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 journalArticlepeer-review

23 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

Bibliographical note

Funding Information:
C.M.L. thanks Professor Wolfgang Baumeister for the opportunity to do sabbatical work at the Max Planck Institute of Biochemistry, where the cryo- TEM work was done. This work was supported by National Science Foundation Grants MCB-1413534 (to C.M.L.), DEB-4W4596 (to M.J.Y.), and DMR-1309423 (to R.B.). This study is dedicated to the memory of Professor William “Bill” Klug, whose infectious enthusiasm for studies of viral structure and function were an inspiration to all who worked with him.

Funding Information:
ACKNOWLEDGMENTS. C.M.L. thanks Professor Wolfgang Baumeister for the opportunity to do sabbatical work at the Max Planck Institute of Biochemistry, where the cryo-TEM work was done. This work was supported by National Science Foundation Grants MCB-1413534 (to C.M.L.), DEB-4W4596 (to M.J.Y.), and DMR-1309423 (to R.B.). This study is dedicated to the memory of Professor William “Bill” Klug, whose infectious enthusiasm for studies of viral structure and function were an inspiration to all who worked with him.

Keywords

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

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