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Origin of viruses: primordial replicators recruiting capsids from hosts

Nature Reviews Microbiology volume 17, pages 449–458 (2019)Cite this article

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Abstract

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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Fig. 1: The three major scenarios for the origin of viruses.
Fig. 2: Evolution of viral and cellular replication modules from the ancestral RNA recognition motif.
Fig. 3: Major viral structural proteins and their cellular homologues.
Fig. 4: The chimeric scenario for the origin of viruses.

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References

  1. Danovaro, R. et al. Virus-mediated archaeal hecatomb in the deep seafloor. Sci. Adv. 2, e1600492 (2016).

    PubMed  PubMed Central  Google Scholar 

  2. Chow, C. E. & Suttle, C. A. Biogeography of viruses in the sea. Annu. Rev. Virol. 2, 41–66 (2015).

    CAS  PubMed  Google Scholar 

  3. Cobián Güemes, A. G. et al. Viruses as winners in the game of life. Annu. Rev. Virol. 3, 197–214 (2016).

    PubMed  Google Scholar 

  4. Koonin, E. V. & Dolja, V. V. A virocentric perspective on the evolution of life. Curr. Opin. Virol. 3, 546–557 (2013).

    PubMed  PubMed Central  Google Scholar 

  5. Raoult, D. & Forterre, P. Redefining viruses: lessons from mimivirus. Nat. Rev. Microbiol. 6, 315–319 (2008).

    CAS  PubMed  Google Scholar 

  6. 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).

    PubMed  PubMed Central  Google Scholar 

  7. Iranzo, J., Puigbo, P., Lobkovsky, A. E., Wolf, Y. I. & Koonin, E. V. Inevitability of genetic parasites. Genome Biol. Evol. 8, 2856–2869 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  8. Koonin, E. V. Viruses and mobile elements as drivers of evolutionary transitions. Philos. Trans. R Soc. B Biol. Sci. 371, 20150442 (2016).

    Google Scholar 

  9. Forterre, P. & Prangishvili, D. The major role of viruses in cellular evolution: facts and hypotheses. Curr. Opin. Virol. 3, 558–565 (2013).

    CAS  PubMed  Google Scholar 

  10. Frank, J. A. & Feschotte, C. Co-option of endogenous viral sequences for host cell function. Curr. Opin. Virol. 25, 81–89 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  11. Forterre, P. The origin of viruses and their possible roles in major evolutionary transitions. Virus Res. 117, 5–16 (2006).

    CAS  PubMed  Google Scholar 

  12. Luria, S. E. & Darnell, J. E. General Virology (Wiley, 1967).

  13. Sapp, J. The prokaryote-eukaryote dichotomy: meanings and mythology. Microbiol. Mol. Biol. Rev. 69, 292–305 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  14. Flugel, R. M. The precellular scenario of genovirions. Virus Genes 40, 151–154 (2010).

    PubMed  Google Scholar 

  15. Forterre, P. & Prangishvili, D. The origin of viruses. Res. Microbiol. 160, 466–472 (2009).

    CAS  PubMed  Google Scholar 

  16. Koonin, E. V., Senkevich, T. G. & Dolja, V. V. The ancient virus world and evolution of cells. Biol. Direct 1, 29 (2006).

    PubMed  PubMed Central  Google Scholar 

  17. Morse, S. S. (ed.) in The Evolutionary Biology of Viruses 1–28 (Raven Press, 1994).

  18. Holmes, E. C. What does virus evolution tell us about virus origins? J. Virol. 85, 5247–5251 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  19. Abrahao, J. et al. Tailed giant Tupanvirus possesses the most complete translational apparatus of the known virosphere. Nat. Commun. 9, 749 (2018).

    PubMed  PubMed Central  Google Scholar 

  20. Schulz, F. et al. Giant viruses with an expanded complement of translation system components. Science 356, 82–85 (2017).

    CAS  PubMed  Google Scholar 

  21. 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).

    CAS  PubMed  Google Scholar 

  22. Nasir, A. & Caetano-Anolles, G. A phylogenomic data-driven exploration of viral origins and evolution. Sci. Adv. 1, e1500527 (2015).

    PubMed  PubMed Central  Google Scholar 

  23. 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).

    CAS  PubMed  Google Scholar 

  24. 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).

    PubMed  PubMed Central  Google Scholar 

  25. Forterre, P. & Krupovic, M. in Viruses: Essential Agents of Life (ed. Witzany, G.) 43–60 (Springer Netherlands, 2012).

  26. 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).

    CAS  PubMed  Google Scholar 

  27. Roux, S. et al. Ecogenomics and potential biogeochemical impacts of globally abundant ocean viruses. Nature 537, 689–693 (2016).

    CAS  PubMed  Google Scholar 

  28. Pushkarev, A. et al. A distinct abundant group of microbial rhodopsins discovered using functional metagenomics. Nature 558, 595–599 (2018).

    CAS  PubMed  Google Scholar 

  29. 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).

    CAS  PubMed  Google Scholar 

  30. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  31. Koonin, E. V., Dolja, V. V. & Krupovic, M. Origins and evolution of viruses of eukaryotes: the ultimate modularity. Virology 479–480, 2–25 (2015).

    PubMed  PubMed Central  Google Scholar 

  32. Krupovic, M. & Bamford, D. H. Order to the viral universe. J. Virol. 84, 12476–12479 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  33. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  34. 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).

    CAS  PubMed  Google Scholar 

  35. Autexier, C. & Lue, N. F. The structure and function of telomerase reverse transcriptase. Annu. Rev. Biochem. 75, 493–517 (2006).

    CAS  Google Scholar 

  36. te Velthuis, A. J. Common and unique features of viral RNA-dependent polymerases. Cell. Mol. Life Sci. 71, 4403–4420 (2014).

    Google Scholar 

  37. Venkataraman, S., Prasad, B. & Selvarajan, R. RNA dependent RNA polymerases: insights from structure, function and evolution. Viruses 10, 76 (2018).

    PubMed Central  Google Scholar 

  38. 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).

    PubMed  Google Scholar 

  39. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  40. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  41. Clery, A., Blatter, M. & Allain, F. H. RNA recognition motifs: boring? Not quite. Curr. Opin. Struct. Biol. 18, 290–298 (2008).

    CAS  PubMed  Google Scholar 

  42. Gilbert, W. Origin of life: the RNA world. Nature 319, 618 (1986).

    Google Scholar 

  43. Wolf, Y. I. et al. Origins and evolution of the global RNA virome. mBio 9, e02329–02318 (2018).

    PubMed  PubMed Central  Google Scholar 

  44. 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).

    CAS  PubMed  Google Scholar 

  45. McNeil, B. A., Semper, C. & Zimmerly, S. Group II introns: versatile ribozymes and retroelements. Wiley Interdiscip. Rev. RNA 7, 341–355 (2016).

    CAS  PubMed  Google Scholar 

  46. 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).

    PubMed  PubMed Central  Google Scholar 

  47. Salgado, P. S. et al. The structure of an RNAi polymerase links RNA silencing and transcription. PLOS Biol. 4, e434 (2006).

    PubMed  PubMed Central  Google Scholar 

  48. Weigel, C. & Seitz, H. Bacteriophage replication modules. FEMS Microbiol. Rev. 30, 321–381 (2006).

    CAS  PubMed  Google Scholar 

  49. Novikova, O. & Belfort, M. Mobile group II introns as ancestral eukaryotic elements. Trends Genet. 33, 773–783 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  50. 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).

    PubMed  PubMed Central  Google Scholar 

  51. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  52. 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).

    CAS  PubMed  Google Scholar 

  53. Lee, K. Y. & Lee, B. J. Structural and biochemical properties of novel self-cleaving ribozymes. Molecules 22, E678 (2017).

    PubMed  Google Scholar 

  54. Joyce, G. F. & Szostak, J. W. Protocells and RNA self-replication. Cold Spring Harb. Perspect. Biol. 10, a034801 (2018).

    PubMed  Google Scholar 

  55. Lancet, D., Zidovetzki, R. & Markovitch, O. Systems protobiology: origin of life in lipid catalytic networks. J. R. Soc. Interface 15, 20180159 (2018).

    PubMed  PubMed Central  Google Scholar 

  56. 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).

    CAS  PubMed  Google Scholar 

  57. Martin, W., Baross, J., Kelley, D. & Russell, M. J. Hydrothermal vents and the origin of life. Nat. Rev. Microbiol. 6, 805–814 (2008).

    CAS  PubMed  Google Scholar 

  58. Koonin, E. V. & Martin, W. On the origin of genomes and cells within inorganic compartments. Trends Genet. 21, 647–654 (2005).

    CAS  PubMed  Google Scholar 

  59. Bamford, D. H. Do viruses form lineages across different domains of life? Res. Microbiol. 154, 231–236 (2003).

    CAS  PubMed  Google Scholar 

  60. Forterre, P., Krupovic, M. & Prangishvili, D. Cellular domains and viral lineages. Trends Microbiol. 22, 554–558 (2014).

    CAS  PubMed  Google Scholar 

  61. Caspar, D. L. & Klug, A. Physical principles in the construction of regular viruses. Cold Spring Harb. Symp. Quant. Biol. 27, 1–24 (1962).

    CAS  PubMed  Google Scholar 

  62. Crick, F. H. & Watson, J. D. Structure of small viruses. Nature 177, 473–475 (1956).

    CAS  PubMed  Google Scholar 

  63. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  64. Solovyev, A. G. & Makarov, V. V. Helical capsids of plant viruses: architecture with structural lability. J. Gen. Virol. 97, 1739–1754 (2016).

    CAS  PubMed  Google Scholar 

  65. DiMaio, F. et al. A virus that infects a hyperthermophile encapsidates A-form DNA. Science 348, 914–917 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  66. Ptchelkine, D. et al. Unique architecture of thermophilic archaeal virus APBV1 and its genome packaging. Nat. Commun. 8, 1436 (2017).

    PubMed  PubMed Central  Google Scholar 

  67. Zamora, M. et al. Potyvirus virion structure shows conserved protein fold and RNA binding site in ssRNA viruses. Sci. Adv. 3, eaao2182 (2017).

    PubMed  PubMed Central  Google Scholar 

  68. DiMaio, F. et al. The molecular basis for flexibility in the flexible filamentous plant viruses. Nat. Struct. Mol. Biol. 22, 642–644 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  69. 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).

    PubMed  Google Scholar 

  70. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  71. Jamin, M. & Yabukarski, F. Nonsegmented negative-sense RNA viruses-structural data bring new insights into nucleocapsid assembly. Adv. Virus Res. 97, 143–185 (2017).

    CAS  PubMed  Google Scholar 

  72. Prangishvili, D. et al. The enigmatic archaeal virosphere. Nat. Rev. Microbiol. 15, 724–739 (2017).

    CAS  PubMed  Google Scholar 

  73. Abrescia, N. G., Bamford, D. H., Grimes, J. M. & Stuart, D. I. Structure unifies the viral universe. Annu. Rev. Biochem. 81, 795–822 (2012).

    CAS  PubMed  Google Scholar 

  74. 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).

    CAS  PubMed  Google Scholar 

  75. 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).

    CAS  PubMed  Google Scholar 

  76. Krupovic, M. & Koonin, E. V. Multiple origins of viral capsid proteins from cellular ancestors. Proc. Natl Acad. Sci. USA 114, E2401–E2410 (2017).

    CAS  PubMed  Google Scholar 

  77. Krupovic, M. Networks of evolutionary interactions underlying the polyphyletic origin of ssDNA viruses. Curr. Opin. Virol. 3, 578–586 (2013).

    CAS  PubMed  Google Scholar 

  78. Rossmann, M. G. & Johnson, J. E. Icosahedral RNA virus structure. Annu. Rev. Biochem. 58, 533–573 (1989).

    CAS  PubMed  Google Scholar 

  79. Moreira, D. & López-García, P. Ten reasons to exclude viruses from the tree of life. Nat. Rev. Microbiol. 7, 306–311 (2009).

    CAS  PubMed  Google Scholar 

  80. Sasaki, E. et al. Structure and assembly of scalable porous protein cages. Nat. Commun. 8, 14663 (2017).

    PubMed  PubMed Central  Google Scholar 

  81. 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).

    CAS  PubMed  Google Scholar 

  82. Kerfeld, C. A., Aussignargues, C., Zarzycki, J., Cai, F. & Sutter, M. Bacterial microcompartments. Nat. Rev. Microbiol. 16, 277–290 (2018).

    CAS  PubMed  PubMed Central  Google Scholar 

  83. Krupovic, M. & Koonin, E. V. Cellular origin of the viral capsid-like bacterial microcompartments. Biol. Direct 12, 25 (2017).

    PubMed  PubMed Central  Google Scholar 

  84. Cheng, S. & Brooks, C. L. 3rd. Viral capsid proteins are segregated in structural fold space. PLOS Comput. Biol. 9, e1002905 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  85. Sabath, N., Wagner, A. & Karlin, D. Evolution of viral proteins originated de novo by overprinting. Mol. Biol. Evol. 29, 3767–3780 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  86. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  87. 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).

    CAS  PubMed  Google Scholar 

  88. Locksley, R. M., Killeen, N. & Lenardo, M. J. The TNF and TNF receptor superfamilies: integrating mammalian biology. Cell 104, 487–501 (2001).

    CAS  PubMed  Google Scholar 

  89. Liu, Y. et al. Crystal structure of sTALL-1 reveals a virus-like assembly of TNF family ligands. Cell 108, 383–394 (2002).

    CAS  PubMed  Google Scholar 

  90. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  91. Neu, U., Bauer, J. & Stehle, T. Viruses and sialic acids: rules of engagement. Curr. Opin. Struct. Biol. 21, 610–618 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  92. Maginnis, M. S. Virus-receptor interactions: the key to cellular invasion. J. Mol. Biol. 430, 2590–2611 (2018).

    CAS  PubMed  Google Scholar 

  93. Liu, Y. et al. Sialic acid-dependent cell entry of human enterovirus D68. Nat. Commun. 6, 8865 (2015).

    PubMed  PubMed Central  Google Scholar 

  94. Shi, M. et al. Redefining the invertebrate RNA virosphere. Nature 540, 539–543 (2016).

    CAS  PubMed  Google Scholar 

  95. 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).

    CAS  PubMed  Google Scholar 

  96. Kauffman, K. M. et al. A major lineage of non-tailed dsDNA viruses as unrecognized killers of marine bacteria. Nature 554, 118–122 (2018).

    CAS  PubMed  Google Scholar 

  97. 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).

    PubMed  PubMed Central  Google Scholar 

  98. 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).

    CAS  PubMed  Google Scholar 

  99. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  100. Santos-Perez, I. et al. Structural basis for assembly of vertical single β-barrel viruses. Nat. Commun. 10, 1184 (2019).

    PubMed  PubMed Central  Google Scholar 

  101. Kuhn, R. J. & Rossmann, M. G. Structure and assembly of icosahedral enveloped RNA viruses. Adv. Virus Res. 64, 263–284 (2005).

    CAS  PubMed  Google Scholar 

  102. Krupovic, M. et al. Ortervirales: new virus order unifying five families of reverse-transcribing viruses. J. Virol. 92, e00515-18 (2018).

    CAS  PubMed  PubMed Central  Google Scholar 

  103. 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).

    PubMed  PubMed Central  Google Scholar 

  104. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  105. Fedry, J. et al. The ancient gamete fusogen HAP2 is a eukaryotic class II fusion protein. Cell 168, 904–915 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  106. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  107. Guardado-Calvo, P. & Rey, F. A. The envelope proteins of the bunyavirales. Adv. Virus Res. 98, 83–118 (2017).

    PubMed  Google Scholar 

  108. Modis, Y. Relating structure to evolution in class II viral membrane fusion proteins. Curr. Opin. Virol. 5, 34–41 (2014).

    CAS  PubMed  Google Scholar 

  109. 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).

    PubMed  PubMed Central  Google Scholar 

  110. 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).

    CAS  PubMed  Google Scholar 

  111. Shi, M., Zhang, Y. Z. & Holmes, E. C. Meta-transcriptomics and the evolutionary biology of RNA viruses. Virus Res. 243, 83–90 (2018).

    CAS  PubMed  Google Scholar 

  112. Bale, J. B. et al. Accurate design of megadalton-scale two-component icosahedral protein complexes. Science 353, 389–394 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  113. Butterfield, G. L. et al. Evolution of a designed protein assembly encapsulating its own RNA genome. Nature 552, 415–420 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  114. 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).

    CAS  PubMed  Google Scholar 

  115. 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).

    CAS  PubMed  Google Scholar 

  116. Craig, N. L. et al. (eds) Mobile DNA III 3rd edn (ASM Press, 2015).

  117. 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).

    CAS  PubMed  Google Scholar 

  118. Mizuno, C. M. et al. Numerous cultivated and uncultivated viruses encode ribosomal proteins. Nat. Commun. 10, 752 (2019).

    PubMed  PubMed Central  Google Scholar 

  119. Casadevall, A. Evolution of intracellular pathogens. Annu. Rev. Microbiol. 62, 19–33 (2008).

    CAS  PubMed  Google Scholar 

  120. López-García, P., Eme, L. & Moreira, D. Symbiosis in eukaryotic evolution. J. Theor. Biol. 434, 20–33 (2017).

    PubMed  PubMed Central  Google Scholar 

  121. 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).

    PubMed  PubMed Central  Google Scholar 

  122. Jalasvuori, M. Vehicles, replicators, and intercellular movement of genetic information: evolutionary dissection of a bacterial cell. Int. J. Evol. Biol. 2012, 874153 (2012).

    PubMed  PubMed Central  Google Scholar 

  123. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  124. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  125. Gladyshev, E. A. & Arkhipova, I. R. A widespread class of reverse transcriptase-related cellular genes. Proc. Natl Acad. Sci. USA 108, 20311–20316 (2011).

    CAS  PubMed  Google Scholar 

  126. Arkhipova, I. R. Using bioinformatic and phylogenetic approaches to classify transposable elements and understand their complex evolutionary histories. Mob. DNA 8, 19 (2017).

    PubMed  PubMed Central  Google Scholar 

  127. Gong, Z. & Han, G. Z. Insect retroelements provide novel insights into the origin of hepatitis B viruses. Mol. Biol. Evol. 35, 2254–2259 (2018).

    Google Scholar 

  128. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  129. Koonin, E. V. & Krupovic, M. Polintons, virophages and transpovirons: a tangled web linking viruses, transposons and immunity. Curr. Opin. Virol. 25, 7–15 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  130. Chandler, M. et al. Breaking and joining single-stranded DNA: the HUH endonuclease superfamily. Nat. Rev. Microbiol. 11, 525–538 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  131. 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).

    PubMed  Google Scholar 

  132. 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).

    CAS  PubMed  Google Scholar 

  133. Filée, J. & Forterre, P. Viral proteins functioning in organelles: a cryptic origin? Trends Microbiol. 13, 510–513 (2005).

    PubMed  Google Scholar 

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Acknowledgments

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).

Reviewer information

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.

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Authors and Affiliations

  1. Unité Biologie Moléculaire du Gène chez les Extrêmophiles, Institut Pasteur, Paris, France

    Mart Krupovic

  2. Department of Botany and Plant Pathology, Oregon State University, Corvallis, OR, USA

    Valerian V. Dolja

  3. National Center for Biotechnology Information, National Library of Medicine, Bethesda, MD, USA

    Eugene V. Koonin

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  1. Mart Krupovic
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  2. Valerian V. Dolja
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  3. Eugene V. Koonin
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All authors researched data for the article, contributed substantially to discussion of content, wrote the article and edited the manuscript before submission.

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Correspondence to Mart Krupovic or Eugene V. Koonin.

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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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