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

Rebecca Hochstein, Daniel Bollschweiler, Sanjay Dharmavaram, Nathanael G. Lintner, Jürgen M. Plitzko, Robijn Bruinsma, Harald Engelhardt, Mark J. Young, William S. Klug, C. Martin Lawrence

Research output: Contribution to journalArticle

10 Scopus citations

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 Acidianus 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.

Original languageEnglish (US)
Pages (from-to)2120-2125
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume115
Issue number9
DOIs
StatePublished - Feb 27 2018

Keywords

  • ATSV
  • Archaea
  • Lemon-shaped
  • Spindle-shaped
  • Virus

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    Hochstein, R., Bollschweiler, D., Dharmavaram, S., Lintner, N. G., Plitzko, J. M., Bruinsma, R., Engelhardt, H., Young, M. J., Klug, W. S., & Martin Lawrence, C. (2018). Structural studies of acidianus tailed spindle virus reveal a structural paradigm used in the assembly of spindle-shaped viruses. Proceedings of the National Academy of Sciences of the United States of America, 115(9), 2120-2125. https://doi.org/10.1073/pnas.1719180115