jumped to a protomammal and/or a bird, which gave rise to mammalian and avian FVs
By querying the National Center for Biotechnology Information (NCBI) database (Supplementary Table S1) using a series of BLAST searches (Camacho et al 2009) starting with a coelacanth endogenous FV (CoeEFV) Env protein query, thirteen FV-like endogenous retroviruses (ERVs) sequences were retrieved from the oriental stork genome (Ciconia boyciana; accession number: BDFF02000000)
Summary
Foamy viruses (FVs) are complex retroviruses, belonging to the subfamily Spumaretrovirinae, family Retroviridae. Past virus surveillance revealed that they are highly prevalent among mammals, capable of infecting from primates (Switzer et al 2005; Muniz et al 2015) to cats (Riggs et al 1969; Winkler et al 1997), cows (Malmquist, Van der Maaten, and Boothe 1969; Renshaw and Casey 1994), horses (Tobaly-Tapiero et al 2000), and bats (Wu et al 2012). Various efforts of animal genomic analyses led to the discoveries of additional FVs, but in the form of endogenous retroviruses (ERVs), adding xenarthrans (Katzourakis et al 2009), afrotherians (Katzourakis et al 2014), reptiles (Aiewsakun, Simmonds, and Katzourakis 2019; VC The Author(s) 2020. Wei et al 2019), amphibians (Aiewsakun and Katzourakis 2017), lobe-finned fish (Han and Worobey 2012), ray-finned fish (Llorens et al 2009; Schartl et al 2013; Ruboyianes and Worobey 2016; Aiewsakun and Katzourakis 2017), and cartilaginous fish (Han 2015; Aiewsakun and Katzourakis 2017) to the list of vertebrates that FVs can infect, or at least could infect in the past. The evidence for FV infection in birds is still lacking, which is the last major gap in the FV-host range
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