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Hot crenarchaeal viruses reveal deep evolutionary connections

Key Points

  • Viruses that infect the Crenarchaeota are represented by 20 cultured isolates that can infect members of four genera. These viruses represent up to nine new families of viruses owing to their distinctive morphologies and unique genome contents.

  • Acidic hot springs, with temperatures greater than 75°C and pH lower than 4.0, are typically dominated by a wide diversity of crenarchaea. Although molecular signatures of crenarchaea have been detected in a wide range of environments, all of the cultured members are thermophilic and many are acidophilic.

  • Virus morphology might indicate evolutionary history. The spindle-shaped morphology seems to be limited to the Archaea with isolates infecting both the Euryarchaeota and the Crenarchaeota. The icosahedral morphology seems to share an evolutionary connection with viruses infecting the Euryarchaeota as well as the Bacteria and Eukarya.

  • All of the isolated crenarchaeal viruses contain dsDNA genomes, most of which have been completely sequenced. Sequencing has revealed few ORFs with similarity to known genes in the public databases, however, threading algorithms and structural studies have led to possible functions being proposed for some of the proteins. As more genomes are sequenced it is becoming clear that some of the genes are shared between individual viruses and groups of viruses.

  • Little is known about the replication cycle for most of the isolated crenarcheal viruses. SSV-like viruses are known to integrate into the genome of the host, as does ATV. Unlike the SSV-like viruses, ATV lyses the host cell when it is induced and then undergoes an extracellular maturation under conditions ideal for its host.

  • Viruses that infect the Crenarchaeota can be isolated from around the world. Although viruses with similar morphology can be isolated from geographically separated hot springs, it is unclear if the viruses are genetically distinct or globally linked. The extent and distribution of the total diversity of crenarchaeal viruses remains to be determined.

Abstract

The discovery of archaeal viruses provides insights into the fundamental biochemistry and evolution of the Archaea. Recent studies have identified a wide diversity of archaeal viruses within the hot springs of Yellowstone National Park and other high-temperature environments worldwide. These viruses are often morphologically unique and code for genes with little similarity to other known genes in the biosphere, a characteristic that has complicated efforts to trace their evolutionary history. Comparative genomics combined with structural analysis indicate that spindle-shaped virus lineages might be unique to the Archaea, whereas other icosahedral viruses might share a common lineage with viruses of Bacteria and Eukarya. These studies provide insights into the evolutionary history of viruses in all three domains of life.

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Figure 1: Typical virus morphologies observed in both environmental samples and enrichment cultures established from hot, acidic environments.
Figure 2: Comparison of the evolutionary history of different types of virus compared with the 16S rDNA-based tree of life.
Figure 3: Cryo-transmission-electron microscopy image reconstruction of Sulfolobus turreted icosahedral virus.
Figure 4: Schematic representations of selected crenarchaeal viral genomes illustrating examples of shared gene families.

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Acknowledgements

We would like to acknowledge the pioneering work of W. Zillig in the study of archaeal viruses. Much of our work described in this review was supported by funding from the National Science Foundation and NASA.

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DATABASES

Entrez Genome

ATV

HSV-1

PBCV1

PRD1

SH1

SSV1

SSV2

SSVRH

STIV

STSV1

Sulfolobus tengchongensis

Entrez Genome Project

Methanococcus voltae

FURTHER INFORMATION

Mark Young's homepage

3D-PSSM

Phyre

Fugue

Chimera

Universal Virus Database of the International Committee on Taxonomy of Viruses

Glossary

Methanogen

Anaerobic archaeon that produces methane as a waste product of autotrophic metabolism.

Halophile

An aerobic organism that requires salt for survival. Extreme halophiles (environmental salt concentration >15%) are all archaea.

Thermophile

An organism with an optimal growth rate above 50°C. Organisms with optimal growth rates at temperatures greater than 75°C are classified as hyperthermophiles.

Polyamine

An organic compound synthesized in cells and required for growth. These compounds have two or more amine groups and are positively charged, enabling them to bind DNA.

Glycosyltransferase

An enzyme that tranfers glycosyl (carbohydrate radical) from one compound to another. There are several families of these enzymes.

Tyrosine recombinase

A diverse group of proteins involved in recombination between DNA at specific sites. Functions include integration of virus genomes, relaxation of DNA supercoils, conjugation and genome separation during cell division.

Holliday junction resolvase

An enzyme that cleaves concatamer junctions to create linear duplex DNA during genome replication in poxviruses.

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Ortmann, A., Wiedenheft, B., Douglas, T. et al. Hot crenarchaeal viruses reveal deep evolutionary connections. Nat Rev Microbiol 4, 520–528 (2006). https://doi.org/10.1038/nrmicro1444

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