The Enigmatic Archaeal Virosphere

Overview

Journal Nat Rev Microbiol

Specialties Infectious Diseases
Microbiology

Date 2017 Nov 11

PMID 29123227

Citations 100

Authors

David Prangishvili

Dennis H Bamford

Patrick Forterre

Jaime Iranzo

Eugene V Koonin

Mart Krupovic

Affiliations

Soon will be listed here.

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.

Citing Articles

Architecture and Assembly of Structurally Complex Viruses.

San Martin C Subcell Biochem. 2024; 105:431-467.

PMID: 39738954 DOI: 10.1007/978-3-031-65187-8_12.

Metagenomic characterization of viruses and mobile genetic elements associated with the DPANN archaeal superphylum.

Wu Z, Liu S, Ni J Nat Microbiol. 2024; 9(12):3362-3375.

PMID: 39448846 DOI: 10.1038/s41564-024-01839-y.

DNA polymerase swapping in Caudoviricetes bacteriophages.

Yutin N, Tolstoy I, Mutz P, Wolf Y, Krupovic M, Koonin E Virol J. 2024; 21(1):200.

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Cell-to-cell interactions revealed by cryo-tomography of a DPANN co-culture system.

Johnson M, Shepherd D, Sakai H, Mudaliyar M, Pandurangan A, Short F Nat Commun. 2024; 15(1):7066.

PMID: 39152123 PMC: 11329633. DOI: 10.1038/s41467-024-51159-2.

Jumping DNA polymerases in bacteriophages.

Yutin N, Tolstoy I, Mutz P, Wolf Y, Krupovic M, Koonin E bioRxiv. 2024; .

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References

Bidgood S, Mercer J . Cloak and Dagger: Alternative Immune Evasion and Modulation Strategies of Poxviruses. Viruses. 2015; 7(8):4800-25. PMC: 4576205. DOI: 10.3390/v7082844. View

Pietila M, Laurinmaki P, Russell D, Ko C, Jacobs-Sera D, Butcher S . Insights into head-tailed viruses infecting extremely halophilic archaea. J Virol. 2013; 87(6):3248-60. PMC: 3592136. DOI: 10.1128/JVI.03397-12. View

Pietila M, Laurinavicius S, Sund J, Roine E, Bamford D . The single-stranded DNA genome of novel archaeal virus halorubrum pleomorphic virus 1 is enclosed in the envelope decorated with glycoprotein spikes. J Virol. 2009; 84(2):788-98. PMC: 2798366. DOI: 10.1128/JVI.01347-09. View

Rice G, Tang L, Stedman K, Roberto F, Spuhler J, Gillitzer E . 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 U S A. 2004; 101(20):7716-20. PMC: 419672. DOI: 10.1073/pnas.0401773101. View

Prangishvili D, Arnold H, Gotz D, Ziese U, Holz I, Kristjansson J . A novel virus family, the Rudiviridae: Structure, virus-host interactions and genome variability of the sulfolobus viruses SIRV1 and SIRV2. Genetics. 1999; 152(4):1387-96. PMC: 1460677. DOI: 10.1093/genetics/152.4.1387. View

Porter K, Kukkaro P, Bamford J, Bath C, Kivela H, Dyall-Smith M . SH1: A novel, spherical halovirus isolated from an Australian hypersaline lake. Virology. 2005; 335(1):22-33. DOI: 10.1016/j.virol.2005.01.043. View

Quax T, Lucas S, Reimann J, Pehau-Arnaudet G, Prevost M, Forterre P . Simple and elegant design of a virion egress structure in Archaea. Proc Natl Acad Sci U S A. 2011; 108(8):3354-9. PMC: 3044396. DOI: 10.1073/pnas.1018052108. View

Prangishvili D . Archaeal viruses: living fossils of the ancient virosphere?. Ann N Y Acad Sci. 2015; 1341:35-40. DOI: 10.1111/nyas.12710. View

Xiang X, Chen L, Huang X, Luo Y, She Q, Huang L . Sulfolobus tengchongensis spindle-shaped virus STSV1: virus-host interactions and genomic features. J Virol. 2005; 79(14):8677-86. PMC: 1168784. DOI: 10.1128/JVI.79.14.8677-8686.2005. View

10.

Forterre P . The common ancestor of archaea and eukarya was not an archaeon. Archaea. 2013; 2013:372396. PMC: 3855935. DOI: 10.1155/2013/372396. View

11.

Hurley J, Hanson P . Membrane budding and scission by the ESCRT machinery: it's all in the neck. Nat Rev Mol Cell Biol. 2010; 11(8):556-66. PMC: 2922035. DOI: 10.1038/nrm2937. View

12.

Veesler D, Ng T, Sendamarai A, Eilers B, Lawrence C, Lok S . Atomic structure of the 75 MDa extremophile Sulfolobus turreted icosahedral virus determined by CryoEM and X-ray crystallography. Proc Natl Acad Sci U S A. 2013; 110(14):5504-9. PMC: 3619359. DOI: 10.1073/pnas.1300601110. View

13.

Bize A, Karlsson E, Ekefjard K, Quax T, Pina M, Prevost M . A unique virus release mechanism in the Archaea. Proc Natl Acad Sci U S A. 2009; 106(27):11306-11. PMC: 2708744. DOI: 10.1073/pnas.0901238106. View

14.

Pietila M, Demina T, Atanasova N, Oksanen H, Bamford D . Archaeal viruses and bacteriophages: comparisons and contrasts. Trends Microbiol. 2014; 22(6):334-44. DOI: 10.1016/j.tim.2014.02.007. View

15.

DiMaio F, Yu X, Rensen E, Krupovic M, Prangishvili D, Egelman E . Virology. A virus that infects a hyperthermophile encapsidates A-form DNA. Science. 2015; 348(6237):914-7. PMC: 5512286. DOI: 10.1126/science.aaa4181. View

16.

Szymczyna B, Taurog R, Young M, Snyder J, Johnson J, Williamson J . Synergy of NMR, computation, and X-ray crystallography for structural biology. Structure. 2009; 17(4):499-507. PMC: 2705668. DOI: 10.1016/j.str.2009.03.001. View

17.

Nishimura Y, Watai H, Honda T, Mihara T, Omae K, Roux S . Environmental Viral Genomes Shed New Light on Virus-Host Interactions in the Ocean. mSphere. 2017; 2(2). PMC: 5332604. DOI: 10.1128/mSphere.00359-16. View

18.

Sinclair R, Ravantti J, Bamford D . Nucleic and Amino Acid Sequences Support Structure-Based Viral Classification. J Virol. 2017; 91(8). PMC: 5375668. DOI: 10.1128/JVI.02275-16. View

19.

Vestergaard G, Haring M, Peng X, Rachel R, Garrett R, Prangishvili D . A novel rudivirus, ARV1, of the hyperthermophilic archaeal genus Acidianus. Virology. 2005; 336(1):83-92. DOI: 10.1016/j.virol.2005.02.025. View

20.

Adriaenssens E, van Zyl L, Cowan D, Trindade M . Metaviromics of Namib Desert Salt Pans: A Novel Lineage of Haloarchaeal Salterproviruses and a Rich Source of ssDNA Viruses. Viruses. 2016; 8(1). PMC: 4728574. DOI: 10.3390/v8010014. View