Snapshots of native pre-50S ribosomes reveal a biogenesis factor network and evolutionary specialization

Rainer Nikolay; Tarek Hilal; Sabine Schmidt; Bo Qin; David Schwefel; Carlos H Vieira-Vieira; Thorsten Mielke; Jörg Bürger; Justus Loerke; Kazuaki Amikura; Timo Flügel; Takuya Ueda; Matthias Selbach; Elke Deuerling; Christian M T Spahn

doi:10.1016/j.molcel.2021.02.006

Snapshots of native pre-50S ribosomes reveal a biogenesis factor network and evolutionary specialization

Mol Cell. 2021 Mar 18;81(6):1200-1215.e9. doi: 10.1016/j.molcel.2021.02.006. Epub 2021 Feb 26.

Authors

Affiliations

¹ Institut für Medizinische Physik und Biophysik, Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany. Electronic address: [email protected].
² Institut für Medizinische Physik und Biophysik, Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany; Freie Universität Berlin, Research Centre for Electron Microscopy, Fabeckstr. 36a, 14195 Berlin, Germany.
³ Molekulare Mikrobiologie, Universität Konstanz, Konstanz, Germany.
⁴ Institut für Medizinische Physik und Biophysik, Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany.
⁵ Proteome Dynamics, Max Delbrück Center for Molecular Medicine in the Helmholtz Association (MDC), Robert-Rössle-Str. 10, 13125 Berlin, Germany; Faculty of Life Sciences, Humboldt Universität zu Berlin, Berlin, Germany.
⁶ Microscopy and Cryo-Electron Microscopy Service Group, Max Planck Institute for Molecular Genetics, Ihnestr. 63-73, 14195 Berlin, Germany.
⁷ Institut für Medizinische Physik und Biophysik, Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany; Microscopy and Cryo-Electron Microscopy Service Group, Max Planck Institute for Molecular Genetics, Ihnestr. 63-73, 14195 Berlin, Germany.
⁸ Department of Computational Biology and Medical Sciences, Graduate School of Frontier Sciences, The University of Tokyo, FSB-401, 5-1-5, Kashiwanoha, Kashiwa, Chiba 277-8562, Japan.
⁹ Proteome Dynamics, Max Delbrück Center for Molecular Medicine in the Helmholtz Association (MDC), Robert-Rössle-Str. 10, 13125 Berlin, Germany; Charité-Universitätsmedizin Berlin, 10117 Berlin, Germany.
¹⁰ Institut für Medizinische Physik und Biophysik, Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany. Electronic address: [email protected].

PMID: 33639093
DOI: 10.1016/j.molcel.2021.02.006

Abstract

Ribosome biogenesis is a fundamental multi-step cellular process that culminates in the formation of ribosomal subunits, whose production and modification are regulated by numerous biogenesis factors. In this study, we analyze physiologic prokaryotic ribosome biogenesis by isolating bona fide pre-50S subunits from an Escherichia coli strain with the biogenesis factor ObgE, affinity tagged at its native gene locus. Our integrative structural approach reveals a network of interacting biogenesis factors consisting of YjgA, RluD, RsfS, and ObgE on the immature pre-50S subunit. In addition, our study provides mechanistic insight into how the GTPase ObgE, in concert with other biogenesis factors, facilitates the maturation of the 50S functional core and reveals both conserved and divergent evolutionary features of ribosome biogenesis between prokaryotes and eukaryotes.

Keywords: 50S subunit; ObgE; RluD; RsfS; YjgA; cryo-electron microscopy; ribosome; ribosome assembly; ribosome biogenesis; structure.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Escherichia coli Proteins* / chemistry
Escherichia coli Proteins* / genetics
Escherichia coli Proteins* / metabolism
Evolution, Molecular*
Genetic Loci*
Hydro-Lyases* / chemistry
Hydro-Lyases* / genetics
Hydro-Lyases* / metabolism
Monomeric GTP-Binding Proteins* / chemistry
Monomeric GTP-Binding Proteins* / genetics
Monomeric GTP-Binding Proteins* / metabolism
Ribosome Subunits, Large, Bacterial* / chemistry
Ribosome Subunits, Large, Bacterial* / genetics
Ribosome Subunits, Large, Bacterial* / metabolism

Substances

Escherichia coli Proteins
ObgE protein, E coli
Monomeric GTP-Binding Proteins
Hydro-Lyases
RluD protein, E coli