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CryoEM structure and assembly mechanism of a bacterial virus genome gatekeeper

Author

Listed:
  • Igor Orlov

    (Université de Strasbourg
    University of Glasgow, Scottish Centre for Macromolecular Imaging)

  • Stéphane Roche

    (Université Paris-Saclay, CEA, CNRS, Institute for Integrative Biology of the Cell (I2BC))

  • Sandrine Brasilès

    (Université Paris-Saclay, CEA, CNRS, Institute for Integrative Biology of the Cell (I2BC))

  • Natalya Lukoyanova

    (Birkbeck College)

  • Marie-Christine Vaney

    (Institut Pasteur, Université Paris Cité, CNRS UMR3569, Unité de Virologie Structurale)

  • Paulo Tavares

    (Université Paris-Saclay, CEA, CNRS, Institute for Integrative Biology of the Cell (I2BC))

  • Elena V. Orlova

    (Birkbeck College)

Abstract

Numerous viruses package their dsDNA genome into preformed capsids through a portal gatekeeper that is subsequently closed. We report the structure of the DNA gatekeeper complex of bacteriophage SPP1 (gp612gp1512gp166) in the post-DNA packaging state at 2.7 Å resolution obtained by single particle cryo-electron microscopy. Comparison of the native SPP1 complex with assembly-naïve structures of individual components uncovered the complex program of conformational changes leading to its assembly. After DNA packaging, gp15 binds via its C-terminus to the gp6 oligomer positioning gp15 subunits for oligomerization. Gp15 refolds its inner loops creating an intersubunit β-barrel that establishes different types of contacts with six gp16 subunits. Gp16 binding and oligomerization is accompanied by folding of helices that close the portal channel to keep the viral genome inside the capsid. This mechanism of assembly has broad functional and evolutionary implications for viruses of the prokaryotic tailed viruses-herpesviruses lineage.

Suggested Citation

  • Igor Orlov & Stéphane Roche & Sandrine Brasilès & Natalya Lukoyanova & Marie-Christine Vaney & Paulo Tavares & Elena V. Orlova, 2022. "CryoEM structure and assembly mechanism of a bacterial virus genome gatekeeper," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-34999-8
    DOI: 10.1038/s41467-022-34999-8
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    References listed on IDEAS

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    1. Lei Sun & Xinzheng Zhang & Song Gao & Prashant A. Rao & Victor Padilla-Sanchez & Zhenguo Chen & Siyang Sun & Ye Xiang & Sriram Subramaniam & Venigalla B. Rao & Michael G. Rossmann, 2015. "Cryo-EM structure of the bacteriophage T4 portal protein assembly at near-atomic resolution," Nature Communications, Nature, vol. 6(1), pages 1-11, November.
    2. Jingwei Xu & Dianhong Wang & Miao Gui & Ye Xiang, 2019. "Structural assembly of the tailed bacteriophage ϕ29," Nature Communications, Nature, vol. 10(1), pages 1-16, December.
    3. Douglas E. Smith & Sander J. Tans & Steven B. Smith & Shelley Grimes & Dwight L. Anderson & Carlos Bustamante, 2001. "The bacteriophage φ29 portal motor can package DNA against a large internal force," Nature, Nature, vol. 413(6857), pages 748-752, October.
    4. Alan A. Simpson & Yizhi Tao & Petr G. Leiman & Mohammed O. Badasso & Yongning He & Paul J. Jardine & Norman H. Olson & Marc C. Morais & Shelley Grimes & Dwight L. Anderson & Timothy S. Baker & Michael, 2000. "Structure of the bacteriophage φ29 DNA packaging motor," Nature, Nature, vol. 408(6813), pages 745-750, December.
    5. Zhihai Li & Jingjing Pang & Lili Dong & Xuekui Yu, 2021. "Structural basis for genome packaging, retention, and ejection in human cytomegalovirus," Nature Communications, Nature, vol. 12(1), pages 1-14, December.
    6. Ana Cuervo & Montserrat Fàbrega-Ferrer & Cristina Machón & José Javier Conesa & Francisco J. Fernández & Rosa Pérez-Luque & Mar Pérez-Ruiz & Joan Pous & M. Cristina Vega & José L. Carrascosa & Miquel , 2019. "Structures of T7 bacteriophage portal and tail suggest a viral DNA retention and ejection mechanism," Nature Communications, Nature, vol. 10(1), pages 1-11, December.
    7. Yun-Tao Liu & Jonathan Jih & Xinghong Dai & Guo-Qiang Bi & Z. Hong Zhou, 2019. "Cryo-EM structures of herpes simplex virus type 1 portal vertex and packaged genome," Nature, Nature, vol. 570(7760), pages 257-261, June.
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