Abstract
Advances in understanding over the last decade or so highlight the need for a reappraisal of the role of viruses in relation to the origins and evolution of cellular life, as well as in the homeostasis of the biosphere on which all of life depends. The relevant advances have, in particular, revealed an important contribution of viruses to the evolution of the placental mammals, while also contributing key roles to mammalian embryogenesis, genomic evolution, and physiology. Part of this reappraisal will include the origins of viruses, a redefinition of their quintessential nature, and a suggestion as to how we might view viruses in relation to the tree of life.
This is a preview of subscription content, log in via an institution.
Buying options
Tax calculation will be finalised at checkout
Purchases are for personal use only
Learn about institutional subscriptionsReferences
Aiewakun P, Katzourakis A (2017) Marine origin of retroviruses in the early Palaeozoic era. Nat Comm 8:13954. https://doi.org/10.1038/ncomms13954|www.nature.com/naturecommunications
Angly FE, Felts B, Breitbart M, Salamon P, Edwards RA et al (2006) The marine Viromes of four oceanic regions. PLoS Biol 4(11):2121–2131
Bannert N, Hofmann H, Block A, Hohn O (2018) HERVs new role in cancer: from accused perpetrators to cheerful protectors. Frontiers in Microbiol 9:178
Bansho Y, Ichihashi N, Kazuta Y, Matsuura T, Suzuki H, Yomo T (2012) Importance of parasite RNA species repression for prolonged translation-coupled RNA self-replication. Chem Biol 19:478–487
Battistuzzi FU, Feijao A, Hedges SB (2004) A genomic timescale of prokaryotic evolution: insights into the origin of methanogenesis, phototrophy, and the colonization of land. BMC Evol Biol 4:44. https://doi.org/10.1186/1471-2148-4-44
Bell PJL (2009) The viral eukaryogenesis hypothesis: a key role for viruses in the emergence of eukaryotes from a prokaryotic world environment. Ann NY Acad Sci 1178:91–105
Blaise S, de Parseval N, Bénit L, Heidmann T (2003) Genomewide screening for fusogenic human endogenous retrovirus envelopes identifies syncytin 2, a gene conserved on primate evolution. Proc Natl Acad Sci U S A 100:13013–13018
Blond J-L, Lavillette D, Cheynet V, Bouton O, Oriol G et al (2000) An envelope glycoprotein of the human endogenous retrovirus HERV-W is expressed in the human placenta and fuses cells expressing the type D mammalian retrovirus receptor. J Virol 74:3321–3329
Bolze P-A, Mommert M, Mallet F (2017) Contributions of syncytins and other endogenous retroviral envelopes to human placenta pathologies. Prog Mol Biol and Trans Sci 1877-1173:111–162. https://doi.org/10.1016/bs.pmbts.2016.005
Bosch E, Jobling MA (2003) Duplications of the AZFa region of the human Y chromosome are mediated by homologous recombination between HERVs and are compatible with male fertility. Hum Mol Genet 12:341–347
Bremermann HJ (1983) Parasites at the origin of life. J Math Biol 16:165–180
Buzdin A, Kovalskaya-Alexandrova E, Gogvadze E, Sverdlov E (2006) At least 50% of human-specific HERV-K (HML-2) long terminal repeats serve in vivo as active promoters for host nonrepetitive DNA transcription. J Virol 80:10752–10762
Chaikeeratisak V, Nguyen K, Khanna K, Brilot AF, Erb ML et al (2017) Assembly of a nucleus-like structure during viral replication in bacteria. Science 355:194–197
Chuong EB, Elde NC, Feschotte C (2016) Regulatory evolution of innate immunity through co-option of endogenous retroviruses. Science 351:1083–1087
Claverie JM, Ogata H (2009) Ten good reasons not to exclude viruses from the evolutionary picture. Nat Rev Microbiol 7(8):615. https://doi.org/10.1038/nrmicro2108-c3
Colizzi ES, Hogeweg P (2016) Parasites sustain and enhance RNA-like replicators through spatial self-organisation. PLoS Comput Biol 12(4):e1004902. https://doi.org/10.1371/journal.pcbi.1004902
Collier L, Oxford J (1993) Human Virology. Oxford University Press, Oxford
Cornelis G, Heidmann O, Bernard-Stoecklin S, Reynaud K, Véron G et al (2012) Ancestral capture of syncytin-Car1, a fusogenic endogenous retroviral envelope gene involved in placentation and conserved in Carnivora. Proc Natl Acad Sci U S A 109(7):E432–E441. https://doi.org/10.1073/pnas.1115346109
Cornelis G, Heidmann O, Degrelle SA, Vernochet C, Lavialle C et al (2013) Captured retroviral envelope syncytin gene associated with unique placental structure of higher ruminants. Proc Natl Acad Sci U S A 110(9):E828–E837. https://doi.org/10.1073/pnas.1215787110
Cornelis G, Vernochet C, Carradec Q, Souquere S, Mulot B et al (2015) Retroviral envelope gene captures and syncytin exaptation for placentation in marsupials. Proc Natl Acad Sci U S A 111(41):E4332–E4341. https://doi.org/10.1073/pnas.1417000112
Cornelis G, Vernochet C, Malicorne S, Souquere S, Tzika AC et al (2014) Retroviral envelope syncytin capture in an ancestrally diverged mammalian clade for placentation in the primitive Afrotherian tenrecs. Proc Natl Acad Sci U S A 111(41):E4332–E4341. www.pnas.org/cgi/doi/10.1073/pnas.1412268111
d’Herelle F (1926) The bacteriophage and its behaviour. Ballière, Tindall and Cox, London. Chapter V: 211. See also pp 326, 343 and 354
Dawkins R, Leelayuwat C, Gaudieri S, Tay G, Hui J et al (1999) Genomics of the major histocompatibility complex: haplotypes, duplication, retroviruses and disease. Immunol Rev 167:275–304
De Bary A (1879) Die Erscheinung der Symbiose. In: Vortrag auf der Versammlung der Naturforscher und Ärtze zu Cassel. Verlag von Karl J Trubner, Strasburg, pp 1–30
De La Torre JC, Holland JJ (1990) RNA virus quasispecies populations can suppress vastly superior mutant progeny. J Virol 64(12):6278–6281
Dodd MS, Papineau D, Grenne T, Slack JF, Rittner M et al (2017) Evidence for early life in Earth’s oldest hydrothermal vent precipitates. Nature 543:60–64
Doolittle WF (2000) Uprooting the tree of life. Sci Amer 282:90–95
Douglas A (1994) Symbiotic interactions. Oxford University Press, New York
Dupressoir AC, Vernochet O, Bawa Harper F, Pierron G et al (2009) Syncytin-a knockout mice demonstrate the critical role in placentation of fusogenic, endogenous retrovirus-derived, envelope gene. Proc Natl Acad Sci U S A 106(2):12127–12132
Durzyńska J, Goździcka-Jósefiak A (2015) Viruses and cells intertwined since the dawn of evolution. Virol J 12:169. https://doi.org/10.1186/s12985-015-0400-7
Eckardt NA (2006) Genetic and epigenetic regulation of embryogenesis. Plant Cell 18:781–784
Eigen M, Schuster P (1977) The Hypercycle. A principle of natural self-organisation. Part a: emergence of the Hypercycle. Naturwissenschaften 64:541–565
Eigen M, Schuster P (1978a) The Hypercycle. A principle of natural self-organisation. Part B: the abstract Hypercycle. Naturwissenschaften 65:7–41
Eigen M, Schuster P (1978b) The Hypercycle. A principle of natural self-organisation. Part C: the realistic Hypercycle. Naturwissenschaften 65:341–369
Eigen M, Schuster P (1979) The Hypercycle: a principle of natural self-organization. Springer ISBN 0-387-09293-5
Fei C, Atterby C, Edqvist P-H, Ponten F, Zhang WW et al (2014) Detection of the human endogenous retrovirus ERV3-encoded Env-protein in human tissues using antibody-based proteomics. J Roy Soc Med 107(1):22–29. https://doi.org/10.1177/0141076813509981
Fierz W (2017) Multiple sclerosis: an example of pathogenic viral interaction? Virol J 14:42–48. https://doi.org/10.1186/s12985-017-0719-3
Filée J, Forterre P, Laurent J (2003) The role played by viruses in the evolution of their hosts: a view based on informational protein phylogenies. Research in Virol 154:237–243
Fisher S (2010) Are RNA viruses vestiges of an RNA world? J Gen Philos Sci 41:121–141
Forterre P (2006) The origin of viruses and their possible roles in major evolutionary transitions. Virus Res 117:5–16
Forterre P (2013) The Great Virus Comeback (translated from the French). Biol Aujourdhui 207(3):153–168
Frank AB (1877) Über die biologischen Verhältnisse des Thallus eineger Krustenflechten. Beitrage zur Biologie der Pflanzen 2:123–200
Frank AB (1885) Über die auf Wurzelsymbiose beruhende Ernährung gewisser Bäume durch unterirdische Pilze. Berichte der Deutschen Botanischen Gesellschaft 3:128–145
Fuhrman JA (1999) Marine viruses and their biogeochemical and ecological effects. Nature 399:541–548
Glansdorf N, Xu Y, Labedan B (2008) The last universal common ancestor: emergence, constitution and genetic legacy of an elusive forerunner. Biol Direct 3:29. https://doi.org/10.1186/1745-6150-3-29
Gribaldo S, Brochier-Armanet C (2006) The origin and evolution of Archaea: a state of the art. Phil Trans Roy Soc B 361:1007–1022. https://doi.org/10.1098/rstb.2006.1841
Grow EJ, Flynn RA, Chavez SL, Bayless NL, Wossidlo M, Wesche DJ, Martin L, Ware CB, Blish CA, Chang HY, Pera RA, Wysocka J (2015a) Intrinsic retroviral reactivation in human preimplantation embryos and pluripotent cells. Nature 522:221–225
Grow EJ, Flynn RA, Chavez SL, Bayless NL, Wossidlo M et al (2015b) Intrinsic retroviral reactivation in human preimplantation embryos and pluripotent cells. Nature 522:221–225
Guo H, Zhu P, Yan L, Li R, Hu B et al (2014) The DNA methylation landscape of human early embryos. Nature 511:606–610
Hambly E, Suttle CA (2005) The virosphere, diversity, and genetic exchange within phage communities. Curr Opinion Microbiol 8:444–450
Hedge NR, Maddur MS, Kaveri SV, Bayry J (2009) Reasons to include viruses in the tree of life. Nat Rev Microbiol 7(8):615. https://doi.org/10.1038/nrmicro2108-c1
Holland JJ, De La Torre JC, Steinhauer DA (1992) RNA virus populations as quasispecies. Curr Top Microbiol Immunol 176:1–20
Holmes EC (2011) What does virus evolution tell us about virus origins? J Virol 85(11):5427–5251
Hug LA, Baker BJ, Anantharaman K, Brown CT, Probst AJ et al (2016) A new view of the tree of life. Nat Microbiol 1:16048. https://doi.org/10.1038/nmiccrobiol.2016.48
Hughes JF, Coffin JM (2001) Evidence for genomic rearrangements mediated by human endogenous retroviruses during primate evolution. Nat Genet 29:487–489
Jordan K, Rogozin IB, Glazko GV, Koonin EV (2003) Origin of a substantial fraction of human regulatory sequences from transposable elements. Trends Genet 19(2):68–72
Kapitonov VV, Jurka J (1999) The long terminal repeat of an endogenous retrovirus induces alternative splicing and encodes an additional carboxy-terminal sequence in the human leptin receptor. J Mol Evol 48:248–251
Kazazian HH, Wong C, Youssoufian H, Scott AF, Phillips DG, Antonarakis SE (1988) Haemophilia a resulting from de novo insertion of L1 sequences represents a novel mechanism for mutation in man. Nature 332:164–166
Kim H-S, Yi J-M, Hirai H, Huh J-W, Jeong M-S et al (2006) Human endogenous retrovirus (HERV)-R in primates: chromosomal location, gene expression, and evolution. Gene 370:34–42. https://doi.org/10.1016/j.gene.2005.11.008
Koonin EV (2001) The logic of chance: the nature and origin of biological evolution. F.T. Press Science, Upper Saddle River, NJ
Koonin EV (2011) The logic of chance: the nature and origin of biological evolution. F.T. Press Science, New Jersey
Koonin EV, Dolja VV (2013) A virocentric perspective on the evolution of life. Curr Opin Virol 3(5):546–557
Koonin EV, Dolja VV, Krupovic M (2015) Origins and evolution of viruses of eukaryotes: the ultimate modularity. Virol 479-480:2–25
Koonin EV, Senkevich TG, Dolja VV (2006) The ancient virus world and the evolution of cells. Biol Direct 1:29. https://doi.org/10.1186/1745-6150-1-29
Koonin EV, Senkevich TG, Dolja VV (2009) Compelling reasons why viruses are relevant for the origin of cells. Nat Rev Microbiol 7(8):615. https://doi.org/10.1038/nrmicro2108-c5
Krupovic M, Dutilh BE, Adriaenssens EM, Wittmann J, Vogensen FK et al (2016) Taxonomy of prokaryotic viruses: update from the ICTV bacterial and archaeal viruses subcommittee. Arch Virol 161:1095–1099
Krupovic M, Prangishvil D, Hendrix RW, Bamford DH (2011) Genomics of bacterial and Archaeal viruses: dynamics within the prokaryotic Virosphere. Microbiol and Mol Biol Rev 75(4):610–635
Lindell D, Sullivan MB, Johnson ZI, Tolonen AC, Rohwer F, Chisholm W (2004) Transfer of photosynthesis genes to and from Prochlorococcus viruses. Proc Natl Acad Sci U S A 101(30):11013–11018
Long SR (2001) Genes and signals in the rhizobium-legume symbiosis. Plant Physiol 125:69–72
López-García P, Eme L, Moreira D (2017) Symbiosis in eukaryotic evolution. J Theor Biol 434:20–33
López-Garcia P, Moreira D (2009) Ten reasons to exclude viruses from the tree of life. Nat Rev Microbiol 7:306–311
López-Garcia P, Moreira D (2009b) Yet viruses cannot be included in the tree of life. Nature Rev Microbiol 7:306–311. https://doi.org/10.1038/nrmicro2108-c1
Lu X, Sachs F, Ramsay L, Jacques PE, Jacques PÉ et al (2014) The retrovirus HERV-H is a long noncoding RNA required for human embryonic stem cell identity. Nat Struct Mol Biol 21(4):423–425
Ludmir EB, Enquist LW (2009) Viral genomes are part of the phylogenetic tree of life. Nat Rev Microbiol 7(8):615. https://doi.org/10.1038/nrmicro2108-c4
Luria SE, Darnell JE (1967) General virology. John Wiley & Sons, INC., New York
Mameli G, Poddighe L, Astone V, Delogu G, Arru G et al (2009) Novel reliable real-time PCR for differential detection of MSRVenv and syncytin-1 in RNA and DNA from patients with multiple sclerosis. J Virol Methods 161:98–106
Mameli G, Poddighe L, Mei A, Uleri E, Sotgiu S et al (2012) Expression and activation by Epstein Barr virus of human endogenous retroviruses-W in blood cells and astrocytes: inference for multiple sclerosis. PLoS One 7(9):e44991. https://doi.org/10.1371/journal.pone.0044991
Margulis L (1970) Origin of eukaryotic cells. Yale University Press, New Haven and London
Margulis L, Fester R (eds) (1991) Symbiosis as a source of evolutionary innovation. MIT Press, Cambridge Massachusetts and London
Martin J, Herniou E, Cook J, O’Neill RW, Tristem M (1997) Human endogenous retrovirus type I-related viruses have an apparently widespread distribution within vertebrates. J Virol 71:437–443
Medstrand P, Landry JR, Mager DL (2001) Long terminal repeats are used as alternative promoters for the endothelin B receptor and apolipoprotein C-I genes in humans. J Biol Chem 276:1896–1903
Medstrand P, Mager DL (1998) Human-specific integrations of the HERV-K endogenous retrovirus family. J Virol 72:9782–9787
Merezhkovskii C (1910) Retrospectively quoted in his paper, La plante considérée comme un complexe symbiotique. Bull de la Société Naturelles 6:17–98
Mi S, Lee X, Li X-P, Veldman GM, Finnerty H et al (2000) Syncytin is a captive retroviral envelope protein involved in human placental morphogenesis. Nature 403:785–789
Nasir AK, Kim M, Caetano-Annoles G (2012) Viral evolution. Primordial cellular origins and late adaptation to parasitism. Mob Genet Elem 2(5):247–252
Navas-Castillo J (2009) Six comments on the ten reasons for the demotion of viruses. Nat Rev Microbiol 7(8):615. https://doi.org/10.1038/nrmicro2108-c2
Naville M, Volff J-N (2016) Endogenous retroviruses in fish genomes: from relics of past infections to evolutionary innovations? Front Microbiol 7:1197. https://doi.org/10.3389/fmicb.2016.01197
Nowak MA (1992) What is a Quasispecies? TREE 7:118–121
Pender MP, Csurhes PA, Smith C, Douglas NL, Neller MA et al (2018) Epstein-Barr virus-specific T cell therapy for progressive multiple sclerosis. JCI Insight 3(22):e124714. https://doi.org/10.1172/jci.insight.124714
Pierce SK, Mahadevan P, Massey SE, Middlebrooks ML (2016) A preliminary molecular and phylogenetic analysis of the genome of a novel endogenous retrovirus in the sea slug Elysia Chlorotica. Biol Bull 231:236–244
Pierce SK, Maugel TK, Rumpho ME, Hanten JJ, Mondy WL (1999) Annual viral expression in a sea slug population: life cycle control and symbiotic chloroplast maintenance. Biol Bull 197:1–6
Pittoggi C, Sciamanna I, Mattei E, Beraldi R, Lobascio AM et al (2003) Role of endogenous reverse transcriptase in murine early embryo development. Mol Reprod Dev 66:225–236
Pontén F, Gry M, Fagerberg L, Lundberg E, Asplund A et al (2009) A global view of protein expression in human cells, tissues, and organs. Mol Systems Biol 5:337. https://doi.org/10.1038/msb.2009.93
Prangashvili D, Garrett RA (2004) Exceptionally diverse morphotypes and genomes of crenarcheal hyperthermophilic viruses. Biochem Soc Trans 32(2):204–208
Raoult D (2009) There is no such thing as a tree of life (and of course viruses are out!). Nat Rev Microbiol 7(8):615. https://doi.org/10.1038/nrmicro2108-c6
Redon R, Ishikawa S, Fitch KR, Feuk L, Perry GH et al (2006) Global variation in copy number in the human genome. Nature 444:444–454
Roossinck MJ, Martin DP, Roumagnac P (2015) Plant virus Metagenomics: advances in virus discovery. Phytopath Rev 105:716–727
Rosario K, Breitbart M (2011) Exploring the viral world through metagenomics. Curr Opin Virol 1(1):289–297
Routledge SJ, Proudfoot NJ (2002) Definition of transcriptional promoters in the human beta globin locus control region. J Mol Biol 323:601–611
Ryan F (1997) Virus X. Little Brown Publishers, Boston, MA
Ryan F (2002) Darwin’s blind spot. Houghton Mifflin, Boston and New York
Ryan F (2009a) Virolution. Collins Publishers, London, UK
Ryan F (2009b) An alternative approach to medical genetics based on modern evolutionary biology. Part 3: HERVs in diseases. J R Soc Med 102:415–424
Ryan F (2016) Viral symbiosis and the holobiontic nature of the human genome. APMIS 124:11–19
Ryan F (2019) Virusphere. Collins Publishers, London, UK
Sagan L (1967) On the origin of mitosing cells. J Theor Biol 14:255–274
Sapp J (1994) Evolution by association: a history of Symbiosis. Oxford University Press, New York
Shapiro JA (2019) No genome is an island: towards a 21st century agenda for evolution. Ann N Y Acad Sci 1447(1):21–52. https://doi.org/10.1111/nyas.14044
Soygur B, Sati L (2016) The role of syncytins in human reproduction and reproductive organ cancers. Reproduction 152(5):R167–R178. Soc for Reprod and Fertility ISSN 1470-1626 (paper) 1741-7899 (online). https://doi.org/10.1530/REP-16-0031
Spadafora C (2008) A reverse transcriptase-dependent mechanism plays central roles in fundamental biological processes. Systems Biol in Reprod Medi 54:11–21
Sullivan JT, Ronson CW (1998) Evolution of rhizobia by acquisition of a 500-kb symbiosis island that integrates into a phe-tRNA gene. Proc Natl Acad Sci U S A 95:5145–5149
Suttle CA (2005) Viruses in the sea. Nature 437:356–361
Suttle CA (2007) Marine viruses – major players in the global ecosystem. Nat Rev Microbiol 5:801–812
Takeuchi N, Hogewoeg P (2008) Evolution of complexity in RNA-like replicators systems. Biol Direct 3:11. https://doi.org/10.1186/1745-6150-3-11
van de Laagemaat LN, Landry J-R, Mager DL, Medstrand P (2003) Transposable elements in mammals promote regulatory variation and diversification of genes with specialized functions. Trends Genet 19(10):530–536
Vignuzzi M, Stone JK, Arnold JJ, Cameron CE, Andino R (2006) Quasispecies diversity determines pathogenesis through cooperative interactions in a viral population. Nature 439:344–348
Villarreal LP (2005) Viruses and the evolution of life. ASM Press, Washington, DC
Villarreal LP (2014) Force for ancient and recent life: viral and stem-loop RNA consortia promote life. Ann N. Y. Acad Sci 1341:25–34
Villarreal LP, DeFilippis VR (2000) A hypothesis for DNA viruses as the origin of eukaryotic replication proteins. J Virol 74(15):7079–7084
Villarreal LP, Ryan F (2011) Viruses in host evolution: general principles and future extrapolations. Curr Topics in Virol 9:79–90
Villarreal LP, Witzany G (2010) Viruses are essential agents within the roots and stem of the tree of life. J Theoret Biol 262:698–710
Volkman HE, Stetson DB (2014) The enemy within: endogenous retroelements and autoimmune disease. Nat Immun 15(5):415–422
Wilhelm SW, Suttle CA (1999) Viruses and nutrient cycles in the sea. Bioscience 49:781–788
Williamson KE, Fuhrmann JJ, Wommack KE, Radosevich M (2017) Viruses in soil ecosystems: an unknown quantity within an unexplored territory. Ann Rev Virol 4:201–219
Williamson KE, Radosevich M, Smith DW, Wommack KE (2007) Incidence of lysogeny within temperate and extreme soil environments. Environ Microbiol 9:2563–2574
Williamson KE, Radosevich M, Wommack ME (2005) Abundance and diversity of viruses in six Delaware soils. Appl Environ Microbiol 71(60):3119–31125
Woese CR, Kandler O, Wheelis ML (1990) Towards a natural system of organisms: proposal for the domains, Archaea, bacteria and Eukarya. Proc Nat Acad Sci 87(12):4576–4579
Wommack KE, Colwell RR (2000) Viroplankton: viruses in aquatic ecosystems. Microbiol Mol Biol Rev 64:69–114
Zaman L, Meyer JL, Devangam S, Bryson DM, Lenski RE, Ofria C (2014) Coevolution drives the emergence of complex traits and promotes evolvability. PLoS Biol 12(12):e1002023. https://doi.org/10.1371/journal.pbio.1002023
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2020 Springer Nature Switzerland AG
About this chapter
Cite this chapter
Ryan, F. (2020). Viral Symbiosis in the Origins and Evolution of Life with a Particular Focus on the Placental Mammals. In: Kloc, M. (eds) Symbiosis: Cellular, Molecular, Medical and Evolutionary Aspects. Results and Problems in Cell Differentiation, vol 69. Springer, Cham. https://doi.org/10.1007/978-3-030-51849-3_1
Download citation
DOI: https://doi.org/10.1007/978-3-030-51849-3_1
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-030-51848-6
Online ISBN: 978-3-030-51849-3
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)