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  • Review Article
  • Published:

The enigmatic archaeal virosphere

Nature Reviews Microbiology volume 15, pages 724–739 (2017)Cite this article

Subjects

Key Points

  • Crenarchaeal viruses display a remarkable diversity of unexpected, complex morphologies and have genomes with largely unique content.

  • The known viruses of extremely halophilic and methanogenic archaea include some morphologies of crenarchaeal viruses and all known morphologies of bacterial dsDNA viruses.

  • Archaeal viruses display many unique features that have thus far not been observed elsewhere in nature, including A-form DNA in viral particles, virion envelopes containing lipids in a horseshoe conformation and special gateway structures for virion release.

  • Certain aspects of the virus–host interaction in archaea, such as release of enveloped virions by budding, resemble mechanisms that are employed by eukaryotic enveloped viruses.

  • Archaeal viruses have a major role in the ocean sediments by killing their hosts, which results in the release of ∼0.3 to 0.5 gigatonnes of carbon per year globally.

  • Comparative genomics analyses revealed close evolutionary relationships between archaeal viruses and capsidless mobile genetic elements.

Abstract

One of the most prominent features of archaea is the extraordinary diversity of their DNA viruses. Many archaeal viruses differ substantially in morphology from bacterial and eukaryotic viruses and represent unique virus families. The distinct nature of archaeal viruses also extends to the gene composition and architectures of their genomes and the properties of the proteins that they encode. Environmental research has revealed prominent roles of archaeal viruses in influencing microbial communities in ocean ecosystems, and recent metagenomic studies have uncovered new groups of archaeal viruses that infect extremophiles and mesophiles in diverse habitats. In this Review, we summarize recent advances in our understanding of the genomic and morphological diversity of archaeal viruses and the molecular biology of their life cycles and virus–host interactions, including interactions with archaeal CRISPR–Cas systems. We also examine the potential origins and evolution of archaeal viruses and discuss their place in the global virosphere.

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Figure 1: Electron micrographs of archaeal viruses.
Figure 2: Major capsid proteins of cosmopolitan archaeal viruses.
Figure 3: Virion organization of filamentous viruses SIRV2 and AFV1.
Figure 4: Life cycles of lytic and temperate archaeal viruses.
Figure 5: Schematic representation of the gene-sharing network among different families of archaeal viruses.

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References

  1. Woese, C. R. & Fox, G. E. Phylogenetic structure of the prokaryotic domain: the primary kingdoms. Proc. Natl Acad. Sci. USA 74, 5088–5090 (1977).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Hug, L. A. et al. A new view of the tree of life. Nat. Microbiol. 1, 16048 (2016).

    Article  CAS  PubMed  Google Scholar 

  3. Lurie-Weinberger, M. N. & Gophna, U. Archaea in and on the human body: health implications and future directions. PLoS Pathog. 11, e1004833 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Lloyd, K. G., May, M. K., Kevorkian, R. T. & Steen, A. D. Meta-analysis of quantification methods shows that archaea and bacteria have similar abundances in the subseafloor. Appl. Environ. Microbiol. 79, 7790–7799 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Karner, M. B., DeLong, E. F. & Karl, D. M. Archaeal dominance in the mesopelagic zone of the Pacific Ocean. Nature 409, 507–510 (2001).

    Article  CAS  PubMed  Google Scholar 

  6. Offre, P., Spang, A. & Schleper, C. Archaea in biogeochemical cycles. Annu. Rev. Microbiol. 67, 437–457 (2013).

    Article  CAS  PubMed  Google Scholar 

  7. Lloyd, K. G. et al. Predominant archaea in marine sediments degrade detrital proteins. Nature 496, 215–218 (2013).

    Article  CAS  PubMed  Google Scholar 

  8. Takano, Y. et al. Sedimentary membrane lipids recycled by deep-sea benthic archaea. Nat. Geosci. 3, 858–861 (2010).

    Article  CAS  Google Scholar 

  9. Roux, S. et al. Ecogenomics and potential biogeochemical impacts of globally abundant ocean viruses. Nature 537, 689–693 (2016). This study suggests a global impact of archaeal viruses in the epipelagic and mesopelagic ocean.

    Article  CAS  PubMed  Google Scholar 

  10. Danovaro, R. et al. Virus-mediated archaeal hecatomb in the deep seafloor. Sci. Adv. 2, e1600492 (2016). This study shows that archaeal viruses have a profound role in the functioning of deep-sea ecosystems and in global biogeochemical cycles.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Mochizuki, T. et al. Diversity of viruses of the hyperthermophilic archaeal genus Aeropyrum, and isolation of the Aeropyrum pernix bacilliform virus 1, APBV1, the first representative of the family Clavaviridae. Virology 402, 347–354 (2010).

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  14. Häring, M., Rachel, R., Peng, X., Garrett, R. A. & Prangishvili, D. Viral diversity in hot springs of Pozzuoli, Italy, and characterization of a unique archaeal virus. Acidianus bottle-shaped virus, from a new family, the Ampullaviridae. J. Virol. 79, 9904–9911 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Mochizuki, T. et al. Archaeal virus with exceptional virion architecture and the largest single-stranded DNA genome. Proc. Natl Acad. Sci. USA 109, 13386–13391 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. 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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Redder, P. et al. Four newly isolated fuselloviruses from extreme geothermal environments reveal unusual morphologies and a possible interviral recombination mechanism. Environ. Microbiol. 11, 2849–2862 (2009).

    Article  CAS  PubMed  Google Scholar 

  18. Häring, M. et al. Virology: independent virus development outside a host. Nature 436, 1101–1102 (2005).

    Article  CAS  PubMed  Google Scholar 

  19. Hochstein, R. A., Amenabar, M. J., Munson-McGee, J. H., Boyd, E. S. & Young, M. J. Acidianus tailed spindle virus: a new archaeal large tailed spindle virus discovered by culture-independent methods. J. Virol. 90, 3458–3468 (2016). A new spindle-shaped virus and its host are characterized using culture-independent techniques.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Xiang, X. et al. Sulfolobus tengchongensis spindle-shaped virus STSV1: virus-host interactions and genomic features. J. Virol. 79, 8677–8686 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Uldahl, K. B. et al. Life cycle characterization of Sulfolobus monocaudavirus 1, an extremophilic spindle-shaped virus with extracellular tail development. J. Virol. 90, 5693–5699 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Erdmann, S. et al. A novel single-tailed fusiform Sulfolobus virus STSV2 infecting model Sulfolobus species. Extremophiles 18, 51–60 (2014).

    Article  CAS  PubMed  Google Scholar 

  23. Erdmann, S., Le Moine Bauer, S. & Garrett, R. A. Inter-viral conflicts that exploit host CRISPR immune systems of Sulfolobus. Mol. Microbiol. 91, 900–917 (2014).

    Article  CAS  PubMed  Google Scholar 

  24. Prangishvili, D. The wonderful world of archaeal viruses. Annu. Rev. Microbiol. 67, 565–585 (2013).

    Article  CAS  PubMed  Google Scholar 

  25. Prangishvili, D. et al. Structural and genomic properties of the hyperthermophilic archaeal virus ATV with an extracellular stage of the reproductive cycle. J. Mol. Biol. 359, 1203–1216 (2006).

    Article  CAS  PubMed  Google Scholar 

  26. Arnold, H. P., Ziese, U. & Zillig, W. SNDV, a novel virus of the extremely thermophilic and acidophilic archaeon Sulfolobus. Virology 272, 409–416 (2000).

    Article  CAS  PubMed  Google Scholar 

  27. Mochizuki, T., Sako, Y. & Prangishvili, D. Provirus induction in hyperthermophilic archaea: characterization of Aeropyrum pernix spindle-shaped virus 1 and Aeropyrum pernix ovoid virus 1. J. Bacteriol. 193, 5412–5419 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. 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). Comprehensive bipartite network analysis of all known archaeal virus genomes reveals evolutionary connections between different groups of viruses as well as non-viral mobile genetic elements.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Prangishvili, D. et al. A novel virus family, the Rudiviridae: Structure, virus-host interactions and genome variability of the sulfolobus viruses SIRV1 and SIRV2. Genetics 152, 1387–1396 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  30. Vestergaard, G. et al. A novel rudivirus, ARV1, of the hyperthermophilic archaeal genus Acidianus. Virology 336, 83–92 (2005).

    Article  CAS  PubMed  Google Scholar 

  31. Vestergaard, G. et al. Stygiolobus rod-shaped virus and the interplay of crenarchaeal rudiviruses with the CRISPR antiviral system. J. Bacteriol. 190, 6837–6845 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Prangishvili, D., Koonin, E. V. & Krupovic, M. Genomics and biology of Rudiviruses, a model for the study of virus-host interactions in Archaea. Biochem. Soc. Trans. 41, 443–450 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. DiMaio, F. et al. A virus that infects a hyperthermophile encapsidates A-form DNA. Science 348, 914–917 (2015). Near-atomic-resolution structure of the rod-shaped archaeal virus reveals the A-form of DNA in a biological entity and provides clues about the thermostability of the viral particle.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Goulet, A. et al. Acidianus filamentous virus 1 coat proteins display a helical fold spanning the filamentous archaeal viruses lineage. Proc. Natl Acad. Sci. USA 106, 21155–21160 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Szymczyna, B. R. et al. Synergy of NMR, computation, and X-ray crystallography for structural biology. Structure 17, 499–507 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Pina, M., Bize, A., Forterre, P. & Prangishvili, D. The archeoviruses. FEMS Microbiol. Rev. 35, 1035–1054 (2011).

    Article  CAS  PubMed  Google Scholar 

  37. Prangishvili, D. & Krupovic, M. A new proposed taxon for double-stranded DNA viruses, the order “Ligamenvirales”. Arch. Virol. 157, 791–795 (2012).

    Article  CAS  PubMed  Google Scholar 

  38. Rensen, E. I. et al. A virus of hyperthermophilic archaea with a unique architecture among DNA viruses. Proc. Natl Acad. Sci. USA 113, 2478–2483 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Liu, Y. et al. A novel type of polyhedral viruses infecting hyperthermophilic archaea. J. Virol. 91, e00589–e00517 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  40. Pietilä, M. K., Roine, E., Sencilo, A., Bamford, D. H. & Oksanen, H. M. Pleolipoviridae, a newly proposed family comprising archaeal pleomorphic viruses with single-stranded or double-stranded DNA genomes. Arch. Virol. 161, 249–256 (2016).

    Article  CAS  PubMed  Google Scholar 

  41. Pietilä, M. K. et al. Virion architecture unifies globally distributed pleolipoviruses infecting halophilic archaea. J. Virol. 86, 5067–5079 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Pietilä, M. K., Laurinavicius, S., Sund, J., Roine, E. & Bamford, D. H. The single-stranded DNA genome of novel archaeal virus Halorubrum pleomorphic virus 1 is enclosed in the envelope decorated with glycoprotein spikes. J. Virol. 84, 788–798 (2010).

    Article  CAS  PubMed  Google Scholar 

  43. Roine, E. et al. New, closely related haloarchaeal viral elements with different nucleic acid types. J. Virol. 84, 3682–3689 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Pietilä, M. K., Roine, E., Paulin, L., Kalkkinen, N. & Bamford, D. H. An ssDNA virus infecting archaea: a new lineage of viruses with a membrane envelope. Mol. Microbiol. 72, 307–319 (2009).

    Article  CAS  PubMed  Google Scholar 

  45. Sencilo, A., Paulin, L., Kellner, S., Helm, M. & Roine, E. Related haloarchaeal pleomorphic viruses contain different genome types. Nucleic Acids Res. 40, 5523–5534 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Ackermann, H. W. & Prangishvili, D. Prokaryote viruses studied by electron microscopy. Arch. Virol. 157, 1843–1849 (2012).

    Article  CAS  PubMed  Google Scholar 

  47. Pietilä, M. K., Demina, T. A., Atanasova, N. S., Oksanen, H. M. & Bamford, D. H. Archaeal viruses and bacteriophages: comparisons and contrasts. Trends Microbiol. 22, 334–344 (2014).

    Article  CAS  PubMed  Google Scholar 

  48. Krupovic, M., Prangishvili, D., Hendrix, R. W. & Bamford, D. H. Genomics of bacterial and archaeal viruses: dynamics within the prokaryotic virosphere. Microbiol. Mol. Biol. Rev. 75, 610–635 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  49. Pietilä, M. K. et al. Insights into head-tailed viruses infecting extremely halophilic archaea. J. Virol. 87, 3248–3260 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Pietilä, M. K. et al. Structure of the archaeal head-tailed virus HSTV-1 completes the HK97 fold story. Proc. Natl Acad. Sci. USA 110, 10604–10609 (2013). Cryo-EM reconstruction of the archaeal podovirus HSTV-1 capsid reveals a major capsid protein fold found in tailed bacteriophages and eukaryotic herpesviruses.

    Article  PubMed  PubMed Central  Google Scholar 

  51. Pfister, P., Wasserfallen, A., Stettler, R. & Leisinger, T. Molecular analysis of Methanobacterium phage ψM2. Mol. Microbiol. 30, 233–244 (1998).

    Article  CAS  PubMed  Google Scholar 

  52. 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).

    Article  CAS  PubMed  Google Scholar 

  53. Krupovic, M., Spang, A., Gribaldo, S., Forterre, P. & Schleper, C. A thaumarchaeal provirus testifies for an ancient association of tailed viruses with archaea. Biochem. Soc. Trans. 39, 82–88 (2011).

    Article  CAS  PubMed  Google Scholar 

  54. 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).

    Article  CAS  PubMed  Google Scholar 

  55. Veesler, D. et al. Atomic structure of the 75 MDa extremophile Sulfolobus turreted icosahedral virus determined by CryoEM and X-ray crystallography. Proc. Natl Acad. Sci. USA 110, 5504–5509 (2013). Near-atomic-resolution structure of the turrivirus STIV reveals fine details of the virion organization and strengthens the evolutionary connection between STIV and bacterial and eukaryotic viruses with double jelly-roll capsid proteins.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Demina, T. A. et al. HCIV-1 and other tailless icosahedral internal membrane-containing viruses of the family Sphaerolipoviridae. Viruses 9, 32 (2017).

    Article  CAS  PubMed Central  Google Scholar 

  57. Khayat, R. et al. Structure of an archaeal virus capsid protein reveals a common ancestry to eukaryotic and bacterial viruses. Proc. Natl Acad. Sci. USA 102, 18944–18949 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. 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).

    Article  CAS  PubMed  Google Scholar 

  59. Suhanovsky, M. M. & Teschke, C. M. Nature's favorite building block: deciphering folding and capsid assembly of proteins with the HK97-fold. Virology 479–480, 487–497 (2015).

  60. Baker, M. L., Jiang, W., Rixon, F. J. & Chiu, W. Common ancestry of herpesviruses and tailed DNA bacteriophages. J. Virol. 79, 14967–14970 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Yu, X., Jih, J., Jiang, J. & Zhou, Z. H. Atomic structure of the human cytomegalovirus capsid with its securing tegument layer of pp150. Science 356, eaam6892 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Krupovic, M. & Bamford, D. H. Virus evolution: how far does the double beta-barrel viral lineage extend? Nat. Rev. Microbiol. 6, 941–948 (2008).

    Article  CAS  PubMed  Google Scholar 

  64. Sinclair, R. M., Ravantti, J. J. & Bamford, D. H. Nucleic and amino acid sequences support structure-based viral classification. J. Virol. 91, e02275-16 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  65. Jäälinoja, H. T. et al. Structure and host-cell interaction of SH1, a membrane-containing, halophilic euryarchaeal virus. Proc. Natl Acad. Sci. USA 105, 8008–8013 (2008).

    Article  PubMed  PubMed Central  Google Scholar 

  66. Gil-Carton, D. et al. Insight into the assembly of viruses with vertical single β-barrel major capsid proteins. Structure 23, 1866–1877 (2015).

    Article  CAS  PubMed  Google Scholar 

  67. 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).

    Article  PubMed  PubMed Central  Google Scholar 

  68. Strömsten, N. J., Bamford, D. H. & Bamford, J. K. In vitro DNA packaging of PRD1: a common mechanism for internal-membrane viruses. J. Mol. Biol. 348, 617–629 (2005).

    Article  CAS  PubMed  Google Scholar 

  69. Kasson, P. et al. Model for a novel membrane envelope in a filamentous hyperthermophilic virus. eLife 6, e26268 (2017). Near-atomic-resolution structure of an enveloped virion of archaeal virus AFV1 reveals novel membrane organization not previously observed in viruses or cellular organisms.

    Article  PubMed  PubMed Central  Google Scholar 

  70. Valentine, D. L. Adaptations to energy stress dictate the ecology and evolution of the Archaea. Nat. Rev. Microbiol. 5, 316–323 (2007).

    Article  CAS  PubMed  Google Scholar 

  71. Quemin, E. R. et al. Eukaryotic-like virus budding in Archaea. mBio 7, e01439-16 (2016). This electron-tomography study shows that enveloped, spindle-shaped viruses of archaea are released from the cell by a budding mechanism highly reminiscent of that used by many enveloped eukaryotic viruses, such as HIV and influenza virus.

    Article  PubMed  PubMed Central  Google Scholar 

  72. Quemin, E. R. et al. Sulfolobus spindle-shaped virus 1 contains glycosylated capsid proteins, a cellular chromatin protein, and host-derived lipids. J. Virol. 89, 11681–11691 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Kristensen, D. M., Saeed, U., Frishman, D. & Koonin, E. V. A census of α-helical membrane proteins in double-stranded DNA viruses infecting bacteria and archaea. BMC Bioinformatics 16, 380 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  74. Bath, C., Cukalac, T., Porter, K. & Dyall-Smith, M. L. His1 and His2 are distantly related, spindle-shaped haloviruses belonging to the novel virus group, Salterprovirus. Virology 350, 228–239 (2006).

    Article  CAS  PubMed  Google Scholar 

  75. Martin, A. et al. SAV 1, a temperate u.v.-inducible DNA virus-like particle from the archaebacterium Sulfolobus acidocaldarius isolate B12. EMBO J. 3, 2165–2168 (1984).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Hong, C. et al. Lemon-shaped halo archaeal virus His1 with uniform tail but variable capsid structure. Proc. Natl Acad. Sci. USA 112, 2449–2454 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Stedman, K. M., DeYoung, M., Saha, M., Sherman, M. B. & Morais, M. C. Structural insights into the architecture of the hyperthermophilic Fusellovirus SSV1. Virology 474, 105–109 (2015). This work and the one in REF 76 present cryo-EM reconstructions of spindle-shaped archaeal viruses that are hyperthermophilic and hyperhalophilic, respectively.

    Article  CAS  PubMed  Google Scholar 

  78. Bettstetter, M., Peng, X., Garrett, R. A. & Prangishvili, D. AFV1, a novel virus infecting hyperthermophilic archaea of the genus acidianus. Virology 315, 68–79 (2003).

    Article  CAS  PubMed  Google Scholar 

  79. Quemin, E. R. et al. First insights into the entry process of hyperthermophilic archaeal viruses. J. Virol. 87, 13379–13385 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Deng, L. et al. Unveiling cell surface and type IV secretion proteins responsible for archaeal rudivirus entry. J. Virol. 88, 10264–10268 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Klein, R., Rossler, N., Iro, M., Scholz, H. & Witte, A. Haloarchaeal myovirus φCh1 harbours a phase variation system for the production of protein variants with distinct cell surface adhesion specificities. Mol. Microbiol. 83, 137–150 (2012).

    Article  CAS  PubMed  Google Scholar 

  82. Krupovic, M., Gribaldo, S., Bamford, D. H. & Forterre, P. The evolutionary history of archaeal MCM helicases: a case study of vertical evolution combined with hitchhiking of mobile genetic elements. Mol. Biol. Evol. 27, 2716–2732 (2010).

    Article  CAS  PubMed  Google Scholar 

  83. Peng, X., Basta, T., Haring, M., Garrett, R. A. & Prangishvili, D. Genome of the Acidianus bottle-shaped virus and insights into the replication and packaging mechanisms. Virology 364, 237–243 (2007).

    Article  CAS  PubMed  Google Scholar 

  84. Wang, Y. et al. Identification, characterization, and application of the replicon region of the halophilic temperate sphaerolipovirus SNJ1. J. Bacteriol. 198, 1952–1964 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Pina, M. et al. Unique genome replication mechanism of the archaeal virus AFV1. Mol. Microbiol. 92, 1313–1325 (2014).

    Article  CAS  PubMed  Google Scholar 

  88. Martinez-Alvarez, L., Deng, L. & Peng, X. Formation of a viral replication focus in Sulfolobus cells infected by the rudivirus Sulfolobus islandicus rod-shaped virus 2. J. Virol. 91, e00486-17 (2017). This study shows that genome replication of the rod-shaped virus SIRV2 is confined to discrete foci in the cytoplasm, where the host DNA polymerase and viral replication factors are recruited.

    Article  PubMed  PubMed Central  Google Scholar 

  89. Peeters, E. et al. DNA-interacting characteristics of the archaeal rudiviral protein SIRV2_Gp1. Viruses 9, 190 (2017).

    Article  CAS  PubMed Central  Google Scholar 

  90. Gardner, A. F., Bell, S. D., White, M. F., Prangishvili, D. & Krupovic, M. Protein-protein interactions leading to recruitment of the host DNA sliding clamp by the hyperthermophilic Sulfolobus islandicus rod-shaped virus 2. J. Virol. 88, 7105–7108 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Martinez-Alvarez, L., Bell, S. D. & Peng, X. Multiple consecutive initiation of replication producing novel brush-like intermediates at the termini of linear viral dsDNA genomes with hairpin ends. Nucleic Acids Res. 44, 8799–8809 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Dellas, N. et al. Structure-based mutagenesis of Sulfolobus turreted icosahedral virus B204 reveals essential residues in the virion-associated DNA-packaging ATPase. J. Virol. 90, 2729–2739 (2015).

    Article  CAS  PubMed  Google Scholar 

  93. Happonen, L. J. et al. The structure of the NTPase that powers DNA packaging into Sulfolobus turreted icosahedral virus 2. J. Virol. 87, 8388–8398 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Hurley, J. H. & Hanson, P. I. Membrane budding and scission by the ESCRT machinery: it's all in the neck. Nat. Rev. Mol. Cell Biol. 11, 556–566 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Scourfield, E. J. & Martin-Serrano, J. Growing functions of the ESCRT machinery in cell biology and viral replication. Biochem. Soc. Trans. 45, 613–634 (2017).

    Article  CAS  PubMed  Google Scholar 

  96. Makarova, K. S., Yutin, N., Bell, S. D. & Koonin, E. V. Evolution of diverse cell division and vesicle formation systems in Archaea. Nat. Rev. Microbiol. 8, 731–741 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Liu, J. et al. Functional assignment of multiple ESCRT-III homologs in cell division and budding in Sulfolobus islandicus. Mol. Microbiol. 105, 540–553 (2017).

    Article  CAS  PubMed  Google Scholar 

  98. Bize, A. et al. A unique virus release mechanism in the Archaea. Proc. Natl Acad. Sci. USA 106, 11306–11311 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Brumfield, S. K. et al. Particle assembly and ultrastructural features associated with replication of the lytic archaeal virus Sulfolobus turreted icosahedral virus. J. Virol. 83, 5964–5970 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Quax, T. E. F., Krupovic, M., Lucas, S., Forterre, P. & Prangishvili, D. The Sulfolobus rod-shaped virus 2 encodes a prominent structural component of the unique virion release system in Archaea. Virology 404, 1–4 (2010).

    Article  CAS  PubMed  Google Scholar 

  101. Quax, T. E. et al. Simple and elegant design of a virion egress structure in Archaea. Proc. Natl Acad. Sci. USA 108, 3354–3359 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Snyder, J. C., Brumfield, S. K., Peng, N., She, Q. & Young, M. J. Sulfolobus turreted icosahedral virus c92 protein responsible for the formation of pyramid-like cellular lysis structures. J. Virol. 85, 6287–6292 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Daum, B. et al. Self-assembly of the general membrane-remodeling protein PVAP into sevenfold virus-associated pyramids. Proc. Natl Acad. Sci. USA 111, 3829–3834 (2014). This study presents a three-dimensional reconstruction of the virus-associated pyramids employed by rod-shaped virus SIRV2 during the egress.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. Bize, A. et al. Viruses in acidic geothermal environments of the Kamchatka Peninsula. Res. Microbiol. 159, 358–366 (2008).

    Article  CAS  PubMed  Google Scholar 

  105. Rensen, E., Krupovic, M. & Prangishvili, D. Mysterious hexagonal pyramids on the surface of Pyrobaculum cells. Biochimie 118, 365–367 (2015).

    Article  CAS  PubMed  Google Scholar 

  106. Young, R. Phage lysis: three steps, three choices, one outcome. J. Microbiol. 52, 243–258 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. Luo, Y., Pfister, P., Leisinger, T. & Wasserfallen, A. Pseudomurein endoisopeptidases PeiW and PeiP, two moderately related members of a novel family of proteases produced in Methanothermobacter strains. FEMS Microbiol. Lett. 208, 47–51 (2002).

    Article  CAS  PubMed  Google Scholar 

  108. Prangishvili, D., Garrett, R. A. & Koonin, E. V. Evolutionary genomics of archaeal viruses: unique viral genomes in the third domain of life. Virus Res. 117, 52–67 (2006).

    Article  CAS  PubMed  Google Scholar 

  109. 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).

    Article  CAS  PubMed  Google Scholar 

  110. Krupovic, M., White, M. F., Forterre, P. & Prangishvili, D. Postcards from the edge: structural genomics of archaeal viruses. Adv. Virus Res. 82, 33–62 (2012).

    Article  CAS  PubMed  Google Scholar 

  111. Dellas, N., Lawrence, C. M. & Young, M. J. A survey of protein structures from archaeal viruses. Life 3, 118–130 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Iverson, E. A., Goodman, D. A., Gorchels, M. E. & Stedman, K. M. Extreme mutation tolerance: nearly half of the archaeal fusellovirus Sulfolobus spindle-shaped virus 1 genes are not required for virus function, including the minor capsid protein gene, vp3. J. Virol. 91, e02406-16 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  113. Iranzo, J., Krupovic, M. & Koonin, E. V. A network perspective on the virus world. Commun. Integr. Biol. 10, e1296614 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  114. Prangishvili, D. Archaeal viruses: living fossils of the ancient virosphere? Ann. NY Acad. Sci. 1341, 35–40 (2015).

    Article  CAS  PubMed  Google Scholar 

  115. Hendrix, R. W. Bacteriophage genomics. Curr. Opin. Microbiol. 6, 506–511 (2003).

    Article  CAS  PubMed  Google Scholar 

  116. Krupovic, M., Makarova, K. S., Forterre, P., Prangishvili, D. & Koonin, E. V. Casposons: a new superfamily of self-synthesizing DNA transposons at the origin of prokaryotic CRISPR-Cas immunity. BMC Biol. 12, 36 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  117. Krupovic, M., Béguin, P. & Koonin, E. V. Casposons: mobile genetic elements that gave rise to the CRISPR-Cas adaptation machinery. Curr. Opin. Microbiol. 38, 36–43 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. Lopez-Garcia, P., Forterre, P., van der Oost, J. & Erauso, G. Plasmid pGS5 from the hyperthermophilic archaeon Archaeoglobus profundus is negatively supercoiled. J. Bacteriol. 182, 4998–5000 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. Gorlas, A., Krupovic, M., Forterre, P. & Geslin, C. Living side by side with a virus: characterization of two novel plasmids from Thermococcus prieurii, a host for the spindle-shaped virus TPV1. Appl. Environ. Microbiol. 79, 3822–3828 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  120. Geslin, C. et al. Analysis of the first genome of a hyperthermophilic marine virus-like particle, PAV1, isolated from Pyrococcus abyssi. J. Bacteriol. 189, 4510–4519 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  121. Krupovic, M., Gonnet, M., Hania, W. B., Forterre, P. & Erauso, G. Insights into dynamics of mobile genetic elements in hyperthermophilic environments from five new Thermococcus plasmids. PLoS ONE 8, e49044 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. Goulet, A. et al. Getting the best out of long-wavelength X-rays: de novo chlorine/sulfur SAD phasing of a structural protein from ATV. Acta Crystallogr. D Biol. Crystallogr. 66, 304–308 (2010).

    Article  CAS  PubMed  Google Scholar 

  123. 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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  124. Makarova, K. S. et al. An updated evolutionary classification of CRISPR-Cas systems. Nat. Rev. Microbiol. 13, 722–736 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  125. Burstein, D. et al. Major bacterial lineages are essentially devoid of CRISPR-Cas viral defence systems. Nat. Commun. 7, 10613 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  126. Bidgood, S. R. & Mercer, J. Cloak and dagger: alternative immune evasion and modulation strategies of poxviruses. Viruses 7, 4800–4825 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  127. Ressing, M. E. et al. Immune evasion by Epstein-Barr virus. Curr. Top. Microbiol. Immunol. 391, 355–381 (2015).

    CAS  PubMed  Google Scholar 

  128. Zhao, J. H., Hua, C. L., Fang, Y. Y. & Guo, H. S. The dual edge of RNA silencing suppressors in the virus-host interactions. Curr. Opin. Virol. 17, 39–44 (2016).

    Article  CAS  PubMed  Google Scholar 

  129. Chowdhury, S. et al. Structure reveals mechanisms of viral suppressors that intercept a CRISPR RNA-guided surveillance complex. Cell 169, 47–57.e11 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  130. Pawluk, A. et al. Inactivation of CRISPR-Cas systems by anti-CRISPR proteins in diverse bacterial species. Nat. Microbiol. 1, 16085 (2016).

    Article  CAS  PubMed  Google Scholar 

  131. Sontheimer, E. J. & Davidson, A. R. Inhibition of CRISPR-Cas systems by mobile genetic elements. Curr. Opin. Microbiol. 37, 120–127 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  132. Iranzo, J., Lobkovsky, A. E., Wolf, Y. I. & Koonin, E. V. Evolutionary dynamics of the prokaryotic adaptive immunity system CRISPR-Cas in an explicit ecological context. J. Bacteriol. 195, 3834–3844 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  133. Weinberger, A. D., Wolf, Y. I., Lobkovsky, A. E., Gilmore, M. S. & Koonin, E. V. Viral diversity threshold for adaptive immunity in prokaryotes. mBio 3, e00456-12 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  134. Shmakov, S. A. et al. The CRISPR spacer space is dominated by sequences from the species-specific mobilome. mBio 8, e01397-17 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  135. Fineran, P. C. et al. Degenerate target sites mediate rapid primed CRISPR adaptation. Proc. Natl Acad. Sci. USA 111, E1629–E1638 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  136. Manica, A., Zebec, Z., Steinkellner, J. & Schleper, C. Unexpectedly broad target recognition of the CRISPR-mediated virus defence system in the archaeon Sulfolobus solfataricus. Nucleic Acids Res. 41, 10509–10517 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  137. Maniv, I., Jiang, W., Bikard, D. & Marraffini, L. A. Impact of different target sequences on type III CRISPR-Cas immunity. J. Bacteriol. 198, 941–950 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  138. Mousaei, M., Deng, L., She, Q. & Garrett, R. A. Major and minor crRNA annealing sites facilitate low stringency DNA protospacer binding prior to type I-A CRISPR-Cas interference in Sulfolobus. RNA Biol. 13, 1166–1173 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  139. Held, N. L. & Whitaker, R. J. Viral biogeography revealed by signatures in Sulfolobus islandicus genomes. Environ. Microbiol. 11, 457–466 (2009).

    Article  CAS  PubMed  Google Scholar 

  140. Emerson, J. B. et al. Virus-host and CRISPR dynamics in Archaea-dominated hypersaline Lake Tyrrell, Victoria, Australia. Archaea 2013, 370871 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  141. Gudbergsdóttir, S. R., Menzel, P., Krogh, A., Young, M. & Peng, X. Novel viral genomes identified from six metagenomes reveal wide distribution of archaeal viruses and high viral diversity in terrestrial hot springs. Environ. Microbiol. 18, 863–874 (2016). The study describes several novel hyperthermophilic archaeal virus genomes assembled from metagenomic data.

    Article  CAS  PubMed  Google Scholar 

  142. Adriaenssens, E. M., van Zyl, L. J., Cowan, D. A. & Trindade, M. I. Metaviromics of Namib Desert salt pans: a novel lineage of haloarchaeal salterproviruses and a rich source of ssDNA viruses. Viruses 8, 14 (2016).

    Article  CAS  PubMed Central  Google Scholar 

  143. Nigro, O. D. et al. Viruses in the oceanic basement. mBio 8, e02129-16 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  144. Nishimura, Y. et al. Environmental viral genomes shed new light on virus-host interactions in the ocean. mSphere 2, e00359-16 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  145. Philosof, A. et al. Novel abundant oceanic viruses of uncultured marine group II Euryarchaeota identified by genome-centric metagenomics. Curr. Biol. 27, 1362–1368 (2017). This study, along with REF 144, describes the identification of a novel, diverse group of archaeal viruses, called Magroviruses, associated with environmentally abundant, uncultured Marine Group II Euryarchaeota.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  146. Servin-Garciduenas, L. E., Peng, X., Garrett, R. A. & Martinez-Romero, E. Genome sequence of a novel archaeal rudivirus recovered from a mexican hot spring. Genome Announc. 1, e00040-12 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  147. Servin-Garciduenas, L. E., Peng, X., Garrett, R. A. & Martinez-Romero, E. Genome sequence of a novel archaeal fusellovirus assembled from the metagenome of a mexican hot spring. Genome Announc 1, e00164-13 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  148. Garcia-Heredia, I. et al. Reconstructing viral genomes from the environment using fosmid clones: the case of haloviruses. PLoS ONE 7, e33802 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  149. Santos, F. et al. Metagenomic approach to the study of halophages: the environmental halophage 1. Environ. Microbiol. 9, 1711–1723 (2007).

    Article  CAS  PubMed  Google Scholar 

  150. Martinez-Garcia, M., Santos, F., Moreno-Paz, M., Parro, V. & Anton, J. Unveiling viral-host interactions within the 'microbial dark matter'. Nat. Commun. 5, 4542 (2014).

    Article  CAS  PubMed  Google Scholar 

  151. Santos, F. et al. Metatranscriptomic analysis of extremely halophilic viral communities. ISME J. 5, 1621–1633 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  152. Garrett, R. A. et al. Metagenomic analyses of novel viruses and plasmids from a cultured environmental sample of hyperthermophilic neutrophiles. Environ. Microbiol. 12, 2918–2930 (2010).

    Article  CAS  PubMed  Google Scholar 

  153. Bolduc, B. et al. Identification of novel positive-strand RNA viruses by metagenomic analysis of archaea-dominated Yellowstone hot springs. J. Virol. 86, 5562–5573 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  154. 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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  155. Chow, C. E., Winget, D. M., White, R. A., 3rd, Hallam, S. J. & Suttle, C. A. Combining genomic sequencing methods to explore viral diversity and reveal potential virus-host interactions. Front. Microbiol. 6, 265 (2015).

    PubMed  PubMed Central  Google Scholar 

  156. Labonte, J. M. et al. Single-cell genomics-based analysis of virus-host interactions in marine surface bacterioplankton. ISME J. 9, 2386–2399 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  157. Burstein, D. et al. New CRISPR-Cas systems from uncultivated microbes. Nature 542, 237–241 (2017).

    Article  CAS  PubMed  Google Scholar 

  158. Paul, B. G. et al. Targeted diversity generation by intraterrestrial archaea and archaeal viruses. Nat. Commun. 6, 6585 (2015).

    Article  CAS  PubMed  Google Scholar 

  159. Simmonds, P. et al. Consensus statement: virus taxonomy in the age of metagenomics. Nat. Rev. Microbiol. 15, 161–168 (2017).

    Article  CAS  PubMed  Google Scholar 

  160. Häring, M. et al. Morphology and genome organization of the virus PSV of the hyperthermophilic archaeal genera Pyrobaculum and Thermoproteus: a novel virus family, the Globuloviridae. Virology 323, 233–242 (2004).

    Article  CAS  PubMed  Google Scholar 

  161. Stedman, K. in The Springer Index of Viruses ( eds Tidona, C. & Darai, G. ) 561–566 (Springer-Verlag, 2011).

  162. Schleper, C., Kubo, K. & Zillig, W. The particle SSV1 from the extremely thermophilic archaeon Sulfolobus is a virus: demonstration of infectivity and of transfection with viral DNA. Proc. Natl Acad. Sci. USA 89, 7645–7649 (1992).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  163. Porter, K. et al. SH1: A novel, spherical halovirus isolated from an Australian hypersaline lake. Virology 335, 22–33 (2005).

    Article  CAS  PubMed  Google Scholar 

  164. Rice, G. et al. The structure of a thermophilic archaeal virus shows a double-stranded DNA viral capsid type that spans all domains of life. Proc. Natl Acad. Sci. USA 101, 7716–7720 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

D.P. is supported by l'Agence Nationale de la Recherche (France) project EXAVIR and by the European Union's Horizon 2020 research and innovation programme under grant agreement 685778, project VIRUS-X. D.H.B. was supported by the Academy Professors programme, Academy of Finland funding grants 283072 and 255342. P.F. is supported by the European Research Council under the European Union's Seventh Framework Program (FP/2007-2013)/Project EVOMOBIL — ERC Grant Agreement no. 340440. J.I. and E.V.K. are supported by intramural funds of the US Department of Health and Human Services (to the National Library of Medicine). M.K. is supported by l'Agence Nationale de la Recherche (France) project ENVIRA.

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Authors and Affiliations

  1. Department of Microbiology, Institut Pasteur, 25 rue du Dr Roux, Paris, 75015, France

    David Prangishvili, Patrick Forterre & Mart Krupovic

  2. Department of Biosciences, University of Helsinki, Helsinki, 00014, Finland

    Dennis H. Bamford

  3. National Center for Biotechnology Information, National Library of Medicine, Bethesda, 20894, Maryland, USA

    Jaime Iranzo & Eugene V. Koonin

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Contributions

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

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Supplementary information

Supplementary information S1 (table)

Isolates of archaeal viruses (DOC 45 kb)

Glossary

Thermophilic

Requiring high temperatures for optimal growth.

Acidophilic

Thriving under highly acidic conditions.

Alkaliphilic

Thriving under highly alkaline conditions.

Halophilic

Requiring high levels of sodium chloride for growth.

Methanogenic

Producing methane as a metabolic by-product in anoxic conditions.

Benthic

Related to the ecological region at the lowest sea level, including the sediment surface and some subsurface layers.

Epipelagic zone

The illuminated zone at the surface of the sea where enough light is available for photosynthesis.

Mesopelagic zone

The zone close to the sea surface in which light penetrates but is insufficient for photosynthesis.

Hyperthermophilic

Having an optimal growth temperature at or above 80 °C.

Fosmid sequencing

Sequencing of large DNA fragments cloned into a fosmid.

Mutagenic reverse transcription and retrohoming

Targeted replacement of a variable repeat coding region within a gene with a sequence derived from reverse transcription of a cognate non-coding template repeat.

Hyperhalophilic

Requiring extremely high levels of sodium chloride for growth.

Last archaeal common ancestor

The most recent population of organisms from which all extant archaea have a common descent.

Capsid

The protein shell that encloses the genetic material of the virus.

Convergent evolution

The independent evolution of similar features in species of different lineages.

Proviruses

Viral genomes integrated into the host chromosome.

Jelly-roll fold

A structural protein fold composed of eight β-strands arranged in two antiparallel four-stranded β-sheets.

Homology modelling

The construction of an atomic-resolution model of the protein from its amino acid sequence and an experimental three-dimensional structure of a related homologous protein.

A-form

One of the three major forms of double-stranded DNA, with a 23 Å helical diameter and 11 bp per helix turn.

Invertible region

A genome region that can excise and reintegrate into the same genome in inverted orientation.

Protein-primed DNA polymerases

DNA polymerases capable of the protein-primed initiation step of DNA elongation.

Rolling-circle replication

The model of unidirectional DNA replication that can rapidly synthesize multiple copies of circular ssDNA molecules.

Holliday junction resolvase

A highly specialized structure-selective endonuclease that cleaves four-way DNA intermediates that can form during DNA replication.

Strand-displacement

Of genome replication, involving the displacement of a downstream DNA strand encountered during DNA replication.

Strand-coupled genome replication

The model of DNA replication that couples leading-strand and lagging-strand synthesis.

Pseudomurein endoisopeptidase

(PeiP). An enzyme that cleaves pseudomurein cell-wall sacculi of the methanogens.

Endolysin

A type of peptidoglycan-hydrolysing enzyme produced by many bacterial viruses towards the end of the lytic cycle.

Structural genomics

The description of the three-dimensional structure of every protein encoded by a given genome.

Supermodules

Clusters of modules of tightly connected genomes joined through higher-level shared genes.

Mesophiles

Organisms that grow best in moderate temperature, typically between 20 and 45 °C.

CRISPR spacers

Short fragments of viral DNA from previous exposure to the virus, inserted between repetitive sequences of the CRISPR–Cas system.

Protospacers

Fragments of invading mobile genetic element from which CRISPR spacers are derived.

Primed adaptation

A process in which an existing spacer against a foreign DNA promotes rapid and efficient acquisition of additional spacers from the same foreign DNA.

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Prangishvili, D., Bamford, D., Forterre, P. et al. The enigmatic archaeal virosphere. Nat Rev Microbiol 15, 724–739 (2017). https://doi.org/10.1038/nrmicro.2017.125

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