Review

The enigmatic archaeal virosphere

  • Nature Reviews Microbiology 15, 724739 (2017)
  • doi:10.1038/nrmicro.2017.125
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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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References

  1. 1.

    & Phylogenetic structure of the prokaryotic domain: the primary kingdoms. Proc. Natl Acad. Sci. USA 74, 5088–5090 (1977).

  2. 2.

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

  3. 3.

    & Archaea in and on the human body: health implications and future directions. PLoS Pathog. 11, e1004833 (2015).

  4. 4.

    , , & Meta-analysis of quantification methods shows that archaea and bacteria have similar abundances in the subseafloor. Appl. Environ. Microbiol. 79, 7790–7799 (2013).

  5. 5.

    , & Archaeal dominance in the mesopelagic zone of the Pacific Ocean. Nature 409, 507–510 (2001).

  6. 6.

    , & Archaea in biogeochemical cycles. Annu. Rev. Microbiol. 67, 437–457 (2013).

  7. 7.

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

  8. 8.

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

  9. 9.

    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.

  10. 10.

    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.

  11. 11.

    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).

  12. 12.

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

  13. 13.

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

  14. 14.

    , , , & 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).

  15. 15.

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

  16. 16.

    , , , & Unification of the globally distributed spindle-shaped viruses of the Archaea. J. Virol. 88, 2354–2358 (2014).

  17. 17.

    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).

  18. 18.

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

  19. 19.

    , , , & 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.

  20. 20.

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

  21. 21.

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

  22. 22.

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

  23. 23.

    , & Inter-viral conflicts that exploit host CRISPR immune systems of Sulfolobus. Mol. Microbiol. 91, 900–917 (2014).

  24. 24.

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

  25. 25.

    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).

  26. 26.

    , & SNDV, a novel virus of the extremely thermophilic and acidophilic archaeon Sulfolobus. Virology 272, 409–416 (2000).

  27. 27.

    , & 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).

  28. 28.

    , , & 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.

  29. 29.

    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).

  30. 30.

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

  31. 31.

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

  32. 32.

    , & Genomics and biology of Rudiviruses, a model for the study of virus-host interactions in Archaea. Biochem. Soc. Trans. 41, 443–450 (2013).

  33. 33.

    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.

  34. 34.

    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).

  35. 35.

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

  36. 36.

    , , & The archeoviruses. FEMS Microbiol. Rev. 35, 1035–1054 (2011).

  37. 37.

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

  38. 38.

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

  39. 39.

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

  40. 40.

    , , , & Pleolipoviridae, a newly proposed family comprising archaeal pleomorphic viruses with single-stranded or double-stranded DNA genomes. Arch. Virol. 161, 249–256 (2016).

  41. 41.

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

  42. 42.

    , , , & 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).

  43. 43.

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

  44. 44.

    , , , & An ssDNA virus infecting archaea: a new lineage of viruses with a membrane envelope. Mol. Microbiol. 72, 307–319 (2009).

  45. 45.

    , , , & Related haloarchaeal pleomorphic viruses contain different genome types. Nucleic Acids Res. 40, 5523–5534 (2012).

  46. 46.

    & Prokaryote viruses studied by electron microscopy. Arch. Virol. 157, 1843–1849 (2012).

  47. 47.

    , , , & Archaeal viruses and bacteriophages: comparisons and contrasts. Trends Microbiol. 22, 334–344 (2014).

  48. 48.

    , , & Genomics of bacterial and archaeal viruses: dynamics within the prokaryotic virosphere. Microbiol. Mol. Biol. Rev. 75, 610–635 (2011).

  49. 49.

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

  50. 50.

    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.

  51. 51.

    , , & Molecular analysis of Methanobacterium phage ψM2. Mol. Microbiol. 30, 233–244 (1998).

  52. 52.

    , & 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).

  53. 53.

    , , , & A thaumarchaeal provirus testifies for an ancient association of tailed viruses with archaea. Biochem. Soc. Trans. 39, 82–88 (2011).

  54. 54.

    , , , & 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).

  55. 55.

    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.

  56. 56.

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

  57. 57.

    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).

  58. 58.

    & Double-stranded DNA viruses: 20 families and only five different architectural principles for virion assembly. Curr. Opin. Virol. 1, 118–124 (2011).

  59. 59.

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

  60. 60.

    , , & Common ancestry of herpesviruses and tailed DNA bacteriophages. J. Virol. 79, 14967–14970 (2005).

  61. 61.

    , , & Atomic structure of the human cytomegalovirus capsid with its securing tegument layer of pp150. Science 356, eaam6892 (2017).

  62. 62.

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

  63. 63.

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

  64. 64.

    , & Nucleic and amino acid sequences support structure-based viral classification. J. Virol. 91, e02275-16 (2017).

  65. 65.

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

  66. 66.

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

  67. 67.

    , & The double-stranded DNA virosphere as a modular hierarchical network of gene sharing. mBio 7, e00978-16 (2016).

  68. 68.

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

  69. 69.

    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.

  70. 70.

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

  71. 71.

    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.

  72. 72.

    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).

  73. 73.

    , , & A census of α-helical membrane proteins in double-stranded DNA viruses infecting bacteria and archaea. BMC Bioinformatics 16, 380 (2015).

  74. 74.

    , , & His1 and His2 are distantly related, spindle-shaped haloviruses belonging to the novel virus group, Salterprovirus. Virology 350, 228–239 (2006).

  75. 75.

    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).

  76. 76.

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

  77. 77.

    , , , & 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.

  78. 78.

    , , & AFV1, a novel virus infecting hyperthermophilic archaea of the genus acidianus. Virology 315, 68–79 (2003).

  79. 79.

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

  80. 80.

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

  81. 81.

    , , , & 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).

  82. 82.

    , , & 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).

  83. 83.

    , , , & Genome of the Acidianus bottle-shaped virus and insights into the replication and packaging mechanisms. Virology 364, 237–243 (2007).

  84. 84.

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

  85. 85.

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

  86. 86.

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

  87. 87.

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

  88. 88.

    , & 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.

  89. 89.

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

  90. 90.

    , , , & 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).

  91. 91.

    , & 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).

  92. 92.

    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).

  93. 93.

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

  94. 94.

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

  95. 95.

    & Growing functions of the ESCRT machinery in cell biology and viral replication. Biochem. Soc. Trans. 45, 613–634 (2017).

  96. 96.

    , , & Evolution of diverse cell division and vesicle formation systems in Archaea. Nat. Rev. Microbiol. 8, 731–741 (2010).

  97. 97.

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

  98. 98.

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

  99. 99.

    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).

  100. 100.

    , , , & The Sulfolobus rod-shaped virus 2 encodes a prominent structural component of the unique virion release system in Archaea. Virology 404, 1–4 (2010).

  101. 101.

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

  102. 102.

    , , , & Sulfolobus turreted icosahedral virus c92 protein responsible for the formation of pyramid-like cellular lysis structures. J. Virol. 85, 6287–6292 (2011).

  103. 103.

    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.

  104. 104.

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

  105. 105.

    , & Mysterious hexagonal pyramids on the surface of Pyrobaculum cells. Biochimie 118, 365–367 (2015).

  106. 106.

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

  107. 107.

    , , & 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).

  108. 108.

    , & Evolutionary genomics of archaeal viruses: unique viral genomes in the third domain of life. Virus Res. 117, 52–67 (2006).

  109. 109.

    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).

  110. 110.

    , , & Postcards from the edge: structural genomics of archaeal viruses. Adv. Virus Res. 82, 33–62 (2012).

  111. 111.

    , & A survey of protein structures from archaeal viruses. Life 3, 118–130 (2013).

  112. 112.

    , , & 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).

  113. 113.

    , & A network perspective on the virus world. Commun. Integr. Biol. 10, e1296614 (2017).

  114. 114.

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

  115. 115.

    Bacteriophage genomics. Curr. Opin. Microbiol. 6, 506–511 (2003).

  116. 116.

    , , , & Casposons: a new superfamily of self-synthesizing DNA transposons at the origin of prokaryotic CRISPR-Cas immunity. BMC Biol. 12, 36 (2014).

  117. 117.

    , & Casposons: mobile genetic elements that gave rise to the CRISPR-Cas adaptation machinery. Curr. Opin. Microbiol. 38, 36–43 (2017).

  118. 118.

    , , & Plasmid pGS5 from the hyperthermophilic archaeon Archaeoglobus profundus is negatively supercoiled. J. Bacteriol. 182, 4998–5000 (2000).

  119. 119.

    , , & 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).

  120. 120.

    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).

  121. 121.

    , , , & Insights into dynamics of mobile genetic elements in hyperthermophilic environments from five new Thermococcus plasmids. PLoS ONE 8, e49044 (2013).

  122. 122.

    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).

  123. 123.

    , , & Evolution of an archaeal virus nucleocapsid protein from the CRISPR-associated Cas4 nuclease. Biol. Direct 10, 65 (2015).

  124. 124.

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

  125. 125.

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

  126. 126.

    & Cloak and dagger: alternative immune evasion and modulation strategies of poxviruses. Viruses 7, 4800–4825 (2015).

  127. 127.

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

  128. 128.

    , , & The dual edge of RNA silencing suppressors in the virus-host interactions. Curr. Opin. Virol. 17, 39–44 (2016).

  129. 129.

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

  130. 130.

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

  131. 131.

    & Inhibition of CRISPR-Cas systems by mobile genetic elements. Curr. Opin. Microbiol. 37, 120–127 (2017).

  132. 132.

    , , & Evolutionary dynamics of the prokaryotic adaptive immunity system CRISPR-Cas in an explicit ecological context. J. Bacteriol. 195, 3834–3844 (2013).

  133. 133.

    , , , & Viral diversity threshold for adaptive immunity in prokaryotes. mBio 3, e00456-12 (2012).

  134. 134.

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

  135. 135.

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

  136. 136.

    , , & Unexpectedly broad target recognition of the CRISPR-mediated virus defence system in the archaeon Sulfolobus solfataricus. Nucleic Acids Res. 41, 10509–10517 (2013).

  137. 137.

    , , & Impact of different target sequences on type III CRISPR-Cas immunity. J. Bacteriol. 198, 941–950 (2016).

  138. 138.

    , , & 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).

  139. 139.

    & Viral biogeography revealed by signatures in Sulfolobus islandicus genomes. Environ. Microbiol. 11, 457–466 (2009).

  140. 140.

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

  141. 141.

    , , , & 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.

  142. 142.

    , , & Metaviromics of Namib Desert salt pans: a novel lineage of haloarchaeal salterproviruses and a rich source of ssDNA viruses. Viruses 8, 14 (2016).

  143. 143.

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

  144. 144.

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

  145. 145.

    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.

  146. 146.

    , , & Genome sequence of a novel archaeal rudivirus recovered from a mexican hot spring. Genome Announc. 1, e00040-12 (2013).

  147. 147.

    , , & Genome sequence of a novel archaeal fusellovirus assembled from the metagenome of a mexican hot spring. Genome Announc 1, e00164-13 (2013).

  148. 148.

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

  149. 149.

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

  150. 150.

    , , , & Unveiling viral-host interactions within the 'microbial dark matter'. Nat. Commun. 5, 4542 (2014).

  151. 151.

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

  152. 152.

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

  153. 153.

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

  154. 154.

    , & The logic of DNA replication in double-stranded DNA viruses: insights from global analysis of viral genomes. Nucleic Acids Res. 44, 4551–4564 (2016).

  155. 155.

    , , , & Combining genomic sequencing methods to explore viral diversity and reveal potential virus-host interactions. Front. Microbiol. 6, 265 (2015).

  156. 156.

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

  157. 157.

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

  158. 158.

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

  159. 159.

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

  160. 160.

    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).

  161. 161.

    in The Springer Index of Viruses ( & ) 561–566 (Springer-Verlag, 2011).

  162. 162.

    , & 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).

  163. 163.

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

  164. 164.

    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).

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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.

Author information

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, Maryland 20894, 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.

Competing interests

The authors declare no competing financial interests.

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Correspondence to David Prangishvili or Mart Krupovic.

Supplementary information

Word documents

  1. 1.

    Supplementary information S1 (table)

    Isolates of archaeal viruses

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.