The structure of a thermophilic archaeal virus shows a double-stranded DNA viral capsid type that spans all domains of life

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.

Fig. 1.

Genome map of the 17,663-bp circular dsDNA STIV genome. The 36 predicted ORFs >50 amino acids in length and associated with TATA-like elements are indicated. Reading frames plus 1 (red), 2 (blue), 3 (green), and reading frames minus 1 (black) and minus 3 (purple) are indicated. The major structural protein (B345) identified by mass spectrometry is indicated (^*).

Fig. 2.

CryoTEM and image reconstruction of STIV. (A) STIV surface features with turret-like projections extending from each of the 5-fold vertices. (B) Side view of turret-like projections extending 13 nm above the surface of the virus surface. (C) Cross section showing a 3-nm central channel in a single turret-like projection. (D) Electron micrograph of vitrified STIV sample recorded at an underfocus of 1.5 μm. (Bar = 1,000 Å.) (E) A 7.5-Å-thick equatorial section of the cryoelectron microscopy map viewed down the icosahedral 2-fold axis. An arrowhead and a pair of arrows indicate the channel in the 5-fold turret and two leaflets of the putative bilayer, respectively.

Fig. 3.

(A) Surface capsomer architecture of T = 31 STIV (Left), adenovirus (Center), and PRD1 (Right). The icosahedral asymmetric unit (triangle) consists of five trimers (pseudohexamers) of the major capsid protein plus one additional minor capsid protein at the 5-fold vertex. (B) The x-ray crystal structures (ribbon diagrams) of PRD1 (29) (Left) and adenovirus hexon (29) (Right) major coat proteins showing their similar folds. Both contain the “double-jellyroll” motif (red and green). (C) Fitting of the PRD1 P3 coat protein x-ray crystal structure (ribbons) into the STIV cryoimage reconstruction density (blue). Fitting of three trimers corresponding to an icosahedral asymmetric unit of the capsid (Upper). Fitting of a trimer (Lower). The ribbon diagrams of the x-ray atomic structure were ramp-colored from the N terminus of the first (red) to the C terminus of the last trimer (blue).