Abstract
Of the three domains of life (Eukarya, Bacteria, and Archaea), the least understood is Archaea and its associated viruses. Many Archaea are extremophiles, with species that are capable of growth at some of the highest temperatures and extremes of pH of all known organisms. Phylogenetic rRNA-encoding DNA analysis places many of the hyperthermophilic Archaea (species with an optimum growth > or = 80 degrees C) at the base of the universal tree of life, suggesting that thermophiles were among the first forms of life on earth. Very few viruses have been identified from Archaea as compared to Bacteria and Eukarya. We report here the structure of a hyperthermophilic virus isolated from an archaeal host found in hot springs in Yellowstone National Park. The sequence of the circular double-stranded DNA viral genome shows that it shares little similarity to other known genes in viruses or other organisms. By comparing the tertiary and quaternary structures of the coat protein of this virus with those of a bacterial and an animal virus, we find conformational relationships among all three, suggesting that some viruses may have a common ancestor that precedes the division into three domains of life >3 billion years ago.
MeSH Terms
Capsid/physiology
DNA Viruses/genetics,isolation & purification,physiology
Genome, Viral
Microscopy, Electron
Molecular Sequence Data
Protein Structure, Tertiary
Sulfolobus/virology
Authors & Affiliations
9 authors, click to expand affiliations / ORCID
Rice George
Thermal Biology Institute and Department of Microbiology, Montana State University, Bozeman, MT 59717, USA.
Tang Liang
Stedman Kenneth
Roberto Francisco
Spuhler Josh
Gillitzer Eric
Johnson John E
Douglas Trevor
Young Mark
References (28)
28 references, click to expand
-
Do viruses form lineages across different domains of life?
Res Microbiol. 2003 May;154(4):231-6
PMID: 12798226
-
Remarkable morphological diversity of viruses and virus-like particles in hot terrestrial environments.
Arch Virol. 2002 Dec;147(12):2419-29
PMID: 12491107
-
Relationships between fuselloviruses infecting the extremely thermophilic archaeon Sulfolobus: SSV1 and SSV2.
Res Microbiol. 2003 May;154(4):295-302
PMID: 12798235
-
Geographic barriers isolate endemic populations of hyperthermophilic archaea.
Science. 2003 Aug 15;301(5635):976-8
PMID: 12881573
-
AFV1, a novel virus infecting hyperthermophilic archaea of the genus acidianus.
Virology. 2003 Oct 10;315(1):68-79
PMID: 14592760
-
Cryo-electron microscopy of vitrified specimens.
Q Rev Biophys. 1988 May;21(2):129-228
PMID: 3043536
-
Image reconstruction reveals the complex molecular organization of adenovirus.
Cell. 1991 Oct 4;67(1):145-54
PMID: 1913814
-
Complete nucleotide sequence of the virus SSV1 of the archaebacterium Sulfolobus shibatae.
Virology. 1991 Nov;185(1):242-50
PMID: 1926776
-
Bacteriophage PRD1: a broad host range DSDNA tectivirus with an internal membrane.
Adv Virus Res. 1995;45:281-319
PMID: 7793328
-
DNA packaging orders the membrane of bacteriophage PRD1.
EMBO J. 1995 Dec 15;14(24):6078-86
PMID: 8557027
-
SPIDER and WEB: processing and visualization of images in 3D electron microscopy and related fields.
J Struct Biol. 1996 Jan-Feb;116(1):190-9
PMID: 8742743
-
Evidence of viral capsid dynamics using limited proteolysis and mass spectrometry.
J Biol Chem. 1998 Jan 9;273(2):673-6
PMID: 9422714
-
Antiviral agent blocks breathing of the common cold virus.
Proc Natl Acad Sci U S A. 1998 Jun 9;95(12):6774-8
PMID: 9618488
-
Genetic elements in the extremely thermophilic archaeon Sulfolobus.
Extremophiles. 1998 Aug;2(3):131-40
PMID: 9783157
-
Normalized nucleotide frequencies allow the definition of archaeal promoter elements for different archaeal groups and reveal base-specific TFB contacts upstream of the TATA box.
Mol Microbiol. 1999 Mar;31(5):1589-92
PMID: 10200975
-
Extremophiles and their adaptation to hot environments.
FEBS Lett. 1999 Jun 4;452(1-2):22-5
PMID: 10376671
-
A novel virus family, the Rudiviridae: Structure, virus-host interactions and genome variability of the sulfolobus viruses SIRV1 and SIRV2.
Genetics. 1999 Aug;152(4):1387-96
PMID: 10430569
-
Viral evolution revealed by bacteriophage PRD1 and human adenovirus coat protein structures.
Cell. 1999 Sep 17;98(6):825-33
PMID: 10499799
-
Evolutionary insights from studies on viruses of hyperthermophilic archaea.
Res Microbiol. 2003 May;154(4):289-94
PMID: 12798234
-
EMAN: semiautomated software for high-resolution single-particle reconstructions.
J Struct Biol. 1999 Dec 1;128(1):82-97
PMID: 10600563
-
A novel lipothrixvirus, SIFV, of the extremely thermophilic crenarchaeon Sulfolobus.
Virology. 2000 Feb 15;267(2):252-66
PMID: 10662621
-
Viruses of the extremely thermophilic archaeon Sulfolobus.
Trends Microbiol. 2001 Jan;9(1):39-43
PMID: 11166242
-
The complete genome of the crenarchaeon Sulfolobus solfataricus P2.
Proc Natl Acad Sci U S A. 2001 Jul 3;98(14):7835-40
PMID: 11427726
-
Frequency of morphological phage descriptions in the year 2000. Brief review.
Arch Virol. 2001;146(5):843-57
PMID: 11448025
-
Complete genome sequence of an aerobic thermoacidophilic crenarchaeon, Sulfolobus tokodaii strain7.
DNA Res. 2001 Aug 31;8(4):123-40
PMID: 11572479
-
Viruses from extreme thermal environments.
Proc Natl Acad Sci U S A. 2001 Nov 6;98(23):13341-5
PMID: 11606757
-
Angular reconstitution: a posteriori assignment of projection directions for 3D reconstruction.
Ultramicroscopy. 1987;21(2):111-23
PMID: 12425301
-
The structure and evolution of the major capsid protein of a large, lipid-containing DNA virus.
Proc Natl Acad Sci U S A. 2002 Nov 12;99(23):14758-63
PMID: 12411581