The giant mimivirus 1.2 Mb genome is elegantly organized into a 30 nm diameter helical protein shield

  1. Alejandro Villalta
  2. Alain Schmitt
  3. Leandro F Estrozi
  4. Emmanuelle RJ Quemin
  5. Jean-Marie Alempic
  6. Audrey Lartigue
  7. Vojtěch Pražák
  8. Lucid Belmudes
  9. Daven Vasishtan
  10. Agathe MG Colmant
  11. Flora A Honoré
  12. Yohann Couté
  13. Kay Grünewald
  14. Chantal Abergel  Is a corresponding author
  1. Aix-Marseille University, CNRS-AMU UMR7256, France
  2. Univ. Grenoble Alpes, CNRS, CEA,, France
  3. University of Hamburg, Germany
  4. Université Grenoble Alpes, France

Abstract

Mimivirus is the prototype of the Mimiviridae family of giant dsDNA viruses. Little is known about the organization of the 1.2 Mb genome inside the membrane-limited nucleoid filling the ~0.5 µm icosahedral capsids. Cryo-electron microscopy, cryo-electron tomography and proteomics revealed that it is encased into a ~30 nm diameter helical protein shell surprisingly composed of two GMC-type oxidoreductases, which also form the glycosylated fibrils decorating the capsid. The genome is arranged in 5- or 6-start left-handed super-helices, with each DNA-strand lining the central channel. This luminal channel of the nucleoprotein fiber is wide enough to accommodate oxidative stress proteins and RNA polymerase subunits identified by proteomics. Such elegant supramolecular organization would represent a remarkable evolutionary strategy for packaging and protecting the genome, in a state ready for immediate transcription upon unwinding in the host cytoplasm. The parsimonious use of the same protein in two unrelated substructures of the virion is unexpected for a giant virus with thousand genes at its disposal.

Data availability

Mimivirus reunion genome has been deposited under the following accession number: BankIt2382307 Seq1 MW004169.3D reconstruction maps and the corresponding PDB have been deposited to EMDB (Deposition number Cl1a: 7YX4, EMD-14354; Cl1a focused refined: D_1292117739; Cl3a: 7YX5, EMD-14355; Cl2: 7YX3, EMD-14353).The mass spectrometry proteomics data have been deposited to the ProteomeXchange Consortium via the PRIDE partner repository with the dataset identifier PXD021585 and 10.6019/PXD021585.The tomograms have been deposited in EMPIAR under accession number 1131 and tomograms video are provided with the article.

The following data sets were generated

Article and author information

Author details

  1. Alejandro Villalta

    Aix-Marseille University, CNRS-AMU UMR7256, Marseille, France
    Competing interests
    The authors declare that no competing interests exist.
  2. Alain Schmitt

    Aix-Marseille University, CNRS-AMU UMR7256, Marseille, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3565-8692
  3. Leandro F Estrozi

    Univ. Grenoble Alpes, CNRS, CEA,, Grenoble, France
    Competing interests
    The authors declare that no competing interests exist.
  4. Emmanuelle RJ Quemin

    Centre for Structural Systems Biology, University of Hamburg, Hamburg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  5. Jean-Marie Alempic

    Aix-Marseille University, CNRS-AMU UMR7256, Marseille, France
    Competing interests
    The authors declare that no competing interests exist.
  6. Audrey Lartigue

    Aix-Marseille University, CNRS-AMU UMR7256, Marseille, France
    Competing interests
    The authors declare that no competing interests exist.
  7. Vojtěch Pražák

    Centre for Structural Systems Biology, University of Hamburg, Hamburg, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8149-218X
  8. Lucid Belmudes

    Institut de Biosciences et Biotechnologies de Grenoble, Université Grenoble Alpes, Grenoble, France
    Competing interests
    The authors declare that no competing interests exist.
  9. Daven Vasishtan

    Centre for Structural Systems Biology, University of Hamburg, Hamburg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  10. Agathe MG Colmant

    Aix-Marseille University, CNRS-AMU UMR7256, Marseille, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2004-4073
  11. Flora A Honoré

    Aix-Marseille University, CNRS-AMU UMR7256, Marseille, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0390-8730
  12. Yohann Couté

    Institut de Biosciences et Biotechnologies de Grenoble, Université Grenoble Alpes, Grenoble, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3896-6196
  13. Kay Grünewald

    Centre for Structural Systems Biology, University of Hamburg, Hamburg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  14. Chantal Abergel

    Aix-Marseille University, CNRS-AMU UMR7256, Marseille, France
    For correspondence
    Chantal.Abergel@igs.cnrs-mrs.fr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1875-4049

Funding

European Research Council (832601)

  • Chantal Abergel

Agence Nationale de la Recherche (ANR-16-CE11-0033-01)

  • Chantal Abergel

Agence Nationale de la Recherche (ANR-10-INBS-08-01)

  • Yohann Couté

Agence Nationale de la Recherche (ANR-17-EURE-0003)

  • Yohann Couté

Wellcome Trust (107806/Z/15/Z)

  • Kay Grünewald

Deutsche Forschungsgemeinschaft (INST 152/772-1|152/774-1|152/775-1|152/776-1)

  • Kay Grünewald

Alexander von Humboldt-Stiftung (FRA 1200789 HFST-P)

  • Emmanuelle RJ Quemin

Agence Nationale de la Recherche (ANR-10-INBS-04)

  • Chantal Abergel

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Adam Frost, University of California, San Francisco (Adjunct), United States

Publication history

  1. Received: February 4, 2022
  2. Accepted: July 27, 2022
  3. Accepted Manuscript published: July 28, 2022 (version 1)

Copyright

© 2022, Villalta et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Alejandro Villalta
  2. Alain Schmitt
  3. Leandro F Estrozi
  4. Emmanuelle RJ Quemin
  5. Jean-Marie Alempic
  6. Audrey Lartigue
  7. Vojtěch Pražák
  8. Lucid Belmudes
  9. Daven Vasishtan
  10. Agathe MG Colmant
  11. Flora A Honoré
  12. Yohann Couté
  13. Kay Grünewald
  14. Chantal Abergel
(2022)
The giant mimivirus 1.2 Mb genome is elegantly organized into a 30 nm diameter helical protein shield
eLife 11:e77607.
https://doi.org/10.7554/eLife.77607

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