Structural studies of Acidianus tailed spindle virus reveal a structural paradigm used in the assembly of spindle-shaped viruses

Abstract

The spindle-shaped virion morphology is common among archaeal viruses, where it is a defining characteristic of many viral families. However, structural heterogeneity intrinsic to spindle-shaped viruses has seriously hindered efforts to elucidate the molecular architecture of these lemon-shaped capsids. We have utilized a combination of cryo-electron microscopy and X-ray crystallography to study tailed spindle virus (ATSV). These studies reveal the architectural principles that underlie assembly of a spindle-shaped virus. Cryo-electron tomography shows a smooth transition from the spindle-shaped capsid into the tubular-shaped tail and allows low-resolution structural modeling of individual virions. Remarkably, higher-dose 2D micrographs reveal a helical surface lattice in the spindle-shaped capsid. Consistent with this, crystallographic studies of the major capsid protein reveal a decorated four-helix bundle that packs within the crystal to form a four-start helical assembly with structural similarity to the tube-shaped tail structure of ATSV and other tailed, spindle-shaped viruses. Combined, this suggests that the spindle-shaped morphology of the ATSV capsid is formed by a multistart helical assembly with a smoothly varying radius and allows construction of a pseudoatomic model for the lemon-shaped capsid that extends into a tubular tail. The potential advantages that this novel architecture conveys to the life cycle of spindle-shaped viruses, including a role in DNA ejection, are discussed.

Comparative genetic and genomic analysis of the novel fusellovirus Sulfolobus spindle-shaped virus 10

“…Recently proposed structural models of hyperthermophilic archaeal viruses Aeropyrum pernix bacilliform virus 1 (APBV1) ( Ptchelkine et al. 2017 ) and Acidianus tailed spindle virus ( Hochstein et al. 2018 ) may provide insight into the morphological perturbations of VP3 deletions in SSV1 and SSV10.…”

Archaeal Viruses from High-Temperature Environments

“…Cryo-tomography has been used to study the interaction of the STIV turrets with fibers extending from the host cell surface (unpublished data [ 64 ]). The large spindle-shaped archaeal virus, Acidianus tailed spindle virus (ATSV), was recently examined by tomography and, unlike bacteriophages with distinct head and tail structures, the head and tail of ATSV appear to be a single continuous structure [ 92 ], suggesting a new virion assembly mechanism [ 93 ]. The capsid structure of a thermophilic virus MTIV was solved to 22Å using a combination of tomography and single particle reconstruction, revealing a new virion architecture [ 47 ].…”

“…For example, the large-tailed spindle virus ATSV was initially isolated directly from environmental hot spring samples, and its host identified using both viral FISH and cellular CRISPR/Cas analysis [ 43 ]. Prior to host identification, the major coat protein was identified, cloned, and the structure was solved [ 92 ], which lead to hypothesis about viral evolution, gene conservation, and novel mechanisms for viral [ 93 ]. One promising approach is the application of SCG to environmental samples.…”

The intriguing world of archaeal viruses

“…Some of these viruses assemble into previously unknown architectures. For example, Acidianus tailed spindle virus (ATSV) uses rope-like strands that slide against one other to assemble varying widths of its lemon-shaped capsid and tail, and packages the double stranded DNA (dsDNA) genome asymmetrically within capsid [2,3]. Typically, the only identifiable viral gene homologs in most archaeal virus genomes are to other archaeal viruses or their cellular hosts, with few having known functions.…”