Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Perspective
  • Published:

The LUCA and its complex virome

Abstract

The last universal cellular ancestor (LUCA) is the most recent population of organisms from which all cellular life on Earth descends. The reconstruction of the genome and phenotype of the LUCA is a major challenge in evolutionary biology. Given that all life forms are associated with viruses and/or other mobile genetic elements, there is no doubt that the LUCA was a host to viruses. Here, by projecting back in time using the extant distribution of viruses across the two primary domains of life, bacteria and archaea, and tracing the evolutionary histories of some key virus genes, we attempt a reconstruction of the LUCA virome. Even a conservative version of this reconstruction suggests a remarkably complex virome that already included the main groups of extant viruses of bacteria and archaea. We further present evidence of extensive virus evolution antedating the LUCA. The presence of a highly complex virome implies the substantial genomic and pan-genomic complexity of the LUCA itself.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Distribution of known viruses across the evolutionary tree of bacteria.
Fig. 2: Distribution of known viruses across the evolutionary tree of archaea.
Fig. 3: Reconstruction of the LUCA virome from the divergence of the bacterial and archaeal viromes.
Fig. 4: Evolution of double-stranded DNA viruses antedating the LUCA.

Similar content being viewed by others

References

  1. Forterre, P. & Prangishvili, D. The great billion-year war between ribosome- and capsid-encoding organisms (cells and viruses) as the major source of evolutionary novelties. Ann. N. Y. Acad. Sci. 1178, 65–77 (2009).

    CAS  PubMed  Google Scholar 

  2. 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 

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

    CAS  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. Szathmary, E. & Demeter, L. Group selection of early replicators and the origin of life. J. Theor. Biol. 128, 463–486 (1987).

    CAS  PubMed  Google Scholar 

  8. Takeuchi, N. & Hogeweg, P. The role of complex formation and deleterious mutations for the stability of RNA-like replicator systems. J. Mol. Evol. 65, 668–686 (2007).

    CAS  PubMed  Google Scholar 

  9. Takeuchi, N. & Hogeweg, P. Evolutionary dynamics of RNA-like replicator systems: a bioinformatic approach to the origin of life. Phys. Life Rev. 9, 219–263 (2012).

    PubMed  PubMed Central  Google Scholar 

  10. Eigen, M. The origin of genetic information: viruses as models. Gene 135, 37–47 (1993).

    CAS  PubMed  Google Scholar 

  11. Eigen, M. Selforganization of matter and the evolution of biological macromolecules. Naturwissenschaften 58, 465–523 (1971).

    CAS  PubMed  Google Scholar 

  12. Baltimore, D. Expression of animal virus genomes. Bacteriol. Rev. 35, 235–241 (1971).

    CAS  PubMed  PubMed Central  Google Scholar 

  13. Koonin, E. V. et al. Global organization and proposed megataxonomy of the virus world. Microbiol. Mol. Biol. Rev. 84, e00061-19 (2020).

    PubMed  PubMed Central  Google Scholar 

  14. International Committee on Taxonomy of Viruses Executive Committee. The new scope of virus taxonomy: partitioning the virosphere into 15 hierarchical ranks. Nat. Microbiol. 5, 668–674 (2020).

    CAS  Google Scholar 

  15. Siddell, S. G. et al. Additional changes to taxonomy ratified in a special vote by the international committee on taxonomy of viruses (October 2018). Arch. Virol. 164, 943–946 (2019).

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  17. Munson-McGee, J. H., Snyder, J. C. & Young, M. J. Archaeal viruses from high-temperature environments. Genes 9, E128 (2018).

    PubMed  Google Scholar 

  18. 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 

  19. Krupovic, M., Dolja, V. V. & Koonin, E. V. Origin of viruses: primordial replicators recruiting capsids from hosts. Nat. Rev. Microbiol. 17, 449–458 (2019).

    CAS  PubMed  Google Scholar 

  20. Koonin, E. V. Comparative genomics, minimal gene-sets and the last universal common ancestor. Nat. Rev. Microbiol. 1, 127–136 (2003).

    CAS  PubMed  Google Scholar 

  21. Glansdorff, N., Xu, Y. & Labedan, B. The last universal common ancestor: emergence, constitution and genetic legacy of an elusive forerunner. Biol. Direct 3, 29 (2008).

    PubMed  PubMed Central  Google Scholar 

  22. Weiss, M. C. et al. The physiology and habitat of the last universal common ancestor. Nat. Microbiol. 1, 16116 (2016).

    CAS  PubMed  Google Scholar 

  23. Doolittle, W. F. Uprooting the tree of life. Sci. Am. 282, 90–95 (2000).

    CAS  PubMed  Google Scholar 

  24. Puigbo, P., Wolf, Y. I. & Koonin, E. V. Search for a ‘Tree of Life’ in the thicket of the phylogenetic forest. J. Biol. 8, 59 (2009).

    PubMed  PubMed Central  Google Scholar 

  25. Berkemer, S. J. & McGlynn, S. E. A new analysis of archaea-bacteria domain separation: variable phylogenetic distance and the tempo of early evolution. Mol. Biol. Evol. https://doi.org/10.1093/molbev/msaa089 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  26. Fournier, G. P., Andam, C. P. & Gogarten, J. P. Ancient horizontal gene transfer and the last common ancestors. BMC Evol. Biol. 15, 70 (2015).

    PubMed  PubMed Central  Google Scholar 

  27. Ouzounis, C. A., Kunin, V., Darzentas, N. & Goldovsky, L. A minimal estimate for the gene content of the last universal common ancestor–exobiology from a terrestrial perspective. Res. Microbiol. 157, 57–68 (2006).

    CAS  PubMed  Google Scholar 

  28. Gogarten, J. P. & Taiz, L. Evolution of proton pumping ATPases: rooting the tree of life. Photosynth. Res. 33, 137–146 (1992).

    CAS  PubMed  Google Scholar 

  29. Mirkin, B. G., Fenner, T. I., Galperin, M. Y. & Koonin, E. V. Algorithms for computing parsimonious evolutionary scenarios for genome evolution, the last universal common ancestor and dominance of horizontal gene transfer in the evolution of prokaryotes. BMC Evol. Biol. 3, 2 (2003).

    PubMed  PubMed Central  Google Scholar 

  30. Brown, J. R. & Doolittle, W. F. Archaea and the prokaryote-to-eukaryote transition. Microbiol. Mol. Biol. Rev. 61, 456–502 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  31. Leipe, D. D., Aravind, L. & Koonin, E. V. Did DNA replication evolve twice independently? Nucleic Acids Res. 27, 3389–3401 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  32. Pereto, J., Lopez-Garcia, P. & Moreira, D. Ancestral lipid biosynthesis and early membrane evolution. Trends Biochem. Sci. 29, 469–477 (2004).

    CAS  PubMed  Google Scholar 

  33. Lombard, J., Lopez-Garcia, P. & Moreira, D. The early evolution of lipid membranes and the three domains of life. Nat. Rev. Microbiol. 10, 507–515 (2012).

    CAS  PubMed  Google Scholar 

  34. Mushegian, A. R. & Koonin, E. V. A minimal gene set for cellular life derived by comparison of complete bacterial genomes. Proc. Natl Acad. Sci. USA 93, 10268–10273 (1996).

    CAS  PubMed  PubMed Central  Google Scholar 

  35. 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  PubMed Central  Google Scholar 

  36. Raia, P. et al. Structure of the DP1-DP2 PolD complex bound with DNA and its implications for the evolutionary history of DNA and RNA polymerases. PLoS Biol. 17, e3000122 (2019).

    PubMed  PubMed Central  Google Scholar 

  37. Sauguet, L. The extended “two-barrel” polymerases superfamily: structure, function and evolution. J. Mol. Biol. 431, 4167–4183 (2019).

    CAS  PubMed  Google Scholar 

  38. Koonin, E. V., Krupovic, M., Ishino, S. & Ishino, Y. The replication machinery of LUCA: common origin of DNA replication and transcription. BMC Biol. 18, 61 (2020).

    CAS  PubMed  PubMed Central  Google Scholar 

  39. Werner, F. & Grohmann, D. Evolution of multisubunit RNA polymerases in the three domains of life. Nat. Rev. Microbiol. 9, 85–98 (2011).

    CAS  PubMed  Google Scholar 

  40. Martin, W. & Russell, M. J. On the origins of cells: a hypothesis for the evolutionary transitions from abiotic geochemistry to chemoautotrophic prokaryotes, and from prokaryotes to nucleated cells. Philos. Trans. R. Soc. Lond. B Biol. Sci. 358, 59–83 (2003).

    CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  42. Mulkidjanian, A. Y., Galperin, M. Y. & Koonin, E. V. Co-evolution of primordial membranes and membrane proteins. Trends Biochem. Sci. 34, 206–215 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  43. Villanueva, L. et al. Bridging the divide: bacteria synthesizing archaeal membrane lipids. Preprint at bioRxiv https://doi.org/10.1101/448035 (2018).

    Article  Google Scholar 

  44. Caforio, A. et al. Converting Escherichia coli into an archaebacterium with a hybrid heterochiral membrane. Proc. Natl Acad. Sci. USA 115, 3704–3709 (2018).

    CAS  PubMed  PubMed Central  Google Scholar 

  45. Rajagopal, M. & Walker, S. Envelope structures of gram-positive bacteria. Curr. Top. Microbiol. Immunol. 404, 1–44 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  46. Auer, G. K. & Weibel, D. B. Bacterial cell mechanics. Biochemistry 56, 3710–3724 (2017).

    CAS  PubMed  Google Scholar 

  47. Sleytr, U. B., Schuster, B., Egelseer, E. M. & Pum, D. S-layers: principles and applications. FEMS Microbiol. Rev. 38, 823–864 (2014).

    CAS  PubMed  Google Scholar 

  48. Vernikos, G., Medini, D., Riley, D. R. & Tettelin, H. Ten years of pan-genome analyses. Curr. Opin. Microbiol. 23, 148–154 (2015).

    CAS  PubMed  Google Scholar 

  49. Medini, D., Donati, C., Tettelin, H., Masignani, V. & Rappuoli, R. The microbial pan-genome. Curr. Opin. Genet. Dev. 15, 589–594 (2005).

    CAS  PubMed  Google Scholar 

  50. Puigbo, P., Lobkovsky, A. E., Kristensen, D. M., Wolf, Y. I. & Koonin, E. V. Genomes in turmoil: quantification of genome dynamics in prokaryote supergenomes. BMC Biol. 12, 66 (2014).

    PubMed  PubMed Central  Google Scholar 

  51. Parks, D. H. et al. A standardized bacterial taxonomy based on genome phylogeny substantially revises the tree of life. Nat. Biotechnol. 36, 996–1004 (2018).

    CAS  PubMed  Google Scholar 

  52. Embley, T. M. & Martin, W. Eukaryotic evolution, changes and challenges. Nature 440, 623–630 (2006).

    CAS  PubMed  Google Scholar 

  53. Kristensen, D. M., Cai, X. & Mushegian, A. Evolutionarily conserved orthologous families in phages are relatively rare in their prokaryotic hosts. J. Bacteriol. 193, 1806–1814 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  54. Iranzo, J., Krupovic, M. & Koonin, E. V. The double-stranded DNA virosphere as a modular hierarchical network of gene sharing. mBio 7, e00978-16 (2016).

    PubMed  PubMed Central  Google Scholar 

  55. Duda, R. L. & Teschke, C. M. The amazing HK97 fold: versatile results of modest differences. Curr. Opin. Virol. 36, 9–16 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  56. Krupovic, M., Forterre, P. & Bamford, D. H. Comparative analysis of the mosaic genomes of tailed archaeal viruses and proviruses suggests common themes for virion architecture and assembly with tailed viruses of bacteria. J. Mol. Biol. 397, 144–160 (2010).

    CAS  PubMed  Google Scholar 

  57. Sencilo, A. et al. Snapshot of haloarchaeal tailed virus genomes. RNA Biol. 10, 803–816 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  58. Cheng, H., Shen, N., Pei, J. & Grishin, N. V. Double-stranded DNA bacteriophage prohead protease is homologous to herpesvirus protease. Protein Sci. 13, 2260–2269 (2004).

    CAS  PubMed  PubMed Central  Google Scholar 

  59. Low, S. J., Dzunkova, M., Chaumeil, P. A., Parks, D. H. & Hugenholtz, P. Evaluation of a concatenated protein phylogeny for classification of tailed double-stranded DNA viruses belonging to the order Caudovirales. Nat. Microbiol. 4, 1306–1315 (2019).

    CAS  PubMed  Google Scholar 

  60. Dion, M. B., Oechslin, F. & Moineau, S. Phage diversity, genomics and phylogeny. Nat. Rev. Microbiol. 18, 125–138 (2020).

    CAS  PubMed  Google Scholar 

  61. Philosof, A. et al. Novel abundant oceanic viruses of uncultured marine group II euryarchaeota. Curr. Biol. 27, 1362–1368 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  62. 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 

  63. Yutin, N., Bäckström, 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 

  64. 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 

  65. Krupovic, M. & Bamford, D. H. Archaeal proviruses TKV4 and MVV extend the PRD1-adenovirus lineage to the phylum euryarchaeota. Virology 375, 292–300 (2008).

    CAS  PubMed  Google Scholar 

  66. Krupovic, M. et al. Integrated mobile genetic elements in Thaumarchaeota. Env. Microbiol. 21, 2056–2078 (2019).

    CAS  Google Scholar 

  67. Jalasvuori, M. & Koskinen, K. Extending the hosts of Tectiviridae into four additional genera of Gram-positive bacteria and more diverse Bacillus species. Virology 518, 136–142 (2018).

    CAS  PubMed  Google Scholar 

  68. Roux, S. et al. Cryptic inoviruses revealed as pervasive in bacteria and archaea across earth’s biomes. Nat. Microbiol. 4, 1895–1906 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  69. Roux, S., Krupovic, M., Poulet, A., Debroas, D. & Enault, F. Evolution and diversity of the microviridae viral family through a collection of 81 new complete genomes assembled from virome reads. PLoS One 7, e40418 (2012).

    PubMed  PubMed Central  Google Scholar 

  70. Creasy, A., Rosario, K., Leigh, B. A., Dishaw, L. J. & Breitbart, M. Unprecedented diversity of ssDNA phages from the family Microviridae detected within the gut of a protochordate model organism (Ciona robusta). Viruses 10, 404 (2018).

    PubMed Central  Google Scholar 

  71. Tisza, M. J. et al. Discovery of several thousand highly diverse circular DNA viruses. eLife 9, e51971 (2020).

    CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  73. Wolf, Y. I. et al. Origins and evolution of the global RNA virome. mBio 9, e02329-18 (2018).

    PubMed  PubMed Central  Google Scholar 

  74. Krishnamurthy, S. R., Janowski, A. B., Zhao, G., Barouch, D. & Wang, D. Hyperexpansion of RNA bacteriophage diversity. PLoS Biol. 14, e1002409 (2016).

    PubMed  PubMed Central  Google Scholar 

  75. Callanan, J. et al. Expansion of known ssRNA phage genomes: from tens to over a thousand. Sci. Adv. 6, eaay5981 (2020).

    CAS  PubMed  PubMed Central  Google Scholar 

  76. 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  PubMed Central  Google Scholar 

  77. Zimmerly, S. & Wu, L. An unexplored diversity of reverse transcriptases in bacteria. Microbiol. Spectr. 3, MDNA3-0058-2014 https://doi.org/10.1128/microbiolspec.MDNA3-0058-2014 (2015).

  78. Gilbert, W. The origin of life: the RNA world. Nature 319, 618 (1986).

    Google Scholar 

  79. Joyce, G. F. The antiquity of RNA-based evolution. Nature 418, 214–221 (2002).

    CAS  PubMed  Google Scholar 

  80. Bernhardt, H. S. The RNA world hypothesis: the worst theory of the early evolution of life (except for all the others)(a). Biol. Direct 7, 23 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  81. Catchpole, R. J. & Forterre, P. The evolution of reverse gyrase suggests a nonhyperthermophilic last universal common ancestor. Mol. Biol. Evol. 36, 2737–2747 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  82. Cantine, M. D. & Fournier, G. P. Environmental adaptation from the origin of life to the last universal common ancestor. Orig. Life Evol. Biosph. 48, 35–54 (2018).

    PubMed  Google Scholar 

  83. Boussau, B., Blanquart, S., Necsulea, A., Lartillot, N. & Gouy, M. Parallel adaptations to high temperatures in the Archaean eon. Nature 456, 942–945 (2008).

    CAS  PubMed  Google Scholar 

  84. Groussin, M. & Gouy, M. Adaptation to environmental temperature is a major determinant of molecular evolutionary rates in archaea. Mol. Biol. Evol. 28, 2661–2674 (2011).

    CAS  PubMed  Google Scholar 

  85. Forterre, P. The common ancestor of archaea and eukarya was not an archaeon. Archaea 2013, 372396 (2013).

    PubMed  PubMed Central  Google Scholar 

  86. Krupovic, M., Quemin, E. R., Bamford, D. H., Forterre, P. & Prangishvili, D. Unification of the globally distributed spindle-shaped viruses of the Archaea. J. Virol. 88, 2354–2358 (2014).

    PubMed  PubMed Central  Google Scholar 

  87. 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  PubMed Central  Google Scholar 

  88. 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 

  89. De Colibus, L. et al. Assembly of complex viruses exemplified by a halophilic euryarchaeal virus. Nat. Commun. 10, 1456 (2019).

    PubMed  PubMed Central  Google Scholar 

  90. 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 

  91. Liu, Y. et al. A novel type of polyhedral viruses infecting hyperthermophilic archaea. J. Virol. 91, e00589-17 (2017).

    PubMed  PubMed Central  Google Scholar 

  92. Wang, F. et al. A packing for A-form DNA in an icosahedral virus. Proc. Natl Acad. Sci. USA 116, 22591–22597 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  93. Kelley, L. L. et al. Structure of the hypothetical protein PF0899 from pyrococcus furiosus at 1.85 a resolution. Acta Crystallogr. Sect. F. Struct. Biol. Cryst. Commun. 63, 549–552 (2007).

    PubMed  Google Scholar 

  94. Holm, L. DALI and the persistence of protein shape. Protein Sci. 29, 128–140 (2020).

    CAS  PubMed  Google Scholar 

  95. Grininger, M., Zeth, K. & Oesterhelt, D. Dodecins: a family of lumichrome binding proteins. J. Mol. Biol. 357, 842–857 (2006).

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  97. Ilyina, T. V. & Koonin, E. V. Conserved sequence motifs in the initiator proteins for rolling circle DNA replication encoded by diverse replicons from eubacteria, eucaryotes and archaebacteria. Nucleic Acids Res. 20, 3279–3285 (1992).

    CAS  PubMed  PubMed Central  Google Scholar 

  98. Kazlauskas, D., Varsani, A., Koonin, E. V. & Krupovic, M. Multiple origins of prokaryotic and eukaryotic single-stranded DNA viruses from bacterial and archaeal plasmids. Nat. Commun. 10, 3425 (2019).

    PubMed  PubMed Central  Google Scholar 

  99. Redrejo-Rodríguez, M. et al. Primer-independent DNA synthesis by a family B DNA polymerase from self-replicating mobile genetic elements. Cell Rep. 21, 1574–1587 (2017).

    PubMed  PubMed Central  Google Scholar 

  100. Kim, J. G. et al. Spindle-shaped viruses infect marine ammonia-oxidizing thaumarchaea. Proc. Natl Acad. Sci. USA 116, 15645–15650 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  101. 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 

  102. 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 

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

    CAS  PubMed  Google Scholar 

  104. Brezellec, P. et al. Domestication of lambda phage genes into a putative third type of replicative helicase matchmaker. Genome Biol. Evol. 9, 1561–1566 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  105. Pfister, P., Wasserfallen, A., Stettler, R. & Leisinger, T. Molecular analysis of methanobacterium phage psiM2. Mol. Microbiol. 30, 233–244 (1998).

    CAS  PubMed  Google Scholar 

  106. Iro, M. et al. The lysogenic region of virus phiCh1: identification of a repressor-operator system and determination of its activity in halophilic Archaea. Extremophiles 11, 383–396 (2007).

    CAS  PubMed  Google Scholar 

  107. Dellas, N., Snyder, J. C., Bolduc, B. & Young, M. J. Archaeal viruses: diversity, replication, and structure. Annu. Rev. Virol. 1, 399–426 (2014).

    PubMed  Google Scholar 

  108. Zhaxybayeva, O. & Gogarten, J. P. Cladogenesis, coalescence and the evolution of the three domains of life. Trends Genet. 20, 182–187 (2004).

    CAS  PubMed  Google Scholar 

  109. Mendler, K. et al. AnnoTree: visualization and exploration of a functionally annotated microbial tree of life. Nucleic Acids Res. 47, 4442–4448 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  110. Roux, S., Hallam, S. J., Woyke, T. & Sullivan, M. B. Viral dark matter and virus-host interactions resolved from publicly available microbial genomes. eLife 4, e08490 (2015).

    PubMed Central  Google Scholar 

  111. Krupovic, M. & Bamford, D. H. Putative prophages related to lytic tailless marine dsDNA phage PM2 are widespread in the genomes of aquatic bacteria. BMC Genomics 8, 236 (2007).

    PubMed  PubMed Central  Google Scholar 

  112. Pawlowski, A., Rissanen, I., Bamford, J. K., Krupovic, M. & Jalasvuori, M. Gammasphaerolipovirus, a newly proposed bacteriophage genus, unifies viruses of halophilic archaea and thermophilic bacteria within the novel family Sphaerolipoviridae. Arch. Virol. 159, 1541–1554 (2014).

    CAS  PubMed  Google Scholar 

  113. Wang, F. et al. Structure of a filamentous virus uncovers familial ties within the archaeal virosphere. Virus Evol. 6, veaa023 (2020).

    PubMed  PubMed Central  Google Scholar 

  114. Weidenbach, K. et al. Methanosarcina spherical virus, a novel archaeal lytic virus targeting methanosarcina strains. J. Virol. 91, e00955-17 (2017).

    PubMed  PubMed Central  Google Scholar 

  115. Liu, Y. et al. Identification and characterization of SNJ2, the first temperate pleolipovirus integrating into the genome of the SNJ1-lysogenic archaeal strain. Mol. Microbiol. 98, 1002–1020 (2015).

    CAS  PubMed  Google Scholar 

  116. Wang, J. et al. A novel family of tyrosine integrases encoded by the temperate pleolipovirus SNJ2. Nucleic Acids Res. 46, 2521–2536 (2018).

    CAS  PubMed  PubMed Central  Google Scholar 

  117. Altschul, S. F. et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25, 3389–3402 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

E.V.K. is supported by the funds of the Intramural Research Program of the National Institutes of Health of the USA. M.K. was supported by l’Agence Nationale de la Recherche grant ANR-17-CE15-0005-01.

Author information

Authors and Affiliations

Authors

Contributions

M.K. and E.V.K. researched data for article. M.K., V.V.D. and E.V.K. substantially contributed to discussion of content. M.K. and E.V.K. wrote the manuscript. M.K., V.V.D. and E.V.K. reviewed and edited the manuscript before submission.

Corresponding authors

Correspondence to Mart Krupovic or Eugene V. Koonin.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Peer review information

Nature Reviews Microbiology thanks J. P. Gogarten, P. López-García and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Krupovic, M., Dolja, V.V. & Koonin, E.V. The LUCA and its complex virome. Nat Rev Microbiol 18, 661–670 (2020). https://doi.org/10.1038/s41579-020-0408-x

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41579-020-0408-x

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing