Recombination Marks the Evolutionary Dynamics of a Recently Endogenized Retrovirus
Language English Country United States Media print
Document type Journal Article, Research Support, Non-U.S. Gov't, Research Support, U.S. Gov't, Non-P.H.S.
PubMed
34480565
PubMed Central
PMC8662619
DOI
10.1093/molbev/msab252
PII: 6364191
Knihovny.cz E-resources
- Keywords
- CrERV, endogenous retrovirus, genome diversity, insertional polymorphism, mule deer, recombination,
- MeSH
- Biological Evolution MeSH
- Endogenous Retroviruses * genetics MeSH
- Phylogeny MeSH
- Evolution, Molecular MeSH
- Recombination, Genetic MeSH
- Deer * genetics MeSH
- Animals MeSH
- Check Tag
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Research Support, U.S. Gov't, Non-P.H.S. MeSH
All vertebrate genomes have been colonized by retroviruses along their evolutionary trajectory. Although endogenous retroviruses (ERVs) can contribute important physiological functions to contemporary hosts, such benefits are attributed to long-term coevolution of ERV and host because germline infections are rare and expansion is slow, and because the host effectively silences them. The genomes of several outbred species including mule deer (Odocoileus hemionus) are currently being colonized by ERVs, which provides an opportunity to study ERV dynamics at a time when few are fixed. We previously established the locus-specific distribution of cervid ERV (CrERV) in populations of mule deer. In this study, we determine the molecular evolutionary processes acting on CrERV at each locus in the context of phylogenetic origin, genome location, and population prevalence. A mule deer genome was de novo assembled from short- and long-insert mate pair reads and CrERV sequence generated at each locus. We report that CrERV composition and diversity have recently measurably increased by horizontal acquisition of a new retrovirus lineage. This new lineage has further expanded CrERV burden and CrERV genomic diversity by activating and recombining with existing CrERV. Resulting interlineage recombinants then endogenize and subsequently expand. CrERV loci are significantly closer to genes than expected if integration were random and gene proximity might explain the recent expansion of one recombinant CrERV lineage. Thus, in mule deer, retroviral colonization is a dynamic period in the molecular evolution of CrERV that also provides a burst of genomic diversity to the host population.
Department of Biology The Pennsylvania State University University Park PA USA
Institute of Molecular Genetics Academy of Sciences of the Czech Republic Prague Czech Republic
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Ali L, Rizvi T, Mustafa F.. 2016. Cross- and co-packaging of retroviral RNAs and their consequences. Viruses 8:276. PubMed PMC
Anai Y, Ochi H, Watanabe S, Nakagawa S, Kawamura M, Gojobori T, Nishigaki K.. 2012. Infectious endogenous retroviruses in cats and emergence of recombinant viruses. J Virol. 86(16):8634–8644. PubMed PMC
Antony JM, DesLauriers AM, Bhat RK, Ellestad KK, Power C.. 2011. Human endogenous retroviruses and multiple sclerosis: innocent bystanders or disease determinants? Biochim Biophys Acta. 1812(2):162–176. PubMed PMC
Arnaud F, Caporale M, Varela M, Biek R, Chessa B, Alberti A, Golder M, Mura M, Zhang Y, Yu L, et al.2007. A paradigm for virus–host coevolution: sequential counter-adaptations between endogenous and exogenous retroviruses. PLoS Pathog. 3(11):e170. PubMed PMC
Bamunusinghe D, Naghashfar Z, Buckler-White A, Plishka R, Baliji S, Liu Q, Kassner J, Oler AJ, Hartley J, Kozak CA.. 2016. Sequence diversity, intersubgroup relationships, and origins of the mouse leukemia gammaretroviruses of laboratory and wild mice. J Virol. 90(8):4186–4198. PubMed PMC
Bao L, Elleder D, Malhotra R, DeGiorgio M, Maravegias T, Horvath L, Carrel L, Gillin C, Hron T, Fábryová H, et al.2014. Computational and statistical analyses of insertional polymorphic endogenous retroviruses in a non-model organism. Computation 2(4):221–245.
Belshaw R, Dawson ALA, Woolven-Allen J, Redding J, Burt A, Tristem M.. 2005. Genomewide screening reveals high levels of insertional polymorphism in the human endogenous retrovirus family HERV-K(HML2): implications for present-day activity. J Virol. 79(19):12507–12514. PubMed PMC
Belshaw R, Katzourakis A, Paces J, Burt A, Tristem M.. 2005. High copy number in human endogenous retrovirus families is associated with copying mechanisms in addition to reinfection. Mol Biol Evol. 22(4):814–817. PubMed
Belshaw R, Pereira V, Katzourakis A, Talbot G, Paces J, Burt A, Tristem M.. 2004. Long-term reinfection of the human genome by endogenous retroviruses. Proc Natl Acad Sci U S A. 101(14):4894–4899. PubMed PMC
Belshaw R, Watson J, Katzourakis A, Howe A, Woolven-Allen J, Burt A, Tristem M.. 2007. Rate of recombinational deletion among human endogenous retroviruses. J Virol. 81(17):9437–9442. PubMed PMC
Bénit L, De Parseval N, Casella JF, Callebaut I, Cordonnier A, Heidmann T.. 1997. Cloning of a new murine endogenous retrovirus, MuERV-L, with strong similarity to the human HERV-L element and with a gag coding sequence closely related to the Fv1 restriction gene. J Virol. 71(7):5652–5657. PubMed PMC
Benit L, Dessen P, Heidmann T.. 2001. Identification, phylogeny, and evolution of retroviral elements based on their envelope genes. J Virol. 75(23):11709–11719. PubMed PMC
Bininda-Emonds ORP, Cardillo M, Jones KE, MacPhee RDE, Beck RMD, Grenyer R, Price SA, Vos RA, Gittleman JL, Purvis A.. 2007. The delayed rise of present-day mammals. Nature 446(7135):507–512. PubMed
Blanco-Melo D, Gifford RJ, Bieniasz PD.. 2017. Co-option of an endogenous retrovirus envelope for host defense in hominid ancestors. Elife 6:e22519. PubMed PMC
Boeke JD, Stoye JP.. 1997. Retrotransposons, endogenous retroviruses, and the evolution of retroelements. In: Coffin JM, Hughes SH, Varmus HE, editors. Retroviruses. New York: Cold Spring Harbor Laboratory Press. p. 343–435. PubMed
Bolinger C, Boris-Lawrie K.. 2009. Mechanisms employed by retroviruses to exploit host factors for translational control of a complicated proteome. Retrovirology 6:8. PubMed PMC
Bouckaert R, Heled J, Kühnert D, Vaughan T, Wu C-H, Xie D, Suchard MA, Rambaut A, Drummond AJ.. 2014. BEAST 2: a software platform for Bayesian evolutionary analysis. PLoS Comput Biol. 10(4):e1003537. PubMed PMC
Bruen TC, Philippe H, Bryant D.. 2006. A simple and robust statistical test for detecting the presence of recombination. Genetics 172(4):2665–2681. PubMed PMC
Bruno M, Mahgoub M, Macfarlan TS.. 2019. The arms race between KRAB–Zinc finger proteins and endogenous retroelements and its impact on mammals. Annu Rev Genet. 53:393–416. PubMed
Campbell IM, Gambin T, Dittwald P, Beck CR, Shuvarikov A, Hixson P, Patel A, Gambin A, Shaw CA, Rosenfeld JA, et al.2014. Human endogenous retroviral elements promote genome instability via non-allelic homologous recombination. BMC Biol. 12:74. PubMed PMC
Cantarel BL, Korf I, Robb SMC, Parra G, Ross E, Moore B, Holt C, Sánchez Alvarado A, Yandell M.. 2008. MAKER: an easy-to-use annotation pipeline designed for emerging model organism genomes. Genome Res. 18(1):188–196. PubMed PMC
Chaisson MJP, Huddleston J, Dennis MY, Sudmant PH, Malig M, Hormozdiari F, Antonacci F, Surti U, Sandstrom R, Boitano M, et al.2015. Resolving the complexity of the human genome using single-molecule sequencing. Nature 517(7536):608–611. PubMed PMC
Coffin JM. 1996. Retroviridae and their replication. In: Fields BN, Knipe DM, Howley PM, editors. Virology. New York: Raven Press. p. 1767–1848.
Cohen CJ, Lock WM, Mager DL.. 2009. Endogenous retroviral LTRs as promoters for human genes: a critical assessment. Gene 448(2):105–114. PubMed
Daugherty MD, Malik HS.. 2012. Rules of engagement: molecular insights from host-virus arms races. Annu Rev Genet. 46:677–700. PubMed
Desfarges S, Ciuffi A.. 2010. Retroviral integration site selection. Viruses 2(1):111–130. PubMed PMC
Dewannieux M, Dupressoir A, Harper F, Pierron G, Heidmann T.. 2004. Identification of autonomous IAP LTR retrotransposons mobile in mammalian cells. Nat Genet. 36(5):534–539. PubMed
Duggal NK, Emerman M.. 2012. Evolutionary conflicts between viruses and restriction factors shape immunity. Nat Rev Immunol. 12(10):687–695. PubMed PMC
Edgar RC. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32(5):1792–1797. PubMed PMC
Elleder D, Kim O, Padhi A, Bankert JG, Simeonov I, Schuster SC, Wittekindt NE, Motameny S, Poss M.. 2012. Polymorphic integrations of an endogenous gammaretrovirus in the mule deer genome. J Virol. 86(5):2787–2796. PubMed PMC
Evans LH, Alamgir ASM, Owens N, Weber N, Virtaneva K, Barbian K, Babar A, Malik F, Rosenke K.. 2009. Mobilization of endogenous retroviruses in mice after infection with an exogenous retrovirus. J Virol. 83(6):2429–2435. PubMed PMC
Fábryová H, Hron T, Kabíčková H, Poss M, Elleder D.. 2015. Induction and characterization of a replication competent cervid endogenous gammaretrovirus (CrERV) from mule deer cells. Virology 485:96–103. PubMed
Feschotte C, Gilbert C.. 2012. Endogenous viruses: insights into viral evolution and impact on host biology. Nat Rev Genet. 13(4):283–296. PubMed
Finnerty H, Mi S, Veldman GM, McCoy JM, LaVallie E, Edouard P, Tang X-Y, Howes S, Keith JC, Racie L, et al.2000. Syncytin is a captive retroviral envelope protein involved in human placental morphogenesis. Nature 403(6771):785–789. PubMed
Fu B, Ma H, Liu D.. 2019. Endogenous retroviruses function as gene expression regulatory elements during mammalian pre-implantation embryo development. Int J Mol Sci. 20:790. PubMed PMC
Gallagher DS, Derr JN, Womack JE.. 1994. Chromosome conservation among the advanced pecorans and determination of the primitive bovid karyotype. J Hered. 85(3):204–210. PubMed
Geis FK, Goff SP.. 2020. Silencing and transcriptional regulation of endogenous retroviruses: an overview. Viruses 12:884. PubMed PMC
Gifford RJ, Katzourakis A, De Ranter J, Magiorkinis G, Belshaw R.. 2012. Env-less endogenous retroviruses are genomic superspreaders. Proc Natl Acad Sci U S A. 109(19):7385–7390. PubMed PMC
Göke J, Ng HH.. 2016. CTRL + INSERT: retrotransposons and their contribution to regulation and innovation of the transcriptome. EMBO Rep. 17(8):1131–1144. PubMed PMC
Gregory TR. 2019. Animal genome size database. Available from: https://www.genomesize.com/result_species.php?id=4226. Accessed August 30, 2021.
Guindon S, Gascuel O.. 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol. 52(5):696–704. PubMed
Haig D. 2012. Retroviruses and the placenta. Curr Biol. 22(15):R609–R613. PubMed
Halo JV, Pendleton AL, Jarosz AS, Gifford RJ, Day ML, Kidd JM.. 2019. Origin and recent expansion of an endogenous gammaretroviral lineage in domestic and wild canids. Retrovirology 16(1):6. PubMed PMC
Hanafusa H. 1965. Analysis of the defectiveness of rous sarcoma virus III. Determining influence of a new helper virus on the host range and susceptibility to interference of RSV. Virology 25(2):248–255. PubMed
Harris RS. 2007. Improved pairwise alignment of genomic DNA [thesis]. State College, PA: The Pennsylvania State University.
Hoang ML, Tan FJ, Lai DC, Celniker SE, Hoskins RA, Dunham MJ, Zheng Y, Koshland D.. 2010. Competitive repair by naturally dispersed repetitive DNA during non-allelic homologous recombination. PLoS Genet. 6(12):e1001228. PubMed PMC
Holt C, Yandell M.. 2011. MAKER2: an annotation pipeline and genome-database management tool for second-generation genome projects. BMC Bioinformatics 12:491. PubMed PMC
Hughes JF, Coffin JM.. 2004. Human endogenous retrovirus K solo-LTR formation and insertional polymorphisms: implications for human and viral evolution. Proc Natl Acad Sci U S A. 101(6):1668–1672. PubMed PMC
Hunter DR, Bao L, Poss M.. 2017. Assignment of endogenous retrovirus integration sites using a mixture model. Ann Appl Stat. 11(2):751–770.
Hurst TP, Magiorkinis G.. 2017. Epigenetic control of human endogenous retrovirus expression: focus on regulation of long-terminal repeats (LTRs). Viruses 9:1–13. PubMed PMC
Isbel L, Whitelaw E.. 2012. Endogenous retroviruses in mammals: an emerging picture of how ERVs modify expression of adjacent genes. Bioessays 34(9):734–738. PubMed
Jern P, Coffin JM.. 2008. Effects of retroviruses on host genome function. Annu Rev Genet. 42:709–732. PubMed
Johnson WE. 2015. Endogenous retroviruses in the genomics era. Annu Rev Virol. 2(1):135–159. PubMed
Johnson WE, Coffin JM.. 1999. Constructing primate phylogenies from ancient retrovirus sequences. Proc Natl Acad Sci U S A. 96(18):10254–10260. PubMed PMC
Kamath PL, Poss M, Elleder D, Powell JH, Bao L, Cross PC.. 2014. The population history of endogenous retroviruses in mule deer (Odocoileus hemionus). J Hered. 105(2):173–187. PubMed PMC
Kawasaki J, Nishigaki K.. 2018. Tracking the continuous evolutionary processes of an endogenous retrovirus of the domestic cat: ERV-DC. Viruses 10:179. PubMed PMC
Kent WJ. 2002. BLAT – the BLAST-like alignment tool. Genome Res. 12(4):656–664. PubMed PMC
Kijima TE, Innan H.. 2010. On the estimation of the insertion time of LTR retrotransposable elements. Mol Biol Evol. 27(4):896–904. PubMed
Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg SL.. 2013. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol. 14(4):R36. PubMed PMC
Kim H-S. 2012. Genomic impact, chromosomal distribution and transcriptional regulation of HERV elements. Mol Cells. 33(6):539–544. PubMed PMC
Kim J, Larkin DM, Cai Q, Asan Zhang Y, Ge R-L, Auvil L, Capitanu B, Zhang G, Lewin HA, et al.2013. Reference-assisted chromosome assembly. Proc Natl Acad Sci U S A. 110:1785–1790. PubMed PMC
Kozak C. 2014. Origins of the endogenous and infectious laboratory mouse gammaretroviruses. Viruses 7(1):1–26. PubMed PMC
Kurth R, Bannert N.. 2010. Beneficial and detrimental effects of human endogenous retroviruses. Int J Cancer. 126(2):306–314. PubMed
Lavie L, Kitova M, Maldener E, Meese E, Mayer J.. 2005. CpG methylation directly regulates transcriptional activity of the human endogenous retrovirus family HERV-K(HML-2). J Virol. 79(2):876–883. PubMed PMC
Li H, Durbin R.. 2009. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25(14):1754–1760. PubMed PMC
Li W, Lee M, Henderson L, Tyagi R, Bachani M, Steiner J, Campanac E, Hoffman DA, von Geldern G, Johnson K, et al.2015. Human endogenous retrovirus-K contributes to motor neuron disease. Sci Transl Med. 7(307):307ra153. PubMed PMC
Li W, Lin L, Malhotra R, Yang L, Acharya R, Poss M.. 2019. A computational framework to assess genome-wide distribution of polymorphic human endogenous retrovirus-K In human populations. PLoS Comput Biol. 15:e1006564. PubMed PMC
Li W, Yang L, Harris RS, Lin L, Olson TL, Hamele CE, Feith DJ, Loughran TP, Poss M.. 2019. Retrovirus insertion site analysis of LGL leukemia patient genomes. BMC Med Genomics. 12(1):88. PubMed PMC
Löber U, Hobbs M, Dayaram A, Tsangaras K, Jones K, Alquezar-Planas DE, Ishida Y, Meers J, Mayer J, Quedenau C, et al.2018. Degradation and remobilization of endogenous retroviruses by recombination during the earliest stages of a germ-line invasion. Proc Natl Acad Sci U S A. 115(34):8609–8614. PubMed PMC
Löwer R, Löwer J, Kurth R.. 1996. The viruses in all of us: characteristics and biological significance of human endogenous retrovirus sequences. Proc Natl Acad Sci U S A. 93(11):5177–5184. PubMed PMC
Löytynoja A, Goldman N.. 2005. An algorithm for progressive multiple alignment of sequences with insertions. Proc Natl Acad Sci U S A. 102(30):10557–10562. PubMed PMC
Lu X, Sachs F, Ramsay L, Jacques P-É, Göke J, Bourque G, Ng H-H.. 2014. The retrovirus HERVH is a long noncoding RNA required for human embryonic stem cell identity. Nat Struct Mol Biol. 21(4):423–425. PubMed
Luo GX, Taylor J.. 1990. Template switching by reverse transcriptase during DNA synthesis. J Virol. 64(9):4321–4328. PubMed PMC
Luo R, Liu B, Xie Y, Li Z, Huang W, Yuan J, He G, Chen Y, Pan Q, Liu Y, et al.2012. SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler. Gigascience 1(1):18. PubMed PMC
Mager DL, Freeman JD.. 1995. HERV-H endogenous retroviruses: presence in the New World branch but amplification in the old world primate lineage. Virology 213(2):395–404. PubMed
Magiorkinis G, Belshaw R, Katzourakis A.. 2013. “There and back again”: revisiting the pathophysiological roles of human endogenous retroviruses in the post-genomic era. Philos Trans R Soc Lond B Biol Sci. 368(1626):20120504. PubMed PMC
Maksakova IA, Romanish MT, Gagnier L, Dunn CA, van de Lagemaat LN, Mager DL.. 2006. Retroviral elements and their hosts: insertional mutagenesis in the mouse germ line. PLoS Genet. 2(1):e2. PubMed PMC
Matsui T, Leung D, Miyashita H, Maksakova IA, Miyachi H, Kimura H, Tachibana M, Lorincz MC, Shinkai Y.. 2010. Proviral silencing in embryonic stem cells requires the histone methyltransferase ESET. Nature 464(7290):927–931. PubMed
Moyes D, Griffiths DJ, Venables PJ.. 2007. Insertional polymorphisms: a new lease of life for endogenous retroviruses in human disease. Trends Genet. 23(7):326–333. PubMed
Murin CD, Wilson IA, Ward AB.. 2019. Antibody responses to viral infections: a structural perspective across three different enveloped viruses. Nat Microbiol. 4(5):734–747. PubMed PMC
Posada D. 2008. jModelTest: phylogenetic model averaging. Mol Biol Evol. 25(7):1253–1256. PubMed
Rebollo R, Romanish MT, Mager DL.. 2012. Transposable elements: an abundant and natural source of regulatory sequences for host genes. Annu Rev Genet. 46:21–42. PubMed
Roca AL, O’Brien SP, Greenwood AD, Eiden MV, Ishida Y.. 2017. Transmission, evolution, and endogenization: lessons learned from recent retroviral invasions. Microbiol Mol Biol Rev. 82:1–41. PubMed PMC
Sofuku K, Honda T.. 2018. Influence of endogenous viral sequences on gene expression. In: gene expression and regulation in mammalian cells—transcription from general aspects. London: InTech.
Soriano P, Gridley T, Jaenisch R.. 1987. Retroviruses and insertional mutagenesis in mice: proviral integration at the Mov 34 locus leads to early embryonic death. Genes Dev. 1(4):366–375. PubMed
Stamatatos L, Morris L, Burton DR, Mascola JR.. 2009. Neutralizing antibodies generated during natural HIV-1 infection: good news for an HIV-1 vaccine? Nat Med. 15(8):866–870. PubMed
Stocking C, Kozak CA.. 2008. Murine endogenous retroviruses. Cell Mol Life Sci. 65(21):3383–3398. PubMed PMC
Stoye JP. 2012. Studies of endogenous retroviruses reveal a continuing evolutionary saga. Nat Rev Microbiol. 10(6):395–406. PubMed
Subramanian RP, Wildschutte JH, Russo C, Coffin JM.. 2011. Identification, characterization, and comparative genomic distribution of the HERV-K (HML-2) group of human endogenous retroviruses. Retrovirology 8:90. PubMed PMC
Suspène R, Sommer P, Henry M, Ferris S, Guétard D, Pochet S, Chester A, Navaratnam N, Wain-Hobson S, Vartanian JP.. 2004. APOBEC3G is a single-stranded DNA cytidine deaminase and functions independently of HIV reverse transcriptase. Nucleic Acids Res. 32(8):2421–2429. PubMed PMC
Sze A, Olagnier D, Lin R, van Grevenynghe J, Hiscott J.. 2013. SAMHD1 host restriction factor: a link with innate immune sensing of retrovirus infection. J Mol Biol. 425(24):4981–4994. PubMed
Trapnell C, Pachter L, Salzberg SL.. 2009. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25(9):1105–1111. PubMed PMC
Turner G, Barbulescu M, Su M, Jensen-Seaman MI, Kidd KK, Lenz J.. 2001. Insertional polymorphisms of full-length endogenous retroviruses in humans. Curr Biol. 11(19):1531–1535. PubMed
Vinogradov AE. 1998. Genome size and GC-percent in vertebrates as determined by flow cytometry: the triangular relationship. Cytometry 31(2):100–109. PubMed
Vogt VM., , . 1997. Retroviral virions and genomes. In: Coffin JM, Hughes SH, Varmus HE, editors. Retroviruses. New York: Cold Spring Harbor Laboratory Press. p. 27–70. PubMed
Weiss RA. 2006. The discovery of endogenous retroviruses. Retrovirology 3:67. PubMed PMC
Wildschutte JH, Ram D, Subramanian R, Stevens VL, Coffin JM.. 2014. The distribution of insertionally polymorphic endogenous retroviruses in breast cancer patients and cancer-free controls. Retrovirology 11:62. PubMed PMC
Wildschutte JH, Williams ZH, Montesion M, Subramanian RP, Kidd JM, Coffin JM.. 2016. Discovery of unfixed endogenous retrovirus insertions in diverse human populations. Proc Natl Acad Sci U S A. 113(16):E2326–E2334. PubMed PMC
Xue B, Sechi LA, Kelvin DJ.. 2020. Human endogenous retrovirus K (HML-2) in health and disease. Front Microbiol. 11:1690. PubMed PMC
Yao S, Sukonnik T, Kean T, Bharadwaj RR, Pasceri P, Ellis J.. 2004. Retrovirus silencing, variegation, extinction, and memory are controlled by a dynamic interplay of multiple epigenetic modifications. Mol Ther. 10(1):27–36. PubMed
Zheng Y-H, Jeang K-T, Tokunaga K.. 2012. Host restriction factors in retroviral infection: promises in virus-host interaction. Retrovirology 9:112. PubMed PMC
Zhuo X, Rho M, Feschotte C.. 2013. Genome-wide characterization of endogenous retroviruses in the bat Myotis lucifugus reveals recent and diverse infections. J Virol. 87(15):8493–8501. PubMed PMC