Viruses are ubiquitous parasites of cellular life and the most abundant biological entities on Earth. It is widely accepted that viruses are polyphyletic, but a consensus scenario for their ultimate origin is still lacking. Traditionally, three scenarios for the origin of viruses have been considered: descent from primordial, precellular genetic elements, reductive evolution from cellular ancestors and escape of genes from cellular hosts, achieving partial replicative autonomy and becoming parasitic genetic elements. These classical scenarios give different timelines for the origin(s) of viruses and do not explain the provenance of the two key functional modules that are responsible, respectively, for viral genome replication and virion morphogenesis. Here, we outline a ‘chimeric’ scenario under which different types of primordial, selfish replicons gave rise to viruses by recruiting host proteins for virion formation. We also propose that new groups of viruses have repeatedly emerged at all stages of the evolution of life, often through the displacement of ancestral structural and genome replication genes.
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Danovaro, R. et al. Virus-mediated archaeal hecatomb in the deep seafloor. Sci. Adv. 2, e1600492 (2016).
Chow, C. E. & Suttle, C. A. Biogeography of viruses in the sea. Annu. Rev. Virol. 2, 41–66 (2015).
Cobián Güemes, A. G. et al. Viruses as winners in the game of life. Annu. Rev. Virol. 3, 197–214 (2016).
Koonin, E. V. & Dolja, V. V. A virocentric perspective on the evolution of life. Curr. Opin. Virol. 3, 546–557 (2013).
Raoult, D. & Forterre, P. Redefining viruses: lessons from mimivirus. Nat. Rev. Microbiol. 6, 315–319 (2008).
Koonin, E. V., Wolf, Y. I. & Katsnelson, M. I. Inevitability of the emergence and persistence of genetic parasites caused by evolutionary instability of parasite-free states. Biol. Direct 12, 31 (2017).
Iranzo, J., Puigbo, P., Lobkovsky, A. E., Wolf, Y. I. & Koonin, E. V. Inevitability of genetic parasites. Genome Biol. Evol. 8, 2856–2869 (2016).
Koonin, E. V. Viruses and mobile elements as drivers of evolutionary transitions. Philos. Trans. R Soc. B Biol. Sci. 371, 20150442 (2016).
Forterre, P. & Prangishvili, D. The major role of viruses in cellular evolution: facts and hypotheses. Curr. Opin. Virol. 3, 558–565 (2013).
Frank, J. A. & Feschotte, C. Co-option of endogenous viral sequences for host cell function. Curr. Opin. Virol. 25, 81–89 (2017).
Forterre, P. The origin of viruses and their possible roles in major evolutionary transitions. Virus Res. 117, 5–16 (2006).
Luria, S. E. & Darnell, J. E. General Virology (Wiley, 1967).
Sapp, J. The prokaryote-eukaryote dichotomy: meanings and mythology. Microbiol. Mol. Biol. Rev. 69, 292–305 (2005).
Flugel, R. M. The precellular scenario of genovirions. Virus Genes 40, 151–154 (2010).
Forterre, P. & Prangishvili, D. The origin of viruses. Res. Microbiol. 160, 466–472 (2009).
Koonin, E. V., Senkevich, T. G. & Dolja, V. V. The ancient virus world and evolution of cells. Biol. Direct 1, 29 (2006).
Morse, S. S. (ed.) in The Evolutionary Biology of Viruses 1–28 (Raven Press, 1994).
Holmes, E. C. What does virus evolution tell us about virus origins? J. Virol. 85, 5247–5251 (2011).
Abrahao, J. et al. Tailed giant Tupanvirus possesses the most complete translational apparatus of the known virosphere. Nat. Commun. 9, 749 (2018).
Schulz, F. et al. Giant viruses with an expanded complement of translation system components. Science 356, 82–85 (2017).
Abergel, C., Legendre, M. & Claverie, J. M. The rapidly expanding universe of giant viruses: mimivirus, pandoravirus, pithovirus and mollivirus. FEMS Microbiol. Rev. 39, 779–796 (2015).
Nasir, A. & Caetano-Anolles, G. A phylogenomic data-driven exploration of viral origins and evolution. Sci. Adv. 1, e1500527 (2015).
Colson, P., La Scola, B., Levasseur, A., Caetano-Anolles, G. & Raoult, D. Mimivirus: leading the way in the discovery of giant viruses of amoebae. Nat. Rev. Microbiol. 15, 243–254 (2017).
Abrahao, J. S., Araujo, R., Colson, P. & La Scola, B. The analysis of translation-related gene set boosts debates around origin and evolution of mimiviruses. PLOS Genet. 13, e1006532 (2017).
Forterre, P. & Krupovic, M. in Viruses: Essential Agents of Life (ed. Witzany, G.) 43–60 (Springer Netherlands, 2012).
Fridman, S. et al. A myovirus encoding both photosystem I and II proteins enhances cyclic electron flow in infected Prochlorococcus cells. Nat. Microbiol. 2, 1350–1357 (2017).
Roux, S. et al. Ecogenomics and potential biogeochemical impacts of globally abundant ocean viruses. Nature 537, 689–693 (2016).
Pushkarev, A. et al. A distinct abundant group of microbial rhodopsins discovered using functional metagenomics. Nature 558, 595–599 (2018).
Ahlgren, N. A., Fuchsman, C. A., Rocap, G. & Fuhrman, J. A. Discovery of several novel, widespread, and ecologically distinct marine Thaumarchaeota viruses that encode amoC nitrification genes. ISME J. 13, 618–631 (2019).
Iranzo, J., Krupovic, M. & Koonin, E. V. The double-stranded DNA virosphere as a modular hierarchical network of gene sharing. mBio 7, e00978–00916 (2016).
Koonin, E. V., Dolja, V. V. & Krupovic, M. Origins and evolution of viruses of eukaryotes: the ultimate modularity. Virology 479–480, 2–25 (2015).
Krupovic, M. & Bamford, D. H. Order to the viral universe. J. Virol. 84, 12476–12479 (2010).
Kazlauskas, D., Krupovic, M. & Venclovas, C. The logic of DNA replication in double-stranded DNA viruses: insights from global analysis of viral genomes. Nucleic Acids Res. 44, 4551–4564 (2016).
Forterre, P. Three RNA cells for ribosomal lineages and three DNA viruses to replicate their genomes: a hypothesis for the origin of cellular domain. Proc. Natl Acad. Sci. USA 103, 3669–3674 (2006).
Autexier, C. & Lue, N. F. The structure and function of telomerase reverse transcriptase. Annu. Rev. Biochem. 75, 493–517 (2006).
te Velthuis, A. J. Common and unique features of viral RNA-dependent polymerases. Cell. Mol. Life Sci. 71, 4403–4420 (2014).
Venkataraman, S., Prasad, B. & Selvarajan, R. RNA dependent RNA polymerases: insights from structure, function and evolution. Viruses 10, 76 (2018).
Mönttinen, H. A., Ravantti, J. J. & Poranen, M. M. Common structural core of three-dozen residues reveals intersuperfamily relationships. Mol. Biol. Evol. 33, 1697–1710 (2016).
Iyer, L. M., Koonin, E. V., Leipe, D. D. & Aravind, L. Origin and evolution of the archaeo-eukaryotic primase superfamily and related palm-domain proteins: structural insights and new members. Nucleic Acids Res. 33, 3875–3896 (2005).
Kazlauskas, D. et al. Novel families of archaeo-eukaryotic primases associated with mobile genetic elements of bacteria and archaea. J. Mol. Biol. 430, 737–750 (2018).
Clery, A., Blatter, M. & Allain, F. H. RNA recognition motifs: boring? Not quite. Curr. Opin. Struct. Biol. 18, 290–298 (2008).
Gilbert, W. Origin of life: the RNA world. Nature 319, 618 (1986).
Wolf, Y. I. et al. Origins and evolution of the global RNA virome. mBio 9, e02329–02318 (2018).
Koonin, E. V., Wolf, Y. I., Nagasaki, K. & Dolja, V. V. The Big Bang of picorna-like virus evolution antedates the radiation of eukaryotic supergroups. Nat. Rev. Microbiol. 6, 925–939 (2008).
McNeil, B. A., Semper, C. & Zimmerly, S. Group II introns: versatile ribozymes and retroelements. Wiley Interdiscip. Rev. RNA 7, 341–355 (2016).
Iyer, L. M., Koonin, E. V. & Aravind, L. Evolutionary connection between the catalytic subunits of DNA-dependent RNA polymerases and eukaryotic RNA-dependent RNA polymerases and the origin of RNA polymerases. BMC Struct. Biol. 3, 1 (2003).
Salgado, P. S. et al. The structure of an RNAi polymerase links RNA silencing and transcription. PLOS Biol. 4, e434 (2006).
Weigel, C. & Seitz, H. Bacteriophage replication modules. FEMS Microbiol. Rev. 30, 321–381 (2006).
Novikova, O. & Belfort, M. Mobile group II introns as ancestral eukaryotic elements. Trends Genet. 33, 773–783 (2017).
Agrawal, R. K., Wang, H. W. & Belfort, M. Forks in the tracks: group II introns, spliceosomes, telomeres and beyond. RNA Biol. 13, 1218–1222 (2016).
Takeuchi, N., Hogeweg, P. & Koonin, E. V. On the origin of DNA genomes: evolution of the division of labor between template and catalyst in model replicator systems. PLOS Comput. Biol. 7, e1002024 (2011).
Ren, A., Micura, R. & Patel, D. J. Structure-based mechanistic insights into catalysis by small self-cleaving ribozymes. Curr. Opin. Chem. Biol. 41, 71–83 (2017).
Lee, K. Y. & Lee, B. J. Structural and biochemical properties of novel self-cleaving ribozymes. Molecules 22, E678 (2017).
Joyce, G. F. & Szostak, J. W. Protocells and RNA self-replication. Cold Spring Harb. Perspect. Biol. 10, a034801 (2018).
Lancet, D., Zidovetzki, R. & Markovitch, O. Systems protobiology: origin of life in lipid catalytic networks. J. R. Soc. Interface 15, 20180159 (2018).
Mulkidjanian, A. Y., Bychkov, A. Y., Dibrova, D. V., Galperin, M. Y. & Koonin, E. V. Origin of first cells at terrestrial, anoxic geothermal fields. Proc. Natl Acad. Sci. USA 109, E821–E830 (2012).
Martin, W., Baross, J., Kelley, D. & Russell, M. J. Hydrothermal vents and the origin of life. Nat. Rev. Microbiol. 6, 805–814 (2008).
Koonin, E. V. & Martin, W. On the origin of genomes and cells within inorganic compartments. Trends Genet. 21, 647–654 (2005).
Bamford, D. H. Do viruses form lineages across different domains of life? Res. Microbiol. 154, 231–236 (2003).
Forterre, P., Krupovic, M. & Prangishvili, D. Cellular domains and viral lineages. Trends Microbiol. 22, 554–558 (2014).
Caspar, D. L. & Klug, A. Physical principles in the construction of regular viruses. Cold Spring Harb. Symp. Quant. Biol. 27, 1–24 (1962).
Crick, F. H. & Watson, J. D. Structure of small viruses. Nature 177, 473–475 (1956).
Brum, J. R., Schenck, R. O. & Sullivan, M. B. Global morphological analysis of marine viruses shows minimal regional variation and dominance of non-tailed viruses. ISME J. 7, 1738–1751 (2013).
Solovyev, A. G. & Makarov, V. V. Helical capsids of plant viruses: architecture with structural lability. J. Gen. Virol. 97, 1739–1754 (2016).
DiMaio, F. et al. A virus that infects a hyperthermophile encapsidates A-form DNA. Science 348, 914–917 (2015).
Ptchelkine, D. et al. Unique architecture of thermophilic archaeal virus APBV1 and its genome packaging. Nat. Commun. 8, 1436 (2017).
Zamora, M. et al. Potyvirus virion structure shows conserved protein fold and RNA binding site in ssRNA viruses. Sci. Adv. 3, eaao2182 (2017).
DiMaio, F. et al. The molecular basis for flexibility in the flexible filamentous plant viruses. Nat. Struct. Mol. Biol. 22, 642–644 (2015).
Sun, Y., Li, J., Gao, G. F., Tien, P. & Liu, W. Bunyavirales ribonucleoproteins: the viral replication and transcription machinery. Crit. Rev. Microbiol. 44, 522–540 (2018).
Sun, Y., Guo, Y. & Lou, Z. A versatile building block: the structures and functions of negative-sense single-stranded RNA virus nucleocapsid proteins. Protein Cell 3, 893–902 (2012).
Jamin, M. & Yabukarski, F. Nonsegmented negative-sense RNA viruses-structural data bring new insights into nucleocapsid assembly. Adv. Virus Res. 97, 143–185 (2017).
Prangishvili, D. et al. The enigmatic archaeal virosphere. Nat. Rev. Microbiol. 15, 724–739 (2017).
Abrescia, N. G., Bamford, D. H., Grimes, J. M. & Stuart, D. I. Structure unifies the viral universe. Annu. Rev. Biochem. 81, 795–822 (2012).
Greene, L. H. et al. The CATH domain structure database: new protocols and classification levels give a more comprehensive resource for exploring evolution. Nucleic Acids Res. 35, D291–D297 (2007).
Krupovic, M. & Bamford, D. H. Double-stranded DNA viruses: 20 families and only five different architectural principles for virion assembly. Curr. Opin. Virol. 1, 118–124 (2011).
Krupovic, M. & Koonin, E. V. Multiple origins of viral capsid proteins from cellular ancestors. Proc. Natl Acad. Sci. USA 114, E2401–E2410 (2017).
Krupovic, M. Networks of evolutionary interactions underlying the polyphyletic origin of ssDNA viruses. Curr. Opin. Virol. 3, 578–586 (2013).
Rossmann, M. G. & Johnson, J. E. Icosahedral RNA virus structure. Annu. Rev. Biochem. 58, 533–573 (1989).
Moreira, D. & López-García, P. Ten reasons to exclude viruses from the tree of life. Nat. Rev. Microbiol. 7, 306–311 (2009).
Sasaki, E. et al. Structure and assembly of scalable porous protein cages. Nat. Commun. 8, 14663 (2017).
Ladenstein, R., Fischer, M. & Bacher, A. The lumazine synthase/riboflavin synthase complex: shapes and functions of a highly variable enzyme system. FEBS J. 280, 2537–2563 (2013).
Kerfeld, C. A., Aussignargues, C., Zarzycki, J., Cai, F. & Sutter, M. Bacterial microcompartments. Nat. Rev. Microbiol. 16, 277–290 (2018).
Krupovic, M. & Koonin, E. V. Cellular origin of the viral capsid-like bacterial microcompartments. Biol. Direct 12, 25 (2017).
Cheng, S. & Brooks, C. L. 3rd. Viral capsid proteins are segregated in structural fold space. PLOS Comput. Biol. 9, e1002905 (2013).
Sabath, N., Wagner, A. & Karlin, D. Evolution of viral proteins originated de novo by overprinting. Mol. Biol. Evol. 29, 3767–3780 (2012).
Boraston, A. B., Bolam, D. N., Gilbert, H. J. & Davies, G. J. Carbohydrate-binding modules: fine-tuning polysaccharide recognition. Biochem. J. 382, 769–781 (2004).
Eitoku, M., Sato, L., Senda, T. & Horikoshi, M. Histone chaperones: 30 years from isolation to elucidation of the mechanisms of nucleosome assembly and disassembly. Cell. Mol. Life Sci. 65, 414–444 (2008).
Locksley, R. M., Killeen, N. & Lenardo, M. J. The TNF and TNF receptor superfamilies: integrating mammalian biology. Cell 104, 487–501 (2001).
Liu, Y. et al. Crystal structure of sTALL-1 reveals a virus-like assembly of TNF family ligands. Cell 108, 383–394 (2002).
Shen, S., Bryant, K. D., Brown, S. M., Randell, S. H. & Asokan, A. Terminal N-linked galactose is the primary receptor for adeno-associated virus 9. J. Biol. Chem. 286, 13532–13540 (2011).
Neu, U., Bauer, J. & Stehle, T. Viruses and sialic acids: rules of engagement. Curr. Opin. Struct. Biol. 21, 610–618 (2011).
Maginnis, M. S. Virus-receptor interactions: the key to cellular invasion. J. Mol. Biol. 430, 2590–2611 (2018).
Liu, Y. et al. Sialic acid-dependent cell entry of human enterovirus D68. Nat. Commun. 6, 8865 (2015).
Shi, M. et al. Redefining the invertebrate RNA virosphere. Nature 540, 539–543 (2016).
Benson, S. D., Bamford, J. K., Bamford, D. H. & Burnett, R. M. Does common architecture reveal a viral lineage spanning all three domains of life? Mol. Cell 16, 673–685 (2004).
Kauffman, K. M. et al. A major lineage of non-tailed dsDNA viruses as unrecognized killers of marine bacteria. Nature 554, 118–122 (2018).
Yutin, N., Backstrom, D., Ettema, T. J. G., Krupovic, M. & Koonin, E. V. Vast diversity of prokaryotic virus genomes encoding double jelly-roll major capsid proteins uncovered by genomic and metagenomic sequence analysis. Virol. J. 15, 67 (2018).
Abrescia, N. G. et al. Insights into virus evolution and membrane biogenesis from the structure of the marine lipid-containing bacteriophage PM2. Mol. Cell 31, 749–761 (2008).
Rissanen, I. et al. Bacteriophage P23-77 capsid protein structures reveal the archetype of an ancient branch from a major virus lineage. Structure 21, 718–726 (2013).
Santos-Perez, I. et al. Structural basis for assembly of vertical single β-barrel viruses. Nat. Commun. 10, 1184 (2019).
Kuhn, R. J. & Rossmann, M. G. Structure and assembly of icosahedral enveloped RNA viruses. Adv. Virus Res. 64, 263–284 (2005).
Krupovic, M. et al. Ortervirales: new virus order unifying five families of reverse-transcribing viruses. J. Virol. 92, e00515-18 (2018).
Krupovic, M., Cvirkaite-Krupovic, V., Prangishvili, D. & Koonin, E. V. Evolution of an archaeal virus nucleocapsid protein from the CRISPR-associated Cas4 nuclease. Biol. Direct 10, 65 (2015).
Pinello, J. F. et al. Structure-function studies link class II viral fusogens with the ancestral gamete fusion protein HAP2. Curr. Biol. 27, 651–660 (2017).
Fedry, J. et al. The ancient gamete fusogen HAP2 is a eukaryotic class II fusion protein. Cell 168, 904–915 (2017).
Valansi, C. et al. Arabidopsis HAP2/GCS1 is a gamete fusion protein homologous to somatic and viral fusogens. J. Cell Biol. 216, 571–581 (2017).
Guardado-Calvo, P. & Rey, F. A. The envelope proteins of the bunyavirales. Adv. Virus Res. 98, 83–118 (2017).
Modis, Y. Relating structure to evolution in class II viral membrane fusion proteins. Curr. Opin. Virol. 5, 34–41 (2014).
Krupovic, M. & Koonin, E. V. Homologous capsid proteins testify to the common ancestry of retroviruses, caulimoviruses, pseudoviruses, and metaviruses. J. Virol. 91, e00210-17 (2017).
Dolja, V. V. & Koonin, E. V. Metagenomics reshapes the concepts of RNA virus evolution by revealing extensive horizontal virus transfer. Virus Res. 244, 36–52 (2018).
Shi, M., Zhang, Y. Z. & Holmes, E. C. Meta-transcriptomics and the evolutionary biology of RNA viruses. Virus Res. 243, 83–90 (2018).
Bale, J. B. et al. Accurate design of megadalton-scale two-component icosahedral protein complexes. Science 353, 389–394 (2016).
Butterfield, G. L. et al. Evolution of a designed protein assembly encapsulating its own RNA genome. Nature 552, 415–420 (2017).
Terasaka, N., Azuma, Y. & Hilvert, D. Laboratory evolution of virus-like nucleocapsids from nonviral protein cages. Proc. Natl Acad. Sci. USA 115, 5432–5437 (2018).
Nichols, R. J., Cassidy-Amstutz, C., Chaijarasphong, T. & Savage, D. F. Encapsulins: molecular biology of the shell. Crit. Rev. Biochem. Mol. Biol. 52, 583–594 (2017).
Craig, N. L. et al. (eds) Mobile DNA III 3rd edn (ASM Press, 2015).
Koonin, E. V., Krupovic, M. & Yutin, N. Evolution of double-stranded DNA viruses of eukaryotes: from bacteriophages to transposons to giant viruses. Ann. NY Acad. Sci. 1341, 10–24 (2015).
Mizuno, C. M. et al. Numerous cultivated and uncultivated viruses encode ribosomal proteins. Nat. Commun. 10, 752 (2019).
Casadevall, A. Evolution of intracellular pathogens. Annu. Rev. Microbiol. 62, 19–33 (2008).
López-García, P., Eme, L. & Moreira, D. Symbiosis in eukaryotic evolution. J. Theor. Biol. 434, 20–33 (2017).
Koonin, E. V. & Starokadomskyy, P. Are viruses alive? The replicator paradigm sheds decisive light on an old but misguided question. Stud. Hist. Philos. Biol. Biomed. Sci. 59, 125–134 (2016).
Jalasvuori, M. Vehicles, replicators, and intercellular movement of genetic information: evolutionary dissection of a bacterial cell. Int. J. Evol. Biol. 2012, 874153 (2012).
Koonin, E. V. & Dolja, V. V. Virus world as an evolutionary network of viruses and capsidless selfish elements. Microbiol. Mol. Biol. Rev. 78, 278–303 (2014).
Iranzo, J., Koonin, E. V., Prangishvili, D. & Krupovic, M. Bipartite network analysis of the archaeal virosphere: evolutionary connections between viruses and capsidless mobile elements. J. Virol. 90, 11043–11055 (2016).
Gladyshev, E. A. & Arkhipova, I. R. A widespread class of reverse transcriptase-related cellular genes. Proc. Natl Acad. Sci. USA 108, 20311–20316 (2011).
Arkhipova, I. R. Using bioinformatic and phylogenetic approaches to classify transposable elements and understand their complex evolutionary histories. Mob. DNA 8, 19 (2017).
Gong, Z. & Han, G. Z. Insect retroelements provide novel insights into the origin of hepatitis B viruses. Mol. Biol. Evol. 35, 2254–2259 (2018).
Krupovic, M., Beguin, P. & Koonin, E. V. Casposons: mobile genetic elements that gave rise to the CRISPR-Cas adaptation machinery. Curr. Opin. Microbiol. 38, 36–43 (2017).
Koonin, E. V. & Krupovic, M. Polintons, virophages and transpovirons: a tangled web linking viruses, transposons and immunity. Curr. Opin. Virol. 25, 7–15 (2017).
Chandler, M. et al. Breaking and joining single-stranded DNA: the HUH endonuclease superfamily. Nat. Rev. Microbiol. 11, 525–538 (2013).
Zhao, L., Rosario, K., Breitbart, M. & Duffy, S. Eukaryotic circular rep-encoding single-stranded DNA (CRESS DNA) viruses: ubiquitous viruses with small genomes and a diverse host range. Adv. Virus Res. 103, 71–133 (2019).
Erdmann, S., Tschitschko, B., Zhong, L., Raftery, M. J. & Cavicchioli, R. A plasmid from an Antarctic haloarchaeon uses specialized membrane vesicles to disseminate and infect plasmid-free cells. Nat. Microbiol. 2, 1446–1455 (2017).
Filée, J. & Forterre, P. Viral proteins functioning in organelles: a cryptic origin? Trends Microbiol. 13, 510–513 (2005).
E.V.K. is supported through the intramural programme of the US National Institutes of Health. M.K. was supported by the Agence Nationale de la Recherche (France) project ENVIRA (no. ANR-17-CE15-0005-01).
Nature Reviews Microbiology thanks Raul Andino, Purificación López-García, Didier Raoult and Yong-Zhen Zhang for their contribution to the peer review of this work.
The authors declare no competing interests.
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Krupovic, M., Dolja, V.V. & Koonin, E.V. Origin of viruses: primordial replicators recruiting capsids from hosts. Nat Rev Microbiol 17, 449–458 (2019). https://doi.org/10.1038/s41579-019-0205-6
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