The enigmatic archaeal virosphere

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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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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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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Correspondence to David Prangishvili or Mart Krupovic.

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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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