Ribosome-inactivation by a class of widely distributed C-tail anchored membrane proteins

Njenga, Robert Karari; Boele, Julian; Drepper, Friedel; Sinha, Kasturica; Marouda, Eirini; Huesgen, Pitter F.; Blaby-Haas, Crysten; Koch, Hans-Georg

doi:10.1016/j.str.2024.09.019

Title: Ribosome-inactivation by a class of widely distributed C-tail anchored membrane proteins

Journal Article · 15 October 2024 · Structure

DOI: https://doi.org/10.1016/j.str.2024.09.019 · OSTI ID:2472466

Njenga, Robert Karari ^[1]; Boele, Julian ^[1]; Drepper, Friedel ^[1]; Sinha, Kasturica ^[1]; Marouda, Eirini ^[1]; Huesgen, Pitter F. ^[1]; Blaby-Haas, Crysten ^[2];

^[1]

Univ. of Freiburg (Germany)
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States). Molecular Foundry; USDOE Joint Genome Institute (JGI), Berkeley, CA (United States)

Ribosome hibernation is a commonly used strategy that protects ribosomes under unfavorable conditions and regulates developmental processes. Multiple ribosome-hibernation factors have been identified in all domains of life, but due to their structural diversity and the lack of a common inactivation mechanism, it is currently unknown how many different hibernation factors exist. Here, we show that the YqjD/ElaB/YgaM paralogs, initially discovered as membrane-bound ribosome binding proteins in E. coli, constitute an abundant class of ribosome-hibernating proteins, which are conserved across all proteobacteria and some other bacterial phyla. Our data demonstrate that they inhibit in vitro protein synthesis by interacting with the 50S ribosomal subunit. In vivo cross-linking combined with mass spectrometry revealed their specific interactions with proteins surrounding the ribosomal tunnel exit and even their penetration into the ribosomal tunnel. Thus, YqjD/ElaB/YgaM inhibit translation by blocking the ribosomal tunnel and thus mimic the activity of antimicrobial peptides and macrolide antibiotics.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: German Research Foundation (DFG); USDOE; USDOE Office of Science (SC), Basic Energy Sciences (BES). Scientific User Facilities (SUF); USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 2472466

Journal Information:: Structure, Journal Name: Structure Journal Issue: 12 Vol. 32; ISSN 0969-2126

Publisher:: ElsevierCopyright Statement

Country of Publication:: United States

Language:: English

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YqjD Is an Inner Membrane Protein Associated with Stationary-Phase Ribosomes in Escherichia coli Yoshida, Hideji; Maki, Yasushi; Furuike, Shou Journal of Bacteriology, Vol. 194, Issue 16 https://doi.org/10.1128/JB.00396-12	journal	August 2012
Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. Guzman, L. M.; Belin, D.; Carson, M. J. Journal of Bacteriology, Vol. 177, Issue 14, p. 4121-4130 https://doi.org/10.1128/jb.177.14.4121-4130.1995	journal	July 1995
Comparative characterization of SecA from the alpha-subclass purple bacterium Rhodobacter capsulatus and Escherichia coli reveals differences in membrane and precursor specificity Helde, R.; Wiesler, B.; Wachter, E. Journal of Bacteriology, Vol. 179, Issue 12 https://doi.org/10.1128/jb.179.12.4003-4012.1997	journal	June 1997
Studies on Lysogenesis i. Bertani, G. Journal of Bacteriology, Vol. 62, Issue 3 https://doi.org/10.1128/jb.62.3.293-300.1951	journal	January 1951
Molecular Mimicry of SecA and Signal Recognition Particle Binding to the Bacterial Ribosome Knüpffer, Lara; Fehrenbach, Clara; Denks, Kärt mBio, Vol. 10, Issue 4 https://doi.org/10.1128/mBio.01317-19	journal	August 2019
CsrA coordinates the expression of ribosome hibernation and anti-σ factor proteins Pourciau, Christine; Yakhnin, Helen; Pannuri, Archanna mBio, Vol. 14, Issue 6 https://doi.org/10.1128/mbio.02585-23	journal	December 2023
At the Crossroad of Nucleotide Dynamics and Protein Synthesis in Bacteria Leiva, Lorenzo Eugenio; Zegarra, Victor; Bange, Gert Microbiology and Molecular Biology Reviews, Vol. 87, Issue 1 https://doi.org/10.1128/mmbr.00044-22	journal	March 2023
Ribosome Hibernation Prossliner, Thomas; Skovbo Winther, Kristoffer; Sørensen, Michael Askvad Annual Review of Genetics, Vol. 52, Issue 1 https://doi.org/10.1146/annurev-genet-120215-035130	journal	November 2018
Cellular Defenses against Superoxide and Hydrogen Peroxide Imlay, James A. Annual Review of Biochemistry, Vol. 77, Issue 1 https://doi.org/10.1146/annurev.biochem.77.061606.161055	journal	June 2008
FastTree 2 – Approximately Maximum-Likelihood Trees for Large Alignments Price, Morgan N.; Dehal, Paramvir S.; Arkin, Adam P. PLoS ONE, Vol. 5, Issue 3 https://doi.org/10.1371/journal.pone.0009490	journal	March 2010
The conserved theme of ribosome hibernation: from bacteria to chloroplasts of plants Trösch, Raphael; Willmund, Felix Biological Chemistry, Vol. 400, Issue 7 https://doi.org/10.1515/hsz-2018-0436	journal	June 2019
Ribosome Hibernation as a Stress Response of Bacteria Wang, Tianwen; Liang, Chen; Zheng, Mengyuan Protein & Peptide Letters, Vol. 27, Issue 11 https://doi.org/10.2174/0929866527666200610142118	journal	November 2020
The spatial biology of transcription and translation in rapidly growing Escherichia coli Bakshi, Somenath; Choi, Heejun; Weisshaar, James C. Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.00636	journal	July 2015
The Universally Conserved ATPase YchF Regulates Translation of Leaderless mRNA in Response to Stress Conditions Landwehr, Victoria; Milanov, Martin; Angebauer, Larissa Frontiers in Molecular Biosciences, Vol. 8 https://doi.org/10.3389/fmolb.2021.643696	journal	May 2021
Ribosome Protein Composition Mediates Translation during the Escherichia coli Stationary Phase Reier, Kaspar; Liiv, Aivar; Remme, Jaanus International Journal of Molecular Sciences, Vol. 24, Issue 4 https://doi.org/10.3390/ijms24043128	journal	February 2023
Ribosomal Hibernation-Associated Factors in Escherichia coli Maki, Yasushi; Yoshida, Hideji Microorganisms, Vol. 10, Issue 1 https://doi.org/10.3390/microorganisms10010033	journal	December 2021

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59 BASIC BIOLOGICAL SCIENCES
ElaB
YgaM
YqjD
antimicrobial peptides
macrolide antibiotics
ribosomes
stationary phase
stress response
translation

Title: Ribosome-inactivation by a class of widely distributed C-tail anchored membrane proteins

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