Origin of viruses: primordial replicators recruiting capsids from hosts.
Journal
Nature reviews. Microbiology
ISSN: 1740-1534
Titre abrégé: Nat Rev Microbiol
Pays: England
ID NLM: 101190261
Informations de publication
Date de publication:
07 2019
07 2019
Historique:
pubmed:
31
5
2019
medline:
4
3
2020
entrez:
31
5
2019
Statut:
ppublish
Résumé
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.
Identifiants
pubmed: 31142823
doi: 10.1038/s41579-019-0205-6
pii: 10.1038/s41579-019-0205-6
doi:
Types de publication
Journal Article
Research Support, N.I.H., Intramural
Research Support, Non-U.S. Gov't
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
449-458Références
Danovaro, R. et al. Virus-mediated archaeal hecatomb in the deep seafloor. Sci. Adv. 2, e1600492 (2016).
pubmed: 27757416
pmcid: 5061471
Chow, C. E. & Suttle, C. A. Biogeography of viruses in the sea. Annu. Rev. Virol. 2, 41–66 (2015).
pubmed: 26958906
Cobián Güemes, A. G. et al. Viruses as winners in the game of life. Annu. Rev. Virol. 3, 197–214 (2016).
pubmed: 27741409
Koonin, E. V. & Dolja, V. V. A virocentric perspective on the evolution of life. Curr. Opin. Virol. 3, 546–557 (2013).
pubmed: 23850169
pmcid: 4326007
Raoult, D. & Forterre, P. Redefining viruses: lessons from mimivirus. Nat. Rev. Microbiol. 6, 315–319 (2008).
pubmed: 18311164
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: 29202832
pmcid: 5715634
Iranzo, J., Puigbo, P., Lobkovsky, A. E., Wolf, Y. I. & Koonin, E. V. Inevitability of genetic parasites. Genome Biol. Evol. 8, 2856–2869 (2016).
pubmed: 27503291
pmcid: 5631039
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).
pubmed: 23870799
Frank, J. A. & Feschotte, C. Co-option of endogenous viral sequences for host cell function. Curr. Opin. Virol. 25, 81–89 (2017).
pubmed: 28818736
pmcid: 5610649
Forterre, P. The origin of viruses and their possible roles in major evolutionary transitions. Virus Res. 117, 5–16 (2006).
pubmed: 16476498
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).
pubmed: 15944457
pmcid: 1197417
Flugel, R. M. The precellular scenario of genovirions. Virus Genes 40, 151–154 (2010).
pubmed: 20069351
Forterre, P. & Prangishvili, D. The origin of viruses. Res. Microbiol. 160, 466–472 (2009).
pubmed: 19647075
Koonin, E. V., Senkevich, T. G. & Dolja, V. V. The ancient virus world and evolution of cells. Biol. Direct 1, 29 (2006).
pubmed: 16984643
pmcid: 1594570
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).
pubmed: 21450811
pmcid: 3094976
Abrahao, J. et al. Tailed giant Tupanvirus possesses the most complete translational apparatus of the known virosphere. Nat. Commun. 9, 749 (2018).
pubmed: 29487281
pmcid: 5829246
Schulz, F. et al. Giant viruses with an expanded complement of translation system components. Science 356, 82–85 (2017).
pubmed: 28386012
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).
pubmed: 26391910
Nasir, A. & Caetano-Anolles, G. A phylogenomic data-driven exploration of viral origins and evolution. Sci. Adv. 1, e1500527 (2015).
pubmed: 26601271
pmcid: 4643759
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).
pubmed: 28239153
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: 28207761
pmcid: 5313130
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).
pubmed: 28785078
Roux, S. et al. Ecogenomics and potential biogeochemical impacts of globally abundant ocean viruses. Nature 537, 689–693 (2016).
pubmed: 27654921
Pushkarev, A. et al. A distinct abundant group of microbial rhodopsins discovered using functional metagenomics. Nature 558, 595–599 (2018).
pubmed: 29925949
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).
pubmed: 30315316
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).
pubmed: 27486193
pmcid: 4981718
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: 25771806
pmcid: 5898234
Krupovic, M. & Bamford, D. H. Order to the viral universe. J. Virol. 84, 12476–12479 (2010).
pubmed: 20926569
pmcid: 3004316
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).
pubmed: 27112572
pmcid: 4889955
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).
pubmed: 16505372
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).
pmcid: 5850383
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: 26931141
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).
pubmed: 16027112
pmcid: 1176014
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).
pubmed: 29198957
pmcid: 5862659
Clery, A., Blatter, M. & Allain, F. H. RNA recognition motifs: boring? Not quite. Curr. Opin. Struct. Biol. 18, 290–298 (2008).
pubmed: 18515081
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).
pubmed: 30482837
pmcid: 6282212
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).
pubmed: 18997823
McNeil, B. A., Semper, C. & Zimmerly, S. Group II introns: versatile ribozymes and retroelements. Wiley Interdiscip. Rev. RNA 7, 341–355 (2016).
pubmed: 26876278
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: 12553882
pmcid: 151600
Salgado, P. S. et al. The structure of an RNAi polymerase links RNA silencing and transcription. PLOS Biol. 4, e434 (2006).
pubmed: 17147473
pmcid: 1750930
Weigel, C. & Seitz, H. Bacteriophage replication modules. FEMS Microbiol. Rev. 30, 321–381 (2006).
pubmed: 16594962
Novikova, O. & Belfort, M. Mobile group II introns as ancestral eukaryotic elements. Trends Genet. 33, 773–783 (2017).
pubmed: 28818345
pmcid: 5659887
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: 27726484
pmcid: 5207386
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).
pubmed: 21455287
pmcid: 3063752
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).
pubmed: 29107885
Lee, K. Y. & Lee, B. J. Structural and biochemical properties of novel self-cleaving ribozymes. Molecules 22, E678 (2017).
pubmed: 28441772
Joyce, G. F. & Szostak, J. W. Protocells and RNA self-replication. Cold Spring Harb. Perspect. Biol. 10, a034801 (2018).
pubmed: 30181195
Lancet, D., Zidovetzki, R. & Markovitch, O. Systems protobiology: origin of life in lipid catalytic networks. J. R. Soc. Interface 15, 20180159 (2018).
pubmed: 30045888
pmcid: 6073634
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).
pubmed: 22331915
Martin, W., Baross, J., Kelley, D. & Russell, M. J. Hydrothermal vents and the origin of life. Nat. Rev. Microbiol. 6, 805–814 (2008).
pubmed: 18820700
Koonin, E. V. & Martin, W. On the origin of genomes and cells within inorganic compartments. Trends Genet. 21, 647–654 (2005).
pubmed: 16223546
Bamford, D. H. Do viruses form lineages across different domains of life? Res. Microbiol. 154, 231–236 (2003).
pubmed: 12798226
Forterre, P., Krupovic, M. & Prangishvili, D. Cellular domains and viral lineages. Trends Microbiol. 22, 554–558 (2014).
pubmed: 25129822
Caspar, D. L. & Klug, A. Physical principles in the construction of regular viruses. Cold Spring Harb. Symp. Quant. Biol. 27, 1–24 (1962).
pubmed: 14019094
Crick, F. H. & Watson, J. D. Structure of small viruses. Nature 177, 473–475 (1956).
pubmed: 13309339
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).
pubmed: 23635867
pmcid: 3749506
Solovyev, A. G. & Makarov, V. V. Helical capsids of plant viruses: architecture with structural lability. J. Gen. Virol. 97, 1739–1754 (2016).
pubmed: 27312096
DiMaio, F. et al. A virus that infects a hyperthermophile encapsidates A-form DNA. Science 348, 914–917 (2015).
pubmed: 25999507
pmcid: 5512286
Ptchelkine, D. et al. Unique architecture of thermophilic archaeal virus APBV1 and its genome packaging. Nat. Commun. 8, 1436 (2017).
pubmed: 29127347
pmcid: 5681674
Zamora, M. et al. Potyvirus virion structure shows conserved protein fold and RNA binding site in ssRNA viruses. Sci. Adv. 3, eaao2182 (2017).
pubmed: 28948231
pmcid: 5606705
DiMaio, F. et al. The molecular basis for flexibility in the flexible filamentous plant viruses. Nat. Struct. Mol. Biol. 22, 642–644 (2015).
pubmed: 26167882
pmcid: 4527879
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: 29516765
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).
pubmed: 23136065
pmcid: 4875381
Jamin, M. & Yabukarski, F. Nonsegmented negative-sense RNA viruses-structural data bring new insights into nucleocapsid assembly. Adv. Virus Res. 97, 143–185 (2017).
pubmed: 28057258
Prangishvili, D. et al. The enigmatic archaeal virosphere. Nat. Rev. Microbiol. 15, 724–739 (2017).
pubmed: 29123227
Abrescia, N. G., Bamford, D. H., Grimes, J. M. & Stuart, D. I. Structure unifies the viral universe. Annu. Rev. Biochem. 81, 795–822 (2012).
pubmed: 22482909
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).
pubmed: 17135200
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).
pubmed: 22440622
Krupovic, M. & Koonin, E. V. Multiple origins of viral capsid proteins from cellular ancestors. Proc. Natl Acad. Sci. USA 114, E2401–E2410 (2017).
pubmed: 28265094
Krupovic, M. Networks of evolutionary interactions underlying the polyphyletic origin of ssDNA viruses. Curr. Opin. Virol. 3, 578–586 (2013).
pubmed: 23850154
Rossmann, M. G. & Johnson, J. E. Icosahedral RNA virus structure. Annu. Rev. Biochem. 58, 533–573 (1989).
pubmed: 2673017
Moreira, D. & López-García, P. Ten reasons to exclude viruses from the tree of life. Nat. Rev. Microbiol. 7, 306–311 (2009).
pubmed: 19270719
Sasaki, E. et al. Structure and assembly of scalable porous protein cages. Nat. Commun. 8, 14663 (2017).
pubmed: 28281548
pmcid: 5354205
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).
pubmed: 23551830
Kerfeld, C. A., Aussignargues, C., Zarzycki, J., Cai, F. & Sutter, M. Bacterial microcompartments. Nat. Rev. Microbiol. 16, 277–290 (2018).
pubmed: 29503457
pmcid: 6022854
Krupovic, M. & Koonin, E. V. Cellular origin of the viral capsid-like bacterial microcompartments. Biol. Direct 12, 25 (2017).
pubmed: 29132422
pmcid: 5683377
Cheng, S. & Brooks, C. L. 3rd. Viral capsid proteins are segregated in structural fold space. PLOS Comput. Biol. 9, e1002905 (2013).
pubmed: 23408879
pmcid: 3567143
Sabath, N., Wagner, A. & Karlin, D. Evolution of viral proteins originated de novo by overprinting. Mol. Biol. Evol. 29, 3767–3780 (2012).
pubmed: 22821011
pmcid: 3494269
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).
pubmed: 15214846
pmcid: 1133952
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).
pubmed: 17955179
Locksley, R. M., Killeen, N. & Lenardo, M. J. The TNF and TNF receptor superfamilies: integrating mammalian biology. Cell 104, 487–501 (2001).
pubmed: 11239407
Liu, Y. et al. Crystal structure of sTALL-1 reveals a virus-like assembly of TNF family ligands. Cell 108, 383–394 (2002).
pubmed: 11853672
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).
pubmed: 21330365
pmcid: 3075699
Neu, U., Bauer, J. & Stehle, T. Viruses and sialic acids: rules of engagement. Curr. Opin. Struct. Biol. 21, 610–618 (2011).
pubmed: 21917445
pmcid: 3189341
Maginnis, M. S. Virus-receptor interactions: the key to cellular invasion. J. Mol. Biol. 430, 2590–2611 (2018).
pubmed: 29924965
Liu, Y. et al. Sialic acid-dependent cell entry of human enterovirus D68. Nat. Commun. 6, 8865 (2015).
pubmed: 26563423
pmcid: 4660200
Shi, M. et al. Redefining the invertebrate RNA virosphere. Nature 540, 539–543 (2016).
pubmed: 27880757
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).
pubmed: 15574324
Kauffman, K. M. et al. A major lineage of non-tailed dsDNA viruses as unrecognized killers of marine bacteria. Nature 554, 118–122 (2018).
pubmed: 29364876
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: 29636073
pmcid: 5894146
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).
pubmed: 18775333
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).
pubmed: 23623731
pmcid: 3919167
Santos-Perez, I. et al. Structural basis for assembly of vertical single β-barrel viruses. Nat. Commun. 10, 1184 (2019).
pubmed: 30862777
pmcid: 6414509
Kuhn, R. J. & Rossmann, M. G. Structure and assembly of icosahedral enveloped RNA viruses. Adv. Virus Res. 64, 263–284 (2005).
pubmed: 16139597
Krupovic, M. et al. Ortervirales: new virus order unifying five families of reverse-transcribing viruses. J. Virol. 92, e00515-18 (2018).
pubmed: 29618642
pmcid: 5974489
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: 26514828
pmcid: 4625639
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).
pubmed: 28238660
pmcid: 5393271
Fedry, J. et al. The ancient gamete fusogen HAP2 is a eukaryotic class II fusion protein. Cell 168, 904–915 (2017).
pubmed: 28235200
pmcid: 5332557
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).
pubmed: 28137780
pmcid: 5350521
Guardado-Calvo, P. & Rey, F. A. The envelope proteins of the bunyavirales. Adv. Virus Res. 98, 83–118 (2017).
pubmed: 28433053
Modis, Y. Relating structure to evolution in class II viral membrane fusion proteins. Curr. Opin. Virol. 5, 34–41 (2014).
pubmed: 24525225
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: 28356531
pmcid: 5446648
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).
pubmed: 29103997
Shi, M., Zhang, Y. Z. & Holmes, E. C. Meta-transcriptomics and the evolutionary biology of RNA viruses. Virus Res. 243, 83–90 (2018).
pubmed: 29111455
Bale, J. B. et al. Accurate design of megadalton-scale two-component icosahedral protein complexes. Science 353, 389–394 (2016).
pubmed: 27463675
pmcid: 5485857
Butterfield, G. L. et al. Evolution of a designed protein assembly encapsulating its own RNA genome. Nature 552, 415–420 (2017).
pubmed: 29236688
pmcid: 5927965
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).
pubmed: 29735682
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).
pubmed: 28635326
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).
pubmed: 25727355
Mizuno, C. M. et al. Numerous cultivated and uncultivated viruses encode ribosomal proteins. Nat. Commun. 10, 752 (2019).
pubmed: 30765709
pmcid: 6375957
Casadevall, A. Evolution of intracellular pathogens. Annu. Rev. Microbiol. 62, 19–33 (2008).
pubmed: 18785836
López-García, P., Eme, L. & Moreira, D. Symbiosis in eukaryotic evolution. J. Theor. Biol. 434, 20–33 (2017).
pubmed: 28254477
pmcid: 5638015
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: 26965225
pmcid: 5406846
Jalasvuori, M. Vehicles, replicators, and intercellular movement of genetic information: evolutionary dissection of a bacterial cell. Int. J. Evol. Biol. 2012, 874153 (2012).
pubmed: 22567533
pmcid: 3332184
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).
pubmed: 24847023
pmcid: 4054253
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).
pubmed: 27681128
pmcid: 5126363
Gladyshev, E. A. & Arkhipova, I. R. A widespread class of reverse transcriptase-related cellular genes. Proc. Natl Acad. Sci. USA 108, 20311–20316 (2011).
pubmed: 21876125
Arkhipova, I. R. Using bioinformatic and phylogenetic approaches to classify transposable elements and understand their complex evolutionary histories. Mob. DNA 8, 19 (2017).
pubmed: 29225705
pmcid: 5718144
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).
pubmed: 28472712
pmcid: 5665730
Koonin, E. V. & Krupovic, M. Polintons, virophages and transpovirons: a tangled web linking viruses, transposons and immunity. Curr. Opin. Virol. 25, 7–15 (2017).
pubmed: 28672161
pmcid: 5610638
Chandler, M. et al. Breaking and joining single-stranded DNA: the HUH endonuclease superfamily. Nat. Rev. Microbiol. 11, 525–538 (2013).
pubmed: 23832240
pmcid: 6493337
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: 30635078
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).
pubmed: 28827601
Filée, J. & Forterre, P. Viral proteins functioning in organelles: a cryptic origin? Trends Microbiol. 13, 510–513 (2005).
pubmed: 16157484