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Viruses of the Archaea: a unifying view

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.

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.

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Figure 1: Electron micrographs of archaeal viruses with exceptional morphologies.
Figure 2: Extracellular tail development of Acidianus two-tailed virus (ATV).
Figure 3: Electron micrographs of linear and spherical viruses of the archaea.
Figure 4: Electron micrographs of head-tail viruses of archaea and bacteria.
Figure 5: Genome structure of Acidianus two-tailed virus (ATV).
Figure 6: The families of dsDNA viruses associated with the three domains of life.

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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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Correspondence to David Prangishvili.

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DATABASES

Entrez Genome

AFV1

His1

His2

PBCV1

PSV

SH1

SIFV

SIRV1

STIV

STSV1

TTSV1

Entrez Genome Project

Methanococcus voltae

Pyrococcus abyssi

Sulfolobus solfataricus P2

FURTHER INFORMATION

David Prangishvili's homepage

ICTV

The Sulfolobus Database

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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Prangishvili, D., Forterre, P. & Garrett, R. Viruses of the Archaea: a unifying view. Nat Rev Microbiol 4, 837–848 (2006). https://doi.org/10.1038/nrmicro1527

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