Review Article | Published:

Viruses of the Archaea: a unifying view

Nature Reviews Microbiology volume 4, pages 837848 (2006) | Download Citation

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Abstract

DNA viruses of the Archaea have highly diverse and often exceptionally complex morphotypes. Many have been isolated from geothermally heated hot environments, raising intriguing questions about their origins, and contradicting the widespread notion of limited biodiversity in extreme environments. Here, we provide a unifying view on archaeal viruses, and present them as a particular assemblage that is fundamentally different in morphotype and genome from the DNA viruses of the other two domains of life, the Bacteria and Eukarya.

Key points

  • So far, all characterized archaeal viruses carry dsDNA genomes and exhibit a wide range of virion morphotypes, strongly surpassing the dsDNA viruses of the Bacteria in their diversity.

  • In addition to head-tail viruses, which are common in the Bacteria, the Archaea replicate many viruses with morphologies which have not been observed before for any dsDNA virus. These include fusiforms, droplet and bottle shapes, and linear and spherical virions, with more complex virions combining features of the different forms.

  • Genome sequence analyses demonstrate that most of the archaeal viruses are unrelated to other known viruses and indicate that they might have different, and possibly multiple, evolutionary origins.

  • Assuming that archaeal head-tail viruses originate from the domain Bacteria (there are many arguments for this suggestion), we are faced with the prospect that each of the three domains of life, the Bacteria, Archaea and Eukarya, was originally characterized by a unique set of associated dsDNA viruses.

  • One possible explanation for the existence of three different 'virospheres', each associated with a specific domain, is that these virospheres were selected when the domains first arose. Therefore, the first evolving organisms of each separate domain could have already been infected by different subsets of viruses from the ancestral virosphere, which predated the last universal common ancestor.

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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.

    , & Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Proc. Natl Acad. Sci. USA 87, 4576–4579 (1990).

  3. 3.

    & (eds) Archaea. Evolution, Physiology and Molecular Biology (Blackwell Publishing, Oxford, 2006). This is a recent and comprehensive book that covers the ecology, physiology, molecular biology and evolution of the Archaea.

  4. 4.

    & Bacteriophage of Halobacterium salinarium. Nature 248, 680–681 (1974).

  5. 5.

    , , & Salt-dependent bacteriophage infecting Halobacterium cutirubrum and H. halobium. Nature 256, 314–315 (1975).

  6. 6.

    Bacteriophages of Halobacterium halobium: isolated from fermented fish sauce and primary characterization. Can. J. Microbiol. 28, 916–921 (1982).

  7. 7.

    , & Bacteriophages of Halobacterium halobium: virion DNAs and proteins. Can. J. Microbiol. 29, 627–629 (1983).

  8. 8.

    , & Haloarchaeal viruses: how diverse are they? Res. Microbiol. 154, 309–313 (2003).

  9. 9.

    Evolutionary insights from studies on viruses of hyperthermophilic archaea. Res. Microbiol. 154, 289–294 (2003).

  10. 10.

    , & Evolutionary genomics of archaeal viruses: Unique viral genomes in the third domain of life. Virus Res. 117, 52–67 (2006). Describes a detailed analysis of proteins encoded by archaeal viruses, with an emphasis on the comparative genomics of crenarchaeal viruses.

  11. 11.

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

  12. 12.

    & His1, an archaeal virus of the Fuselloviridae family that infects Haloarcula hispanica. J. Virol. 72, 9392–9395 (1998).

  13. 13.

    et al. PAV1, the first virus-like particle isolated from a hyperthermophilic euryarchaeote, 'Pyrococcus abyssi'. J. Bacteriol. 185, 3888–3894 (2003).

  14. 14.

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

  15. 15.

    et al. SAV1, a temperate u.v.-inducible DNA virus-like particle from the archaebacterium Sulfolobus acidocaldarius isolate B12. EMBO J. 3, 2165–2168 (1984).

  16. 16.

    et al. Complete nucleotide sequence of the virus SSV1 of the archaebacterium Sulfolobus shibatae. Virology 185, 242–250 (1991).

  17. 17.

    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).

  18. 18.

    , & 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).

  19. 19.

    et al. Relationships between fuselloviruses infecting the extremely thermophilic archaeon Sulfolobus: SSV1 and SSV2. Res. Microbiol. 154, 295–302 (2003).

  20. 20.

    et al. Comparative genomic analysis of hyperthermophilic archaeal Fuselloviridae viruses. J. Virol. 78, 1954–1961 (2004).

  21. 21.

    , & Isolation and characterization of an archaebacterial virus-like particle from Methanococcus voltae A3. J. Bacteriol. 171, 93–98 (1989).

  22. 22.

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

  23. 23.

    et al. Remarkable morphological diversity of viruses and virus-like particles in hot terrestrial environments. Arch. Virol. 147, 2419–2429 (2002).

  24. 24.

    et al. Viruses from extreme thermal environments. Proc. Natl Acad. Sci. USA 98, 13341–13345 (2001).

  25. 25.

    et al. Screening for Sulfolobales, their plasmids, and their viruses in Icelandic solfataras. Syst. Appl. Microbiol. 16, 609–628 (1994). References 23, 24 and 25 describe the diversity of viral morphotypes observed in samples from hot springs in the United States and Iceland.

  26. 26.

    , , , , Viral lysis and bacterivory as prokaryotic loss factors along a salinity gradient. Aquat. Microb. Ecol. 11, 215–227 (1996).

  27. 27.

    , & Occurrence of virus-like particles in the Dead Sea. Extremophiles 1, 143–149 (1997). Describes virus-like particles in samples from the hypersaline Dead Sea.

  28. 28.

    , & SSV1-encoded site-specific recombination system in Sulfolobus shibatae. Mol. Gen. Genet. 237, 334–342 (1993).

  29. 29.

    , , , & Positively supercoiled DNA in a virus-like-particle of an archaebacterium. Nature 321, 256–258 (1986).

  30. 30.

    et al. in The Biochemistry of Archaea (Archaebacteria) (ed. Kates, M. et al.) 367–391 (Elsevier Science Publishers B. V., 1993).

  31. 31.

    , , , & 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). Describes the viral diversity in a single acidic, hot spring in southern Italy.

  32. 32.

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

  33. 33.

    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).

  34. 34.

    et al. Sequences and replication of genomes of the archaeal rudiviruses SIRV1 and SIRV2: relationships to the archaeal lipothrixvirus SIFV and some eukaryal viruses. Virology 291, 226–234 (2001).

  35. 35.

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

  36. 36.

    et al. A novel lipothrixvirus, SIFV, of the extremely thermophilic crenarchaeon Sulfolobus. Virology 267, 252–266 (2000).

  37. 37.

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

  38. 38.

    et al. Structure and genome organization of AFV2, a novel archaeal lipothrixvirus with unusual terminal and core structures. J. Bacteriol. 187, 3855–3858 (2005).

  39. 39.

    et al. TTV1, TTV2, TTV3, a family of viruses of the extremely thermophilic, anaerobic sulfur-reducing archaebacterium Thermoproteus tenax. Mol. Gen. Genet. 192, 39–45 (1983).

  40. 40.

    , , & Identification and characterization of the genes encoding three structural proteins of the Thermoproteus tenax virus TTV1. Mol. Gen. Genet. 217, 105–110 (1989).

  41. 41.

    , , , & The genome of the archaeal virus SIRV1 has features in common with genomes of eukaryal viruses. Virology 281, 6–9 (2001).

  42. 42.

    , , & Holliday junction resolving enzymes of archaeal viruses SIRV1 and SIRV2. J. Mol. Biol. 309, 1067–1076 (2001).

  43. 43.

    in Fields Virology (eds Fields, B. N., Knipe, D. M. & Howley, P. M.) 2637–2671 (Lippincott-Raven, Philadelphia, 1996).

  44. 44.

    , , & Transcription of the rod-shaped viruses SIRV1 and SIRV2 of the hyperthermophilic archaeon Sulfolobus. J. Bacteriol. 186, 7745–7753 (2004).

  45. 45.

    et al. A novel archaeal regulatory protein, Sta1, activates transcription from viral promoters. Nucleic Acids Res. 14 Sep 2006 (doi: 10.1093/nar/gk1502). Reports on the strategy of an archaeal virus to co-opt a host-cell regulator to promote the transcription of some of its genes.

  46. 46.

    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).

  47. 47.

    et al. TTSV1, a new virus-like particle isolated from the hyperthermophilic crenarchaeote Thermoproteus tenax. Virology 351, 280–290 (2006).

  48. 48.

    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).

  49. 49.

    et al. Characterization of the archaeal thermophile Sulfolobus turreted icosahedral virus validates an evolutionary link among double-stranded DNA viruses from all domains of life. J. Virol. 80, 7625–7635 (2006).

  50. 50.

    et al. Constituents of SH1, a novel lipid-containing virus infecting the halophilic euryarchaeon Haloarcula hispanica. J. Virol. 79, 9097–9107 (2005).

  51. 51.

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

  52. 52.

    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). Shows that the major capsid protein of STIV is highly similar in structure to capsid proteins of some bacterial and eukaryal viruses.

  53. 53.

    , in Methods in Microbiology — Extremophiles (eds Reiney, F. A. & Oren, A.) 681–702 (Elsevier, London, 2006). Reviews cultivation methods for the haloarchaea and their viruses.

  54. 54.

    , , , & The immunity-conferring plasmid p phi HL from the Halobacterium salinarium phage phiH: nucleotide sequence and transcription. Virology 190, 45–54 (1992).

  55. 55.

    , , & Sequence analysis of the insertion element ISH1.8 and of associated structural changes in the genome of phage phiH of the archaebacterium Halobacterium halobium. EMBO J. 3, 1717–1722 (1984).

  56. 56.

    et al. Halobacterium halobium phage phiH. EMBO J. 1, 87–92 (1982).

  57. 57.

    & Transcription of the halophage phiH repressor gene is abolished by transcription from an inversely oriented lytic promoter. FEBS Lett. 344, 125–128 (1994).

  58. 58.

    et al. Natrialba magadii virus phiCh1: first complete nucleotide sequence and functional organization of a virus infecting a haloalkaliphilic archaeon. Mol. Microbiol. 45, 851–863 (2002).

  59. 59.

    , , & Inversion within the haloalkaliphilic virus phi Ch1 DNA results in differential expression of structural proteins. Mol. Microbiol. 52, 413–426 (2004).

  60. 60.

    et al. Characterization of Natronobacterium magadii phage phi Ch1, a unique archaeal phage containing DNA and RNA. Mol. Microbiol. 23, 603–616 (1997).

  61. 61.

    & HF1 and HF2: novel bacteriophages of halophilic archaea. Virology 197, 678–684 (1993).

  62. 62.

    & Halophage HF2: genome organization and replication strategy. J. Virol. 69, 2322–2327 (1995).

  63. 63.

    , & Haloviruses HF1 and HF2: evidence for a recent and large recombination event. J. Bacteriol. 186, 2810–2817 (2004).

  64. 64.

    et al. HF2: a double-stranded DNA tailed haloarchaeal virus with a mosaic genome. Mol. Microbiol. 44, 283–296 (2002).

  65. 65.

    , & Organization of Methanobacterium thermoautotrophicum bacteriophage psi M1 DNA. Mol. Gen. Genet. 220, 161–164 (1989).

  66. 66.

    , , , , Characterization of psiM1, a virulent phage of Methanobacterium thermoautotrophicum Marburg. Arch. Microbiol. 152, 105–110 (1989).

  67. 67.

    , , & Molecular analysis of Methanobacterium phage psiM2. Mol. Microbiol. 30, 233–244 (1998).

  68. 68.

    , , , & Evolutionary relationships among diverse bacteriophages and prophages: all the world's a phage. Proc. Natl Acad. Sci. USA 96, 2192–2197 (1999).

  69. 69.

    et al. Origins of highly mosaic mycobacteriophage genomes. Cell 113, 171–182 (2003).

  70. 70.

    , , , & Observation of virus-like particles in high temperature enrichment cultures from deep-sea hydrothermal vents. Res. Microbiol. 154, 303–307 (2003).

  71. 71.

    , & in SGM Symposium 66: Prokaryotic Diversity — Mechanisms and Significance. (eds Logan, N. M., Lappin-Scott, H. M. & Oyston, P. C. F.) 131–144 (Cambridge University Press, 2006).

  72. 72.

    in Methods in Microbiology — Extremophiles (eds Reiney, F. A. & Oren, A.) 331–348 (Elsevier, London, 2006). Reviews the methods of isolating archaeal virus–host systems from hydrothermal environments.

  73. 73.

    , , & Hot crenarchaeal viruses reveal deep evolutionary connections. Nature Rev. Microbiol. 4, 520–528 (2006).

  74. 74.

    , , & Structure of A197 from Sulfolobus turreted icosahedral virus: a crenarchaeal viral glycosyltransferase exhibiting the GT-A fold. J. Virol. 80, 7636–7644 (2006).

  75. 75.

    et al. Biochemical and phylogenetic characterization of the dUTPase from the archaeal virus SIRV. J. Biol. Chem. 273, 6024–6029 (1998).

  76. 76.

    et al. Effects of culturing on the population structure of a hyperthermophilic virus. Microb. Ecol. 48, 561–566 (2004).

  77. 77.

    , , & Long stretches of short tandem repeats are present in the largest replicons of the archaea Haloferax mediterranei and Haloferax volcanii and could be involved in replicon partitioning. Mol. Microbiol. 17, 85–93 (1995).

  78. 78.

    , , & A putative viral defence mechanism in archaeal cells. Archaea 2, 59–72 (2006).

  79. 79.

    , , & Intervening sequences of regularly spaced prokaryotic repeats derive from foreign genetic elements. J. Mol. Evol. 60, 174–182 (2005).

  80. 80.

    et al. Identification of 86 candidates for small non-messenger RNAs from the archaeon Archaeoglobus fulgidus. Proc. Natl Acad. Sci. USA 99, 7536–7541 (2002).

  81. 81.

    et al. Identification of novel non-coding RNAs as potential antisense regulators in the archaeon Sulfolobus solfataricus. Mol. Microbiol. 55, 469–481 (2005).

  82. 82.

    , , & Identification of a novel family of sequence repeats among prokaryotes. Omics 6, 23–33 (2002).

  83. 83.

    , , , & A putative RNA-interference-based immune system in prokaryotes: computational analysis of the predicted enzymatic machinery, functional analogies with eukaryotic RNAi, and hypothetical mechanisms of action. Biol. Direct 1, 7 (2006).

  84. 84.

    , , , & Multiple variants of the archaeal DNA rudivirus SIRV1 in a single host and a novel mechanism of genomic variation. Mol. Microbiol. 54, 366–375 (2004).

  85. 85.

    & The TTV1-encoded viral protein TPX: primary structure of the gene and the protein. Nucleic Acids Res. 18, 195 (1990).

  86. 86.

    Frequency of morphological phage descriptions in the year 2000. Brief review. Arch. Virol. 146, 843–857 (2001).

  87. 87.

    , , , & (eds) Virus Taxonomy: Classification and Nomenclature of Viruses (Elsevier, Amsterdam, 2005).

  88. 88.

    & Virioplankton: viruses in aquatic ecosystems. Microbiol. Mol. Biol. Rev. 64, 69–114 (2000).

  89. 89.

    et al. Viruses, plasmids and other genetic elements of thermophilic and hyperthermophilic Archaea. FEMS Microbiol. Rev. 18, 225–236 (1996).

  90. 90.

    , & Horizontal gene transfer in prokaryotes: quantification and classification. Annu. Rev. Microbiol. 55, 709–742 (2001).

  91. 91.

    , & A comparative categorization of gene flux in diverse microbial species. Genomics 86, 462–475 (2005).

  92. 92.

    et al. The genome of Salinibacter ruber: convergence and gene exchange among hyperhalophilic bacteria and archaea. Proc. Natl Acad. Sci. USA 102, 18147–18152 (2005).

  93. 93.

    , & What does structure tell us about virus evolution? Curr. Opin. Struct. Biol. 15, 655–663 (2005). Discusses the potential for structural analyses of virion architecture and coat protein topology to provide insights into viral evolution.

  94. 94.

    , & An emerging phylogenetic core of Archaea: phylogenies of transcription and translation machineries converge following addition of new genome sequences. BMC Evol. Biol. 5, 36 (2005).

  95. 95.

    The origin of viruses and their possible roles in major evolutionary transitions. Virus Res. 117, 5–16 (2006). Presents a hypothesis that viruses played a crucial role in the invention of DNA and the development of its replication mechanisms, and in the formation of the three domains of life.

  96. 96.

    & On the origin of genomes and cells within inorganic compartments. Trends Genet. 21, 647–654 (2005).

  97. 97.

    Viruses take center stage in cellular evolution. Genome Biol. 7, 110 (2006).

  98. 98.

    The two ages of the RNA world, and the transition to the DNA world: a story of viruses and cells. Biochimie 87, 793–803 (2005).

  99. 99.

    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).

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Acknowledgements

We would like to thank all the members of our laboratories who have contributed to this work, and to thank colleagues who have made their unpublished results available to us.

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Affiliations

  1. Molecular Biology of the Gene in Extremophiles Unit, Institut Pasteur, rue du Docteur Roux 25, F-75724 Paris Cedex 15, France.

    • David Prangishvili
    •  & Patrick Forterre
  2. Danish Archaea Centre, Institute of Molecular Biology, Copenhagen University, Sølvgade 83H, DK-1307 Copenhagen K, Denmark.

    • Roger A. Garrett

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Competing interests

The authors declare no competing financial interests.

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Correspondence to David Prangishvili.

Glossary

Fusiform

An organism that is spindle-shaped: wider in the middle and tapering towards the ends.

Hyperthermophile

An organism that has an optimal growth temperature above 80°C.

Extreme halophile

An organism that requires extremely high levels of sodium chloride for growth.

Positively supercoiled DNA

A DNA molecule in which the number of topological links between the two strands is superior to the number of turns.

Lysogen

A bacterium or archaeon that contains a viral genome integrated into the chromosome.

Mesophilic

An organism that grows best in a temperature range between 20°C and 45°C.

Ribbon-helix-helix

(RHH). A structural motif consisting of four helices in an open array of two hairpins.

Helix-turn-helix

(HTH). A structural motif common in DNA-binding proteins; typically the second helix fits into the DNA major groove.

von Willebrand factor A motif

A structural motif that has been implicated in the formation of diverse types of specific protein–protein interaction and cell adhesion.

Small interfering RNA

Non-coding RNAs (around 22 nucleotides long) derived from the processing of long double-stranded RNA during RNA interference. They direct the destruction of mRNA targets that have the same sequence.

Micro RNA

A short (21–22-nucleotide) RNA silencing trigger that is processed from short stem–loop precursors that are encoded in the genomes of metazoans and certain viruses.

Last universal common ancestor

The progenitor from which all current life is thought to have evolved.

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https://doi.org/10.1038/nrmicro1527

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