A packing for A-form DNA in an icosahedral virus

Fengbin Wang; Ying Liu; Zhangli Su; Tomasz Osinski; Guilherme A.P. de Oliveira; James F. Conway; Stefan Schouten; Mart Krupovic; David Prangishvili; Edward H. Egelman

doi:10.1073/pnas.1908242116

A packing for A-form DNA in an icosahedral virus

Fengbin Wang
, Ying Liu
, Zhangli Su
, Tomasz Osinski
, Guilherme A.P. de Oliveira
, James F. Conway
, Stefan Schouten
, Mart Krupovic
, David Prangishvili^*
, Edward H. Egelman

^*Corresponding author for this work

University of Virginia
University of Pittsburgh
Institut Pasteur Paris
Ivane Javakhishvili Tbilisi State University
Royal Netherlands Institute for Sea Research - NIOZ

Research output: Contribution to journal › Article › Academic › peer-review

Abstract

Studies on viruses infecting archaea living in the most extreme environments continue to show a remarkable diversity of structures, suggesting that the sampling continues to be very sparse. We have used electron cryo-microscopy to study at 3.7-Å resolution the structure of the Sulfolobus polyhedral virus 1 (SPV1), which was originally isolated from a hot, acidic spring in Beppu, Japan. The 2 capsid proteins with variant single jelly-roll folds form pentamers and hexamers which assemble into a T = 43 icosahedral shell. In contrast to tailed icosahedral double-stranded DNA (dsDNA) viruses infecting bacteria and archaea, and herpesviruses infecting animals and humans, where naked DNA is packed under very high pressure due to the repulsion between adjacent layers of DNA, the circular dsDNA in SPV1 is fully covered with a viral protein forming a nucleoprotein filament with attractive interactions between layers. Most strikingly, we have been able to show that the DNA is in an A-form, as it is in the filamentous viruses infecting hyperthermophilic acidophiles. Previous studies have suggested that DNA is in the B-form in bacteriophages, and our study is a direct visualization of the structure of DNA in an icosahedral virus.

Original language	English
Pages (from-to)	22591-22597
Number of pages	7
Journal	Proceedings of the National Academy of Sciences of the United States of America
Volume	116
Issue number	45
DOIs	https://doi.org/10.1073/pnas.1908242116
Publication status	Published - 5 Nov 2019

Funding

ACKNOWLEDGMENTS. This work was supported by NIH Grant GM122510 (to E.H.E.); the European Union’s Horizon 2020 Research and Innovation Program Grant 685778, project VIRUS X (to D.P.); and l’Agence Nationale de la Recherche Grant ANR-17-CE15-0005-01 (to M.K.). Imaging by the National Cancer Institute (NCI) National Cryo-EM Facility (Frederick National Laboratory for Cancer Research) was supported by contract HSSN261200800001E. We thank Dr. Ulrich Baxa and Dr. Thomas Edwards for their help in NCI data collection; the Ultrastructural BioImaging unit of Institut Pasteur for access to electron microscopes; and Dr. Wen Jiang (Purdue University) for very helpful discussions.

Keywords

Cryo-EM
DNA structure
Hyperthermophilic acidophiles

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10.1073/pnas.1908242116

packingFinal published version, 2.55 MBLicence: Taverne

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title = "A packing for A-form DNA in an icosahedral virus",

abstract = "Studies on viruses infecting archaea living in the most extreme environments continue to show a remarkable diversity of structures, suggesting that the sampling continues to be very sparse. We have used electron cryo-microscopy to study at 3.7-{\AA} resolution the structure of the Sulfolobus polyhedral virus 1 (SPV1), which was originally isolated from a hot, acidic spring in Beppu, Japan. The 2 capsid proteins with variant single jelly-roll folds form pentamers and hexamers which assemble into a T = 43 icosahedral shell. In contrast to tailed icosahedral double-stranded DNA (dsDNA) viruses infecting bacteria and archaea, and herpesviruses infecting animals and humans, where naked DNA is packed under very high pressure due to the repulsion between adjacent layers of DNA, the circular dsDNA in SPV1 is fully covered with a viral protein forming a nucleoprotein filament with attractive interactions between layers. Most strikingly, we have been able to show that the DNA is in an A-form, as it is in the filamentous viruses infecting hyperthermophilic acidophiles. Previous studies have suggested that DNA is in the B-form in bacteriophages, and our study is a direct visualization of the structure of DNA in an icosahedral virus.",

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A packing for A-form DNA in an icosahedral virus

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