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Melbournevirus-encoded histone doublets are recruited to virus particles and form destabilized nucleosome-like structures

View ORCID ProfileYang Liu, View ORCID ProfileChelsea Marie Toner, View ORCID ProfileNadege Philippe, View ORCID ProfileSandra Jeudy, View ORCID ProfileKeda Zhou, View ORCID ProfileSamuel Bowerman, View ORCID ProfileAlison White, Garrett Edwards, View ORCID ProfileChantal Abergel, View ORCID ProfileKarolin Luger
doi: https://doi.org/10.1101/2021.04.29.441998
Yang Liu
1Department of Biochemistry, University of Colorado at Boulder, 80309 Boulder, Colorado
2Howard Hughes Medical Institute
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Chelsea Marie Toner
1Department of Biochemistry, University of Colorado at Boulder, 80309 Boulder, Colorado
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Nadege Philippe
3Aix–Marseille University, Centre National de la Recherche Scientifique, Information Génomique & Structurale, Unité Mixte de Recherche 7256 (Institut de Microbiologie de la Méditerranée, FR3479, IM2B), 13288 Marseille Cedex 9, France
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Sandra Jeudy
3Aix–Marseille University, Centre National de la Recherche Scientifique, Information Génomique & Structurale, Unité Mixte de Recherche 7256 (Institut de Microbiologie de la Méditerranée, FR3479, IM2B), 13288 Marseille Cedex 9, France
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Keda Zhou
1Department of Biochemistry, University of Colorado at Boulder, 80309 Boulder, Colorado
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Samuel Bowerman
1Department of Biochemistry, University of Colorado at Boulder, 80309 Boulder, Colorado
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Alison White
1Department of Biochemistry, University of Colorado at Boulder, 80309 Boulder, Colorado
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Garrett Edwards
1Department of Biochemistry, University of Colorado at Boulder, 80309 Boulder, Colorado
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Chantal Abergel
3Aix–Marseille University, Centre National de la Recherche Scientifique, Information Génomique & Structurale, Unité Mixte de Recherche 7256 (Institut de Microbiologie de la Méditerranée, FR3479, IM2B), 13288 Marseille Cedex 9, France
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  • For correspondence: karolin.luger@colorado.edu Chantal.Abergel@igs.cnrs-mrs.fr
Karolin Luger
1Department of Biochemistry, University of Colorado at Boulder, 80309 Boulder, Colorado
2Howard Hughes Medical Institute
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  • For correspondence: karolin.luger@colorado.edu Chantal.Abergel@igs.cnrs-mrs.fr
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Summary

The organization of genomic DNA into defined nucleosomes has long been viewed as a hallmark of eukaryotes. This paradigm has been challenged by the identification of ‘minimalist’ histones in archaea, and more recently by the discovery of genes that encode fused remote homologs of the four eukaryotic histones in Marseilleviridae, a subfamily of giant viruses that infect amoebae. We demonstrate that viral doublet histones localize to the cytoplasmic viral factories after virus infection, and ultimately to mature virions. CryoEM structures of viral nucleosome-like particles show strong similarities to eukaryotic nucleosomes, despite the limited sequence identify. The unique connectors that link the histone chains contribute to the observed instability of viral nucleosomes, and some histone tails assume structural roles. Our results further expand the range of ‘organisms’ that have nucleosomes and suggest a specialized function of histones in the biology of these unusual viruses.

One Sentence Summary Some large DNA viruses encode fused histone doublets that are targeted to viral factories and assemble into open nucleosome-like structures.

Competing Interest Statement

The authors have declared no competing interest.

  • Author contributions

    YL
    conceptualization, methodology, validation, formal analysis, investigation, data curation, writing (Original draft, review and editing), visualization, supervision
    CMT
    Methodology; Validation; Formal Analysis; Investigation; Data curation; Writing (Review & Editing); Visualization
    NP
    investigation (in vivo data), data analysis
    SJ
    investigation (in vivo data), data analysis
    KZ
    Methodology; Validation; Formal Analysis; Data curation; Writing; Visualization
    SB
    Methodology; Software; Formal Analysis; Investigation; Data Curation; Writing - Review & Editing; Supervision; Funding Acquisition
    AW
    investigation, formal analysis, data curation
    GE
    investigation, formal analysis, data curation
    CA
    Conceptualization, formal analysis, writing (discussion and editing), Supervision; Project Administration; Funding Acquisition
    KL
    Conceptualization; Writing (Original Draft; Review & Editing); Supervision; Project Administration; Funding Acquisition
  • Copyright 
    The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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    Posted April 29, 2021.
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    Melbournevirus-encoded histone doublets are recruited to virus particles and form destabilized nucleosome-like structures
    Yang Liu, Chelsea Marie Toner, Nadege Philippe, Sandra Jeudy, Keda Zhou, Samuel Bowerman, Alison White, Garrett Edwards, Chantal Abergel, Karolin Luger
    bioRxiv 2021.04.29.441998; doi: https://doi.org/10.1101/2021.04.29.441998
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    Melbournevirus-encoded histone doublets are recruited to virus particles and form destabilized nucleosome-like structures
    Yang Liu, Chelsea Marie Toner, Nadege Philippe, Sandra Jeudy, Keda Zhou, Samuel Bowerman, Alison White, Garrett Edwards, Chantal Abergel, Karolin Luger
    bioRxiv 2021.04.29.441998; doi: https://doi.org/10.1101/2021.04.29.441998

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