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Multiple Infiltration and Cross-Species Transmission of Foamy Viruses

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Multiple Infiltration and Cross-Species Transmission of Foamy Viruses bioRxiv preprint doi: https://doi.org/10.1101/2020.12.18.423569; this version posted December 20, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 1 Multiple infiltration and cross-species transmission of foamy viruses 2 across Paleozoic to Cenozoic era 1,† 1,2,† 1,2 1,* 3 Yicong Chen , Yu-Yi Zhang , Xiaoman Wei , Jie Cui 4 5 1 CAS Key Laboratory of Molecular Virology & Immunology, Institut Pasteur of 6 Shanghai, Center for Biosafety Mega-Science, Chinese Academy of Sciences, 7 Shanghai 200031, China 8 2 University of Chinese Academy of Sciences, Beijing 100049, China 9 10 †These authors contribute equal to this work. 11 ∗Correspondence: [email protected] 12 13 Running title: Complex evolution of amphibian foamy viruses 14 bioRxiv preprint doi: https://doi.org/10.1101/2020.12.18.423569; this version posted December 20, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 15 Abstract 16 Foamy viruses (FVs) are complex retroviruses that can infect humans and other 17 animals. In this study, by integrating transcriptomic and genomic data, we discovered 18 412 FVs from 6 lineages in amphibians, which significantly increased the known set 19 of FVs in amphibians. Among these lineages, salamander FVs maintained a 20 co-evolutionary pattern with their hosts that could be dated back to the Paleozoic era, 21 while, on the contrary, frog FVs were much more likely acquired from cross-species 22 (class level) transmission in the Cenozoic era. In addition, we found three distinct FV 23 lineages had integrated into the genome of a salamander. Unexpectedly, we identified 24 a potential exogenous form of FV circulated in caecilian, demonstrating the existence 25 of exogenous form of FV besides mammals. Our discovery of rare phenomena in 26 amphibian FVs has overturned our collective understanding of the macroevolution of 27 the complex retrovirus. 28 29 Importance 30 Foamy viruses (FVs) represent, more so than other viruses, the best model of 31 co-evolution between a virus and a host. This study represents so far, the largest 32 investigation of amphibian FVs and revealed 412 FVs of 6 distinct lineages from 33 three major orders of amphibians. Besides co-evolutionary pattern, cross-species and 34 repeated infection were also observed during evolution of amphibian FVs. 35 Remarkably, expressed FVs including a potential exogenous form were discovered, 36 suggesting live FVs could be underestimated in nature. These findings revealed the 37 multiple origin and complex evolution of amphibian FVs started from the Paleozoic 38 era. 39 40 Keywords: Foamy virus; Endogenous foamy virus; Expressed foamy virus; 41 Amphibian; Evolution; Cross-species transmission; Multiple origin; Repeated 42 infection 43 bioRxiv preprint doi: https://doi.org/10.1101/2020.12.18.423569; this version posted December 20, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 44 Introduction 45 Retroviruses (family Retroviridae) have great medical and economic significance, as 46 some are associated with severe infectious disease or are oncogenic(1-5). Retroviruses 47 are notable as they occasionally integrate into the germline of a host and become 48 endogenous retroviruses (ERVs), which can be vertically inherited(6, 7). ERVs 49 generated by simple retroviruses are widely distributed in vertebrates(8-17). However, 50 complex retroviruses, such as lenti-, foamy- and delta-retroviruses, have rarely 51 appeared as endogenous forms. 52 53 Foamy viruses (FVs) (subfamily Spumavirinae) are complex retroviruses that exhibit 54 typical co-divergence with their host, providing an ideal framework for understand the 55 long-term evolutionary relationship between viruses and vertebrate hosts(18-21). 56 Exogenous foamy viruses are prevalent in mammals, including primates(18, 22), 57 bovines(23, 24), equines(25), bats(26), and felines(27). Vertebrate genomic analysis 58 first identified endogenous foamy viruses (EFVs) in sloths(28), then they were found 59 in several primate genomes(29-31). The subsequent discovery of EFVs and EFV-like 60 elements in fish and amphibian genomes indicated that foamy viruses, along with 61 their vertebrate hosts, have ancient origins(32, 33). Recently, the discovery of four 62 novel reptile EFVs and two avian EFVs demonstrated that FVs can infect all five 63 major classes of vertebrates(34-37). 64 65 Although substantial number of EFVs had been found across the evolutionary history 66 of vertebrates(28, 30, 38), to date, only a few of them have been found in amphibians, 67 mainly in salamander(32). Most importantly, no potential exogenous foamy viruses 68 have been found outside of mammalian host(32, 37). In this study, by integrating 69 transcriptomic and genomic data, we found >400 FVs of 6 novel lineages of foamy 70 viruses, which significantly increased the set of known foamy viruses in amphibians. 71 Several expressed FVs were revealed, with potential exogenous foamy viruses 72 discovered. Our work also provides novel insight into the early evolution of foamy 73 viruses. 74 bioRxiv preprint doi: https://doi.org/10.1101/2020.12.18.423569; this version posted December 20, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 75 Results 76 Discovery and confirmation of foamy viral elements and expressed foamy viruses in 77 amphibians 78 We screen 19 amphibian genomes (Table S1) using a homologous-based stepwise 79 manner as described in the materials and methods section. This led to the discovery of 80 18 foamy-like ERVs in Spea multiplicate (Mexican spadefoot toad), 64 in Rhinatrema 81 bivittatum (two-lined caecilian), and 131 in Ambystoma mexicanum (axolotl) (Table 82 S2). The foamy-like elements in S. multiplicate showed high similarity with each 83 other. Such high similarity between copies has also been observed in foamy-like 84 elements in R. bivittatum. However, there were two distinct groups of foamy-like 85 ERVs in A. mexicanum that showed an average 64% identity with 99% coverage. 86 87 In order to discover any potential exogenous foamy viruses, we also searched all 88 available amphibian RNA-seq data in the transcriptome sequence assembly (TSA) 89 database. Notably, we also found 58 foamy-like RNA copies in Tylototriton 90 wenxianensis (Wenxian knobby newt), 131 in Taricha granulosa (Rough-skinned 91 Newt), and 10 in R. bivittatum. Homologous comparison with NviFLERV-1 showed 92 that all three groups of foamy-like viral copies harbored typical major coding regions, 93 i.e., GAG, POL and ENV, with an average similarity of 22%–76%. 94 95 To examine whether these viral elements belonged to the clade of foamy viruses, a 96 phylogenetic tree was inferred using the reverse transcriptase (RT) protein of 97 representative viruses from all of the genera of Retroviridae (Fig. 1 and Table S3). 98 Our RT phylogenetic tree revealed that novel viral elements found in amphibians were 99 grouped within the foamy virus clade (bootstrap value > 90), which confirmed that 100 they were indeed foamy viruses. In addition, these foamy-like viral elements could be 101 divided into three clades, where the viral elements found in different newts, including 102 previously identified NviFLERV, clustered together, while the viral elements found in 103 R. bivittatum and S.multiplicate both formed a monophyletic group, respectively. Also, 104 of note was that foamy-like ERVs in A. mexicanum divided into two clusters, bioRxiv preprint doi: https://doi.org/10.1101/2020.12.18.423569; this version posted December 20, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 105 indicating the existence of two lineages of EFVs in A. mexicanum. 106 107 Thus, in accordance with the nomenclature proposed for ERVs(39), the foamy-like 108 ERVs found in S. multiplicate and R. bivittatum were named ERVs-Spuma.n-Smu (n 109 = 1~18) and ERVs-Spuma.n-Rbi (n = 1~64), respectively. Additionally, two lineages 110 in A. mexicanum were designated as ERVs-Spuma.an-Ame (n = 1~104) and 111 ERVs-Spuma.bn-Ame (n = 1~18), respectively. Moreover, the expressed viral 112 elements found in T. wenxianensis, T. granulosa and R. bivittatum were then named 113 expressed NFVtwe.n (exNFVtwe) (n = 1~58), expressed NFVtgr.n (exNFVtgr) (n = 114 1~131) and expressed CFVrbi.n (exCFVrbi) (n = 1~10), respectively. 115 116 EFV and exFV genome characterization 117 14 ERVs-Spuma-Smu, 54 ERVs-Spuma-Rbi, 57 ERVs-Spuma.a-Ame and 15 118 ERVs-Spuma.b-Ame, which were long (> 5 kb in length) were retrieved from their 119 respective genomes, and they were used to construct a consensus sequences for each 120 EFV lineage (Fig. 2A and Data set S1). The consensus genomes of novel EFVs all 121 harbored long pairwise LTRs and exhibited typical foamy virus structure, containing 122 three major genes, GAG, POL, and ENV, and one (ERV-Spuma-Rbi) or two 123 (ERVs-Spuma-Smu, ERVs-Spuma.a-Ame and ERVs-Spuma.b-Ame) putative 124 accessory genes. It is noteworthy that these accessory genes all showed no similarity 125 to any known proteins. By searching against the Conserved Domain Database (CDD) 126 using CD-Search, we were able to identify two typical foamy virus conserved 127 domains in all four consensus EFVs: (1) the Gag_spuma super family domain 128 (cl26624)(40, 41) and the (2) Foamy_virus_ENV super family domain (cl04051)(38).
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