Viruses of the Turriviridae: an emerging model system for studying archaeal virus-host interactions

Abstract

Viruses have played a central role in the evolution and ecology of cellular life since it first arose. Investigations into viral molecular biology and ecological dynamics have propelled abundant progress in our understanding of living systems, including genetic inheritance, cellular signaling and trafficking, and organismal development. As well, the discovery of viral lineages that infect members of all three domains suggest that these lineages originated at the earliest stages of biological evolution. Research into these viruses is helping to elucidate the conditions under which life arose, and the dynamics that directed its early development. Archaeal viruses have only recently become a subject of intense study, but investigations have already produced intriguing and exciting results. STIV was originally discovered in Yellowstone National Park and has been the focus of concentrated research. Through this research, a viral genetic system was created, a novel lysis mechanism was discovered, and the interaction of the virus with cellular ESCRT machinery was revealed. This review will summarize the discoveries within this group of viruses and will also discuss future work.

Keywords: Sulfolobus turreted icosahedral virus; Turriviridae; archaea; viral replication; virus; virus-host interaction.

Figure 1

Electron cryo-microscopy reconstruction of STIV. (A) The overall virus reconstruction is displayed with the different protein components individually colored (B345: light blue, A223: light pink, C381: purple) and with an icosahedral cage overlaid onto it. (B) Blow-up view of an icosahedral face with one capsid icosahedral asymmetric unit colored as in (A) and labeled (1–5 for the trimeric B345 capsomers and P for the A223 penton base). (C) Cross-section of the reconstruction revealing the presence of internal lipid envelop (gold) and the internal genome (red). Adapted from Veesler et al. (2013).

Figure 2

STIV structural proteins. (A) Ribbon representation of B345, the major capsid protein of STIV. β-strands are depicted in cyan, α-helices in yellow, loops in gray. The structure is composed of two domains, an N-terminal domain (left) and a C-terminal domain (right). Each domain adopts the jelly roll fold, which is composed of two four-stranded β-sheets. In the N-terminal domain, the first sheet is formed of strands B, I, D and G (BIDG) at the back of the structure, and the second sheet of strands C, H, E and F (CHEF) at the front of the structure. The two β-sheets pack against each other to form a β-sandwich. Similarly, the C-terminal jelly roll is composed of strands B′, I′, D′, and G’ in the B’I’D’G’ sheet, and strands C′, H′ E’, and F′ in the C’H’E’F′ sheet. Adapted from Khayat et al. (2005). (B) The structure of the STIV turret. β-strands emanating from the A55 membrane anchor are at the bottom, in blue, where they interdigitate with the N terminus of A223 to form a ten-stranded hemolysin-like β-barrel. The two-domain, double jelly roll structure of A223 is shown above that in pink, followed by the three-domain jelly roll structure of C381 in light blue, light purple, and dark purple at the top. To the right, an enlarged view of a single C381 protomer. The N-terminal jelly roll is at the bottom, the C-terminal jelly roll domain at the top. Adapted from Hartman et al. (2019).

Figure 3

Replication cycle of STIV. The several steps involved in host infection by STIV are shown, starting with viral attachment in the top left and ending with viral egress at the top right. Those steps that have been experimentally characterized are indicated by large black arrows and text, and those yet to be characterized are in dark red. The names of gene products originating from the virus are in black and those from the host are in grey. Smaller black and grey arrows indicate the involvement of virus and host gene products, respectively, in various processes of infection, and red arrows indicate hypothesized involvement.

Figure 4

Scanning electron micrograph (SEM) image of STIV1-induced pyramids on the surface of an infected Sulfolobus cell. Scale bar = 200 nm.

Figure 5

Initial viral attachment to pili. (A) Subtomographic average of STIV virions and pili show pilus recognition is mediated by interactions with the 2nd (light purple) and 3rd (dark purple) jelly roll domains of the C381 turret protein. To the right, an enlarged view of a single turret/pilus interaction. (B) Strictly conserved, surface exposed residues lie within these regions and potentially mediate recognition. These include Asn196 and Ser215 in domain 2, and Glu285 and Asn289 in domain 3. Adapted from Hartman et al. (2019).