IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-36145-4.html
   My bibliography  Save this article

Evolution of giant pandoravirus revealed by CRISPR/Cas9

Author

Listed:
  • Hugo Bisio

    (Unite Mixte de Recherche 7256 (Institut de Microbiologie de la Mediterranee, FR3479, IM2B), 13288)

  • Matthieu Legendre

    (Unite Mixte de Recherche 7256 (Institut de Microbiologie de la Mediterranee, FR3479, IM2B), 13288)

  • Claire Giry

    (Unite Mixte de Recherche 7256 (Institut de Microbiologie de la Mediterranee, FR3479, IM2B), 13288)

  • Nadege Philippe

    (Unite Mixte de Recherche 7256 (Institut de Microbiologie de la Mediterranee, FR3479, IM2B), 13288)

  • Jean-Marie Alempic

    (Unite Mixte de Recherche 7256 (Institut de Microbiologie de la Mediterranee, FR3479, IM2B), 13288)

  • Sandra Jeudy

    (Unite Mixte de Recherche 7256 (Institut de Microbiologie de la Mediterranee, FR3479, IM2B), 13288)

  • Chantal Abergel

    (Unite Mixte de Recherche 7256 (Institut de Microbiologie de la Mediterranee, FR3479, IM2B), 13288)

Abstract

Giant viruses (GVs) are a hotspot of unresolved controversies since their discovery, including the definition of “Virus” and their origin. While increasing knowledge of genome diversity has accumulated, GV functional genomics was largely neglected. Here, we describe an experimental framework to genetically modify nuclear GVs and their host Acanthamoeba castellanii using CRISPR/Cas9, shedding light on the evolution from small icosahedral viruses to amphora-shaped GVs. Ablation of the icosahedral major capsid protein in the phylogenetically-related mollivirus highlights a transition in virion shape and size. We additionally demonstrate the existence of a reduced core essential genome in pandoravirus, reminiscent of their proposed smaller ancestors. This proposed genetic expansion led to increased genome robustness, indicating selective pressures for adaptation to uncertain environments. Overall, we introduce new tools for manipulation of the unexplored genome of nuclear GVs and provide experimental evidence suggesting that viral gigantism has aroused as an emerging trait.

Suggested Citation

  • Hugo Bisio & Matthieu Legendre & Claire Giry & Nadege Philippe & Jean-Marie Alempic & Sandra Jeudy & Chantal Abergel, 2023. "Evolution of giant pandoravirus revealed by CRISPR/Cas9," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-36145-4
    DOI: 10.1038/s41467-023-36145-4
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-36145-4
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-023-36145-4?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Kathryn Tunyasuvunakool & Jonas Adler & Zachary Wu & Tim Green & Michal Zielinski & Augustin Žídek & Alex Bridgland & Andrew Cowie & Clemens Meyer & Agata Laydon & Sameer Velankar & Gerard J. Kleywegt, 2021. "Highly accurate protein structure prediction for the human proteome," Nature, Nature, vol. 596(7873), pages 590-596, August.
    2. Senén D. Mendoza & Eliza S. Nieweglowska & Sutharsan Govindarajan & Lina M. Leon & Joel D. Berry & Anika Tiwari & Vorrapon Chaikeeratisak & Joe Pogliano & David A. Agard & Joseph Bondy-Denomy, 2020. "A bacteriophage nucleus-like compartment shields DNA from CRISPR nucleases," Nature, Nature, vol. 577(7789), pages 244-248, January.
    3. Matthieu Legendre & Elisabeth Fabre & Olivier Poirot & Sandra Jeudy & Audrey Lartigue & Jean-Marie Alempic & Laure Beucher & Nadège Philippe & Lionel Bertaux & Eugène Christo-Foroux & Karine Labadie &, 2018. "Diversity and evolution of the emerging Pandoraviridae family," Nature Communications, Nature, vol. 9(1), pages 1-12, December.
    4. John Jumper & Richard Evans & Alexander Pritzel & Tim Green & Michael Figurnov & Olaf Ronneberger & Kathryn Tunyasuvunakool & Russ Bates & Augustin Žídek & Anna Potapenko & Alex Bridgland & Clemens Me, 2021. "Highly accurate protein structure prediction with AlphaFold," Nature, Nature, vol. 596(7873), pages 583-589, August.
    5. Elisabeth Fabre & Sandra Jeudy & Sébastien Santini & Matthieu Legendre & Mathieu Trauchessec & Yohann Couté & Jean-Michel Claverie & Chantal Abergel, 2017. "Noumeavirus replication relies on a transient remote control of the host nucleus," Nature Communications, Nature, vol. 8(1), pages 1-12, April.
    6. Mohammad Moniruzzaman & Carolina A. Martinez-Gutierrez & Alaina R. Weinheimer & Frank O. Aylward, 2020. "Dynamic genome evolution and complex virocell metabolism of globally-distributed giant viruses," Nature Communications, Nature, vol. 11(1), pages 1-11, December.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Qianqian Shao & Irina V. Agarkova & Eric A. Noel & David D. Dunigan & Yunshu Liu & Aohan Wang & Mingcheng Guo & Linlin Xie & Xinyue Zhao & Michael G. Rossmann & James L. Etten & Thomas Klose & Qiangli, 2022. "Near-atomic, non-icosahedrally averaged structure of giant virus Paramecium bursaria chlorella virus 1," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    2. Pierre Azoulay & Joshua Krieger & Abhishek Nagaraj, 2024. "Old Moats for New Models: Openness, Control, and Competition in Generative AI," NBER Chapters, in: Entrepreneurship and Innovation Policy and the Economy, volume 4, National Bureau of Economic Research, Inc.
    3. Deyun Qiu & Jinxin V. Pei & James E. O. Rosling & Vandana Thathy & Dongdi Li & Yi Xue & John D. Tanner & Jocelyn Sietsma Penington & Yi Tong Vincent Aw & Jessica Yi Han Aw & Guoyue Xu & Abhai K. Tripa, 2022. "A G358S mutation in the Plasmodium falciparum Na+ pump PfATP4 confers clinically-relevant resistance to cipargamin," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    4. Shuo-Shuo Liu & Tian-Xia Jiang & Fan Bu & Ji-Lan Zhao & Guang-Fei Wang & Guo-Heng Yang & Jie-Yan Kong & Yun-Fan Qie & Pei Wen & Li-Bin Fan & Ning-Ning Li & Ning Gao & Xiao-Bo Qiu, 2024. "Molecular mechanisms underlying the BIRC6-mediated regulation of apoptosis and autophagy," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    5. Xiaoke Yang & Mingqi Zhu & Xue Lu & Yuxin Wang & Junyu Xiao, 2024. "Architecture and activation of human muscle phosphorylase kinase," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    6. Efren Garcia-Maldonado & Andrew D. Huber & Sergio C. Chai & Stanley Nithianantham & Yongtao Li & Jing Wu & Shyaron Poudel & Darcie J. Miller & Jayaraman Seetharaman & Taosheng Chen, 2024. "Chemical manipulation of an activation/inhibition switch in the nuclear receptor PXR," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    7. Kristy Rochon & Brianna L. Bauer & Nathaniel A. Roethler & Yuli Buckley & Chih-Chia Su & Wei Huang & Rajesh Ramachandran & Maria S. K. Stoll & Edward W. Yu & Derek J. Taylor & Jason A. Mears, 2024. "Structural basis for regulated assembly of the mitochondrial fission GTPase Drp1," Nature Communications, Nature, vol. 15(1), pages 1-10, December.
    8. Fan Lu & Liang Zhu & Thomas Bromberger & Jun Yang & Qiannan Yang & Jianmin Liu & Edward F. Plow & Markus Moser & Jun Qin, 2022. "Mechanism of integrin activation by talin and its cooperation with kindlin," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    9. Martin F. Peter & Christian Gebhardt & Rebecca Mächtel & Gabriel G. Moya Muñoz & Janin Glaenzer & Alessandra Narducci & Gavin H. Thomas & Thorben Cordes & Gregor Hagelueken, 2022. "Cross-validation of distance measurements in proteins by PELDOR/DEER and single-molecule FRET," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    10. Jutta Diessl & Jens Berndtsson & Filomena Broeskamp & Lukas Habernig & Verena Kohler & Carmela Vazquez-Calvo & Arpita Nandy & Carlotta Peselj & Sofia Drobysheva & Ludovic Pelosi & F.-Nora Vögtle & Fab, 2022. "Manganese-driven CoQ deficiency," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    11. Alexander Kroll & Sahasra Ranjan & Martin K. M. Engqvist & Martin J. Lercher, 2023. "A general model to predict small molecule substrates of enzymes based on machine and deep learning," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    12. Lisa-Marie Appel & Vedran Franke & Johannes Benedum & Irina Grishkovskaya & Xué Strobl & Anton Polyansky & Gregor Ammann & Sebastian Platzer & Andrea Neudolt & Anna Wunder & Lena Walch & Stefanie Kais, 2023. "The SPOC domain is a phosphoserine binding module that bridges transcription machinery with co- and post-transcriptional regulators," Nature Communications, Nature, vol. 14(1), pages 1-22, December.
    13. Maciej K. Kocylowski & Hande Aypek & Wolfgang Bildl & Martin Helmstädter & Philipp Trachte & Bernhard Dumoulin & Sina Wittösch & Lukas Kühne & Ute Aukschun & Carolin Teetzen & Oliver Kretz & Botond Ga, 2022. "A slit-diaphragm-associated protein network for dynamic control of renal filtration," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    14. Michael A. Longo & Sunetra Roy & Yue Chen & Karl-Heinz Tomaszowski & Andrew S. Arvai & Jordan T. Pepper & Rebecca A. Boisvert & Selvi Kunnimalaiyaan & Caezanne Keshvani & David Schild & Albino Bacolla, 2023. "RAD51C-XRCC3 structure and cancer patient mutations define DNA replication roles," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    15. Zachary C. Drake & Justin T. Seffernick & Steffen Lindert, 2022. "Protein complex prediction using Rosetta, AlphaFold, and mass spectrometry covalent labeling," Nature Communications, Nature, vol. 13(1), pages 1-9, December.
    16. Leonardo Betancurt-Anzola & Markel Martínez-Carranza & Marc Delarue & Kelly M. Zatopek & Andrew F. Gardner & Ludovic Sauguet, 2023. "Molecular basis for proofreading by the unique exonuclease domain of Family-D DNA polymerases," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    17. Karin Vogel & Tobias Bläske & Marie-Kristin Nagel & Christoph Globisch & Shane Maguire & Lorenz Mattes & Christian Gude & Michael Kovermann & Karin Hauser & Christine Peter & Erika Isono, 2022. "Lipid-mediated activation of plasma membrane-localized deubiquitylating enzymes modulate endosomal trafficking," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    18. Robin Anger & Laetitia Pieulle & Meriam Shahin & Odile Valette & Hugo Guenno & Artemis Kosta & Vladimir Pelicic & Rémi Fronzes, 2023. "Structure of a heteropolymeric type 4 pilus from a monoderm bacterium," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    19. Jie Li & Haonan Zhang & Dongyu Li & Ya-Jun Liu & Edward A. Bayer & Qiu Cui & Yingang Feng & Ping Zhu, 2023. "Structure of the transcription open complex of distinct σI factors," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    20. Hongmin Cai & Shimeng Guo & Youwei Xu & Jun Sun & Junrui Li & Zhikan Xia & Yi Jiang & Xin Xie & H. Eric Xu, 2024. "Cryo-EM structures of adenosine receptor A3AR bound to selective agonists," Nature Communications, Nature, vol. 15(1), pages 1-10, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-36145-4. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.