Structure and cell biology of archaeal virus STIV

Abstract

Recent investigations of archaeal viruses have revealed novel features of their structures and life cycles when compared to eukaryotic and bacterial viruses, yet there are structure-based unifying themes suggesting common ancestral relationships among dsDNA viruses in the three kingdoms of life. Sulfolobus solfataricus and the infecting virus Sulfolobus turreted icosahedral virus (STIV) is one of the well-established model systems to study archaeal virus replication and viral-host interactions. Reliable laboratory conditions to propagate STIV and available genetic tools allowed structural characterization of the virus and viral components that lead to the proposal of common capsid ancestry with PRD1 (bacteriophage), Adenovirus (eukaryotic virus) and PBCV (chlorellavirus). Microarray and proteomics approaches systematically analyzed viral replication and the corresponding host responses. Cellular cryo-electron tomography and thin-section EM studies uncovered the assembly and maturation pathway of STIV and revealed dramatic cellular ultra-structure changes upon infection. The viral-induced pyramid-like protrusions on cell surfaces represent a novel viral release mechanism and previously uncharacterized functions in viral replication.

Fig 1

The structures of STIV. (A) The surface representation of STIV single particle cryo-EM reconstruction. The turret-like vertices are colored in yellow, the capsid shell in cyan, the lipid layer in red, and the genome in blue. (B) The crystal structure of the STIV major capsid protein. α-helices, β-strands and coils are colored in yellow, in cyan, and in gray respectively. (C) C^α- trace of the major capsid protein overlaid onto the difference map of the STIV cryoEM reconstruction. The outer viral membrane leaflet closely follows the capsid shell is shown in dark gray, the minor capsid proteins (PVI) are in blue, and the vertex appendage is in yellow. The proposed C-terminal helices for the major capsid protein subunits are modeled into the difference map to show the interaction with the outer leaflet.

Fig 2. Whole cell cryo electron tomography of Sulfolubs infected with STIV

(A) A computationally isolated tomographic slice of Sulfolubs infected with STIV. SL, s-layer; PS, periplasmic space; CM, cytoplasmic membrane; Pyr, pyramid like protrusion; STIV, STIV particles. (B) Subtomographic slices displaying STIV virions, procapsids and partially assembled particles that contain parts of capsid and membrane viewed perpendicular to the direction of the beam (x-y plane). (C) The model representation of the viral distribution in a cell with cell periphery outlined in gray, virions in blue and procapsids in red. (D) Surface representations of a pyramid in 3D viewed from the side and the top of the structure.