1887

Abstract

Reverse-transcribing retroviruses exist as horizontally transmitted infectious agents or vertically transmitted endogenous retroviruses (ERVs) resident in eukaryotic genomes, and they are phylogenetically related to the long terminal repeat (LTR) class of retrotransposons. ERVs and retrotransposons are often distinguished only by the presence or absence of a gene encoding the envelope glycoprotein (). Endogenous elements of the virus family include the insect-restricted genus of ERVs, for which some members possess , and the pan-eukaryotic genus that lacks an envelope glycoprotein gene. Here we report a novel Nematoda endogenous retrovirus (NERV) clade with core retroviral genes arranged uniquely as a continuous ORF. Reverse transcriptase sequences were phylogenetically related to metaviruses, but envelope glycoprotein sequences resembled those of the and RNA virus families, suggesting gene capture during host cell infection by an RNA virus. NERVs were monophyletic, restricted to the nematode subclass Chromadoria, and included additional ORFs for a small hypothetical protein or a large Upf1-like RNA-dependent AAA-ATPase/helicase indicative of viral transduction of a host gene. Provirus LTR identity, low copy number, ORF integrity and segregation of three loci in taken together with detection of NERV transcriptional activity, support potential infectivity of NERVs, along with their recent emergence and integration. Altogether, NERVs constitute a new and distinct lineage demonstrating retroviral evolution through sequential heterologous gene capture events.

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/content/journal/jgv/10.1099/jgv.0.001739
2022-05-12
2022-05-24
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References

  1. Ellefson JW, Gollihar J, Shroff R, Shivram H, Iyer VR et al. Synthetic evolutionary origin of a proofreading reverse transcriptase. Science 2016; 352:1590–1593 [View Article] [PubMed]
    [Google Scholar]
  2. Goodier JL, Kazazian HH. Retrotransposons revisited: the restraint and rehabilitation of parasites. Cell 2008; 135:23–35 [View Article] [PubMed]
    [Google Scholar]
  3. Krupovic M, Blomberg J, Coffin JM, Dasgupta I, Fan H et al. Ortervirales: new virus order unifying five families of reverse-transcribing viruses. J Virol 2018; 92:e00515-18 [View Article] [PubMed]
    [Google Scholar]
  4. Stewart L, Vogt VM. trans-acting viral protease is necessary and sufficient for activation of avian leukosis virus reverse transcriptase. J Virol 1991; 65:6218–6231 [View Article] [PubMed]
    [Google Scholar]
  5. Craven RC, Bennett RP, Wills JW. Role of the avian retroviral protease in the activation of reverse transcriptase during virion assembly. J Virol 1991; 65:6205–6217 [View Article] [PubMed]
    [Google Scholar]
  6. Bennett RP, Rhee S, Craven RC, Hunter E, Wills JW. Amino acids encoded downstream of gag are not required by Rous sarcoma virus protease during gag-mediated assembly. J Virol 1991; 65:272–280 [View Article] [PubMed]
    [Google Scholar]
  7. Jacks T, Townsley K, Varmus HE, Majors J. Two efficient ribosomal frameshifting events are required for synthesis of mouse mammary tumor virus gag-related polyproteins. Proc Natl Acad Sci U S A 1987; 84:4298–4302 [View Article] [PubMed]
    [Google Scholar]
  8. Moore R, Dixon M, Smith R, Peters G, Dickson C. Complete nucleotide sequence of a milk-transmitted mouse mammary tumor virus: two frameshift suppression events are required for translation of gag and pol. J Virol 1987; 61:480–490 [View Article] [PubMed]
    [Google Scholar]
  9. Jacks T. Translational suppression in gene expression in retroviruses and retrotransposons. Curr Top Microbiol Immunol 1990; 157:93–124 [View Article] [PubMed]
    [Google Scholar]
  10. Yu SF, Baldwin DN, Gwynn SR, Yendapalli S, Linial ML. Human foamy virus replication: a pathway distinct from that of retroviruses and hepadnaviruses. Science 1996; 271:1579–1582 [View Article] [PubMed]
    [Google Scholar]
  11. Rohrmann GF, Karplus PA. Relatedness of baculovirus and gypsy retrotransposon envelope proteins. BMC Evol Biol 2001; 1:1 [View Article] [PubMed]
    [Google Scholar]
  12. Bolinger C, Boris-Lawrie K. Mechanisms employed by retroviruses to exploit host factors for translational control of a complicated proteome. Retrovirology 2009; 6:8 [View Article] [PubMed]
    [Google Scholar]
  13. Armbruester V, Sauter M, Krautkraemer E, Meese E, Kleiman A et al. A novel gene from the human endogenous retrovirus K expressed in transformed cells. Clin Cancer Res 2002; 8:1800–1807 [PubMed]
    [Google Scholar]
  14. Magin C, Löwer R, Löwer J. cORF and RcRE, the Rev/Rex and RRE/RxRE homologues of the human endogenous retrovirus family HTDV/HERV-K. J Virol 1999; 73:9496–9507 [View Article] [PubMed]
    [Google Scholar]
  15. Temin HM. Reverse transcription in the eukaryotic genome: retroviruses, pararetroviruses, retrotransposons, and retrotranscripts. Mol Biol Evol 1985; 2:455–468 [View Article] [PubMed]
    [Google Scholar]
  16. Weiss RA. The discovery of endogenous retroviruses. Retrovirology 2006; 3:67 [View Article] [PubMed]
    [Google Scholar]
  17. Mager DL, Henthorn PS. Identification of a retrovirus-like repetitive element in human DNA. Proc Natl Acad Sci U S A 1984; 81:7510–7514 [View Article] [PubMed]
    [Google Scholar]
  18. Tarlinton RE, Meers J, Young PR. Retroviral invasion of the koala genome. Nature 2006; 442:79–81 [View Article] [PubMed]
    [Google Scholar]
  19. Arkhipova IR, Mazo AM, Cherkasova VA, Gorelova TV, Schuppe NG et al. The steps of reverse transcription of Drosophila mobile dispersed genetic elements and U3-R-U5 structure of their LTRs. Cell 1986; 44:555–563 [View Article] [PubMed]
    [Google Scholar]
  20. Dhar R, McClements WL, Enquist LW, Vande Woude GF. Nucleotide sequences of integrated Moloney sarcoma provirus long terminal repeats and their host and viral junctions. Proc Natl Acad Sci U S A 1980; 77:3937–3941 [View Article] [PubMed]
    [Google Scholar]
  21. Hayward A. Origin of the retroviruses: when, where, and how?. Curr Opin Virol 2017; 25:23–27 [View Article] [PubMed]
    [Google Scholar]
  22. Lee A, Nolan A, Watson J, Tristem M. Identification of an ancient endogenous retrovirus, predating the divergence of the placental mammals. Philos Trans R Soc Lond B Biol Sci 2013; 368:20120503 [View Article] [PubMed]
    [Google Scholar]
  23. Lander ES, Linton LM, Birren B, Nusbaum C, Zody MC et al. Initial sequencing and analysis of the human genome. Nature 2001; 409:860–921 [View Article] [PubMed]
    [Google Scholar]
  24. Boller K, Schönfeld K, Lischer S, Fischer N, Hoffmann A et al. Human endogenous retrovirus HERV-K113 is capable of producing intact viral particles. J Gen Virol 2008; 89:567–572 [View Article] [PubMed]
    [Google Scholar]
  25. Wang J, Han GZ. Frequent retroviral gene co-option during the evolution of vertebrates. Mol Biol Evol 2020; 37:3232–3242 [View Article] [PubMed]
    [Google Scholar]
  26. Wang Z, Qu L, Yao J, Yang X, Li G et al. An EAV-HP insertion in 5' Flanking region of SLCO1B3 causes blue eggshell in the chicken. PLoS Genet 2013; 9:e1003183 [View Article]
    [Google Scholar]
  27. Mi S, Lee X, Li X, Veldman GM, Finnerty H et al. Syncytin is a captive retroviral envelope protein involved in human placental morphogenesis. Nature 2000; 403:785–789 [View Article] [PubMed]
    [Google Scholar]
  28. Pastuzyn ED, Day CE, Kearns RB, Kyrke-Smith M, Taibi AV et al. The neuronal gene arc encodes a repurposed retrotransposon gag protein that mediates intercellular RNA transfer. Cell 2018; 172:275–288 [View Article] [PubMed]
    [Google Scholar]
  29. C. elegans Sequencing Consortium Genome sequence of the nematode C. elegans: a platform for investigating biology. Science 1998; 282:2012–2018 [View Article] [PubMed]
    [Google Scholar]
  30. Bowen NJ, McDonald JF. Genomic analysis of Caenorhabditis elegans reveals ancient families of retroviral-like elements. Genome Res 1999; 9:924–935 [View Article] [PubMed]
    [Google Scholar]
  31. Britten RJ. Active gypsy/Ty3 retrotransposons or retroviruses in Caenorhabditis elegans. Proc Natl Acad Sci U S A 1995; 92:599–601 [View Article] [PubMed]
    [Google Scholar]
  32. Llorens C, Soriano B, Krupovic M, Ictv Report C. ICTV virus taxonomy profile: metaviridae. J Gen Virol 2020; 101:1131–1132 [View Article]
    [Google Scholar]
  33. Soriano B, Krupovic M, Llorens C. ICTV virus taxonomy profile: belpaoviridae 2021. J Gen Virol 2021; 102: [View Article]
    [Google Scholar]
  34. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol 1990; 215:403–410 [View Article] [PubMed]
    [Google Scholar]
  35. Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K et al. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 2011; 7:539 [View Article]
    [Google Scholar]
  36. Gouy M, Guindon S, Gascuel O. SeaView version 4: A multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol 2010; 27:221–224 [View Article]
    [Google Scholar]
  37. Kelley LA, Mezulis S, Yates CM, Wass MN, Sternberg MJ. The phyre2 web portal for protein modeling, prediction and analysis. Nat Protoc 2015; 10:845–858 [View Article]
    [Google Scholar]
  38. Smythe AB, Holovachov O, Kocot KM. Improved phylogenomic sampling of free-living nematodes enhances resolution of higher-level nematode phylogeny. BMC Evol Biol 2019; 19:121 [View Article] [PubMed]
    [Google Scholar]
  39. Hussey RS, Barker K. A comparison of methods of collecting inocula of Meloidogyne spp., including A new technique. Plant Disease Reporter 1973; 57:1025–1028
    [Google Scholar]
  40. Doyle JJ, Doyle JL. A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochemical Bulletin 1987; 19:11–15
    [Google Scholar]
  41. Wicker T, Sabot F, Hua-Van A, Bennetzen JL, Capy P et al. A unified classification system for eukaryotic transposable elements. Nat Rev Genet 2007; 8:973–982 [View Article] [PubMed]
    [Google Scholar]
  42. McClure MA, Johnson MS, Feng DF, Doolittle RF. Sequence comparisons of retroviral proteins: relative rates of change and general phylogeny. Proc Natl Acad Sci U S A 1988; 85:2469–2473 [View Article] [PubMed]
    [Google Scholar]
  43. Malik HS, Henikoff S, Eickbush TH. Poised for contagion: evolutionary origins of the infectious abilities of invertebrate retroviruses. Genome Res 2000; 10:1307–1318 [View Article] [PubMed]
    [Google Scholar]
  44. Snapp EL, McCaul N, Quandte M, Cabartova Z, Bontjer I et al. Structure and topology around the cleavage site regulate post-translational cleavage of the HIV-1 gp160 signal peptide. Elife 2017; 6:e26067 [View Article] [PubMed]
    [Google Scholar]
  45. Rein A. Across the hall from pioneers. Viruses 2021; 13:491 [View Article] [PubMed]
    [Google Scholar]
  46. Belshaw R, Pereira V, Katzourakis A, Talbot G, Paces J et al. Long-term reinfection of the human genome by endogenous retroviruses. Proc Natl Acad Sci U S A 2004; 101:4894–4899 [View Article] [PubMed]
    [Google Scholar]
  47. Belshaw R, Katzourakis A, Paces J, Burt A, Tristem M. High copy number in human endogenous retrovirus families is associated with copying mechanisms in addition to reinfection. Mol Biol Evol 2005; 22:814–817 [View Article] [PubMed]
    [Google Scholar]
  48. Bodem J, Löchelt M, Winkler I, Flower RP, Delius H et al. Characterization of the spliced pol transcript of feline foamy virus: the splice acceptor site of the pol transcript is located in gag of foamy viruses. J Virol 1996; 70:9024–9027 [View Article] [PubMed]
    [Google Scholar]
  49. Jordan I, Enssle J, Güttler E, Mauer B, Rethwilm A. Expression of human foamy virus reverse transcriptase involves a spliced pol mRNA. Virology 1996; 224:314–319 [View Article] [PubMed]
    [Google Scholar]
  50. Enssle J, Jordan I, Mauer B, Rethwilm A. Foamy virus reverse transcriptase is expressed independently from the Gag protein. Proc Natl Acad Sci U S A 1996; 93:4137–4141 [View Article] [PubMed]
    [Google Scholar]
  51. Stehelin D, Varmus HE, Bishop JM, Vogt PK. DNA related to the transforming gene(s) of avian sarcoma viruses is present in normal avian DNA. Nature 1976; 260:170–173 [View Article] [PubMed]
    [Google Scholar]
  52. Goodrich DW, Duesberg PH. Retroviral transduction of oncogenic sequences involves viral DNA instead of RNA. Proc Natl Acad Sci U S A 1988; 85:3733–3737 [View Article] [PubMed]
    [Google Scholar]
  53. Swanstrom R, Parker RC, Varmus HE, Bishop JM. Transduction of a cellular oncogene: the genesis of Rous sarcoma virus. Proc Natl Acad Sci U S A 1983; 80:2519–2523 [View Article] [PubMed]
    [Google Scholar]
  54. Stuhlmann H, Dieckmann M, Berg P. Transduction of cellular neo mRNA by retrovirus-mediated recombination. J Virol 1990; 64:5783–5796 [View Article] [PubMed]
    [Google Scholar]
  55. Herman SA, Coffin JM. Efficient packaging of readthrough RNA in ALV: implications for oncogene transduction. Science 1987; 236:845–848 [View Article] [PubMed]
    [Google Scholar]
  56. Raines MA, Maihle NJ, Moscovici C, Crittenden L, Kung HJ. Mechanism of C-erbB transduction: newly released transducing viruses retain poly(A) tracts of erbB transcripts and encode C-terminally intact erbB proteins. J Virol 1988; 62:2437–2443 [View Article] [PubMed]
    [Google Scholar]
  57. Coffin JM. Genes responsible for transformation by avian RNA tumor viruses. Cancer Res 1976; 36:4282–4288 [PubMed]
    [Google Scholar]
  58. Ajamian L, Abrahamyan L, Milev M, Ivanov PV, Kulozik AE et al. Unexpected roles for UPF1 in HIV-1 RNA metabolism and translation. RNA 2008; 14:914–927 [View Article] [PubMed]
    [Google Scholar]
  59. Lykke-Andersen S, Jensen TH. Nonsense-mediated mRNA decay: an intricate machinery that shapes transcriptomes. Nat Rev Mol Cell Biol 2015; 16:665–677 [View Article] [PubMed]
    [Google Scholar]
  60. Ajamian L, Abel K, Rao S, Vyboh K, García-de-Gracia F et al. HIV-1 Recruits UPF1 but excludes UPF2 to promote nucleocytoplasmic export of the genomic RNA. Biomolecules 2015; 5:2808–2839 [View Article] [PubMed]
    [Google Scholar]
  61. Miller DW, Miller LK. A virus mutant with an insertion of copia-like transposable element. Nature 1982; 299:562–564 [View Article] [PubMed]
    [Google Scholar]
  62. Linial M. Creation of a processed pseudogene by retroviral infection. Cell 1987; 49:93–102 [View Article] [PubMed]
    [Google Scholar]
  63. Oz-Gleenberg I, Herschhorn A, Hizi A. Reverse transcriptases can clamp together nucleic acids strands with two complementary bases at their 3’-termini for initiating DNA synthesis. Nucleic Acids Res 2011; 39:1042–1053 [View Article] [PubMed]
    [Google Scholar]
  64. Cotton JA, Steinbiss S, Yokoi T, Tsai IJ, Kikuchi T. An expressed, endogenous Nodavirus-like element captured by a retrotransposon in the genome of the plant parasitic nematode Bursaphelenchus xylophilus. Sci Rep 2016; 6:39749 [View Article] [PubMed]
    [Google Scholar]
  65. Love DN, Weiss RA. Pseudotypes of vesicular stomatitis virus determined by exogenous and endogenous avian RNA tumor viruses. Virology 1974; 57:271–278 [View Article] [PubMed]
    [Google Scholar]
  66. Weiss RA, Wong AL. Phenotypic mixing between avian and mammalian RNA tumor viruses: I. Envelope pseudotypes of Rous sarcoma virus. Virology 1977; 76:826–834 [View Article] [PubMed]
    [Google Scholar]
  67. Dietzgen RG, Ghedin E, Jiāng D, Kuhn JH, Song T et al. ICTV virus taxonomy profile: nyamiviridae. J Gen Virol 2017; 98:2914–2915 [View Article] [PubMed]
    [Google Scholar]
  68. Hagen J, Sarkies P, Selkirk ME. Lentiviral transduction facilitates RNA interference in the nematode parasite Nippostrongylus brasiliensis. PLoS Pathog 2021; 17:e1009286 [View Article] [PubMed]
    [Google Scholar]
  69. Belyi VA, Levine AJ, Skalka AM. Unexpected inheritance: multiple integrations of ancient bornavirus and ebolavirus/marburgvirus sequences in vertebrate genomes. PLoS Pathog 2010; 6:e1001030 [View Article] [PubMed]
    [Google Scholar]
  70. Thézé J, Leclercq S, Moumen B, Cordaux R, Gilbert C. Remarkable diversity of endogenous viruses in a crustacean genome. Genome Biol Evol 2014; 6:2129–2140 [View Article] [PubMed]
    [Google Scholar]
  71. Álvarez-Ortega S, Brito JA, Subbotin SA. Multigene phylogeny of root-knot nematodes and molecular characterization of Meloidogyne nataliei Golden, Rose & Bird, 1981 (Nematoda: Tylenchida). Sci Rep 2019; 9:11788 [View Article]
    [Google Scholar]
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