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Cryo-EM captures early ribosome assembly in action

Author

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  • Bo Qin

    (Institut für Medizinische Physik und Biophysik, Charité – Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt Universität zu Berlin)

  • Simon M. Lauer

    (Institut für Medizinische Physik und Biophysik, Charité – Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt Universität zu Berlin)

  • Annika Balke

    (Charité – Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Institute of Medical Physics and Biophysics, Group Protein X-ray Crystallography and Signal Transduction)

  • Carlos H. Vieira-Vieira

    (Proteome Dynamics, Max Delbrück Center for Molecular Medicine in the Helmholtz Association (MDC)
    Humboldt Universität zu Berlin)

  • Jörg Bürger

    (Institut für Medizinische Physik und Biophysik, Charité – Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt Universität zu Berlin
    Microscopy and Cryo-Electron Microscopy Service Group, Max Planck Institute for Molecular Genetics)

  • Thorsten Mielke

    (Microscopy and Cryo-Electron Microscopy Service Group, Max Planck Institute for Molecular Genetics)

  • Matthias Selbach

    (Proteome Dynamics, Max Delbrück Center for Molecular Medicine in the Helmholtz Association (MDC)
    Charité -Universitätsmedizin Berlin)

  • Patrick Scheerer

    (Charité – Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Institute of Medical Physics and Biophysics, Group Protein X-ray Crystallography and Signal Transduction)

  • Christian M. T. Spahn

    (Institut für Medizinische Physik und Biophysik, Charité – Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt Universität zu Berlin)

  • Rainer Nikolay

    (Institut für Medizinische Physik und Biophysik, Charité – Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt Universität zu Berlin
    Department of Genome Regulation, Max Planck Institute for Molecular Genetics)

Abstract

Ribosome biogenesis is a fundamental multi-step cellular process in all domains of life that involves the production, processing, folding, and modification of ribosomal RNAs (rRNAs) and ribosomal proteins. To obtain insights into the still unexplored early assembly phase of the bacterial 50S subunit, we exploited a minimal in vitro reconstitution system using purified ribosomal components and scalable reaction conditions. Time-limited assembly assays combined with cryo-EM analysis visualizes the structurally complex assembly pathway starting with a particle consisting of ordered density for only ~500 nucleotides of 23S rRNA domain I and three ribosomal proteins. In addition, our structural analysis reveals that early 50S assembly occurs in a domain-wise fashion, while late 50S assembly proceeds incrementally. Furthermore, we find that both ribosomal proteins and folded rRNA helices, occupying surface exposed regions on pre-50S particles, induce, or stabilize rRNA folds within adjacent regions, thereby creating cooperativity.

Suggested Citation

  • Bo Qin & Simon M. Lauer & Annika Balke & Carlos H. Vieira-Vieira & Jörg Bürger & Thorsten Mielke & Matthias Selbach & Patrick Scheerer & Christian M. T. Spahn & Rainer Nikolay, 2023. "Cryo-EM captures early ribosome assembly in action," Nature Communications, Nature, vol. 14(1), pages 1-10, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-36607-9
    DOI: 10.1038/s41467-023-36607-9
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    References listed on IDEAS

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    1. Shan Wu & Beril Tutuncuoglu & Kaige Yan & Hailey Brown & Yixiao Zhang & Dan Tan & Michael Gamalinda & Yi Yuan & Zhifei Li & Jelena Jakovljevic & Chengying Ma & Jianlin Lei & Meng-Qiu Dong & John L. Wo, 2016. "Diverse roles of assembly factors revealed by structures of late nuclear pre-60S ribosomes," Nature, Nature, vol. 534(7605), pages 133-137, June.
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    4. Jingdong Cheng & Otto Berninghausen & Roland Beckmann, 2021. "A distinct assembly pathway of the human 39S late pre-mitoribosome," Nature Communications, Nature, vol. 12(1), pages 1-10, December.
    5. Yi Zhou & Sharmishtha Musalgaonkar & Arlen W. Johnson & David W. Taylor, 2019. "Tightly-orchestrated rearrangements govern catalytic center assembly of the ribosome," Nature Communications, Nature, vol. 10(1), pages 1-11, December.
    6. Hauke S. Hillen & Elena Lavdovskaia & Franziska Nadler & Elisa Hanitsch & Andreas Linden & Katherine E. Bohnsack & Henning Urlaub & Ricarda Richter-Dennerlein, 2021. "Structural basis of GTPase-mediated mitochondrial ribosome biogenesis and recycling," Nature Communications, Nature, vol. 12(1), pages 1-10, December.
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    Cited by:

    1. Kai Sheng & Ning Li & Jessica N. Rabuck-Gibbons & Xiyu Dong & Dmitry Lyumkis & James R. Williamson, 2023. "Assembly landscape for the bacterial large ribosomal subunit," Nature Communications, Nature, vol. 14(1), pages 1-10, December.

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