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Outer membrane protein assembly mediated by BAM-SurA complexes

Author

Listed:
  • Katherine L. Fenn

    (University of Leeds)

  • Jim E. Horne

    (University of Leeds
    Department of Biochemistry)

  • Joel A. Crossley

    (University of Leeds)

  • Nils Böhringer

    (Justus-Liebig-University Giessen
    Partner Site Giessen-Marburg-Langen
    Fraunhofer Institute for Molecular Biology and Applied Ecology (IME))

  • Romany J. Horne

    (University of Leeds
    Great Abington)

  • Till F. Schäberle

    (Justus-Liebig-University Giessen
    Partner Site Giessen-Marburg-Langen
    Fraunhofer Institute for Molecular Biology and Applied Ecology (IME))

  • Antonio N. Calabrese

    (University of Leeds)

  • Sheena E. Radford

    (University of Leeds)

  • Neil A. Ranson

    (University of Leeds)

Abstract

The outer membrane is a formidable barrier that protects Gram-negative bacteria against environmental threats. Its integrity requires the correct folding and insertion of outer membrane proteins (OMPs) by the membrane-embedded β-barrel assembly machinery (BAM). Unfolded OMPs are delivered to BAM by the periplasmic chaperone SurA, but how SurA and BAM work together to ensure successful OMP delivery and folding remains unclear. Here, guided by AlphaFold2 models, we use disulphide bond engineering in an attempt to trap SurA in the act of OMP delivery to BAM, and solve cryoEM structures of a series of complexes. The results suggest that SurA binds BAM at its soluble POTRA-1 domain, which may trigger conformational changes in both BAM and SurA that enable transfer of the unfolded OMP to the BAM lateral gate for insertion into the outer membrane. Mutations that disrupt the interaction between BAM and SurA result in outer membrane assembly defects, supporting the key role of SurA in outer membrane biogenesis.

Suggested Citation

  • Katherine L. Fenn & Jim E. Horne & Joel A. Crossley & Nils Böhringer & Romany J. Horne & Till F. Schäberle & Antonio N. Calabrese & Sheena E. Radford & Neil A. Ranson, 2024. "Outer membrane protein assembly mediated by BAM-SurA complexes," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-51358-x
    DOI: 10.1038/s41467-024-51358-x
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    References listed on IDEAS

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    1. Antonio N. Calabrese & Bob Schiffrin & Matthew Watson & Theodoros K. Karamanos & Martin Walko & Julia R. Humes & Jim E. Horne & Paul White & Andrew J. Wilson & Antreas C. Kalli & Roman Tuma & Alison E, 2020. "Inter-domain dynamics in the chaperone SurA and multi-site binding to its outer membrane protein clients," Nature Communications, Nature, vol. 11(1), pages 1-16, December.
    2. 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.
    3. Antonino Ingargiola & Eitan Lerner & SangYoon Chung & Shimon Weiss & Xavier Michalet, 2016. "FRETBursts: An Open Source Toolkit for Analysis of Freely-Diffusing Single-Molecule FRET," PLOS ONE, Public Library of Science, vol. 11(8), pages 1-27, August.
    4. Runrun Wu & Jeremy W. Bakelar & Karl Lundquist & Zijian Zhang & Katie M. Kuo & David Ryoo & Yui Tik Pang & Chen Sun & Tommi White & Thomas Klose & Wen Jiang & James C. Gumbart & Nicholas Noinaj, 2021. "Plasticity within the barrel domain of BamA mediates a hybrid-barrel mechanism by BAM," Nature Communications, Nature, vol. 12(1), pages 1-16, December.
    5. Hundeep Kaur & Roman P. Jakob & Jan K. Marzinek & Robert Green & Yu Imai & Jani Reddy Bolla & Elia Agustoni & Carol V. Robinson & Peter J. Bond & Kim Lewis & Timm Maier & Sebastian Hiller, 2021. "The antibiotic darobactin mimics a β-strand to inhibit outer membrane insertase," Nature, Nature, vol. 593(7857), pages 125-129, May.
    6. 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.
    7. Yu Imai & Kirsten J. Meyer & Akira Iinishi & Quentin Favre-Godal & Robert Green & Sylvie Manuse & Mariaelena Caboni & Miho Mori & Samantha Niles & Meghan Ghiglieri & Chandrashekhar Honrao & Xiaoyu Ma , 2019. "A new antibiotic selectively kills Gram-negative pathogens," Nature, Nature, vol. 576(7787), pages 459-464, December.
    8. Matthew T. Doyle & Harris D. Bernstein, 2019. "Bacterial outer membrane proteins assemble via asymmetric interactions with the BamA β-barrel," Nature Communications, Nature, vol. 10(1), pages 1-13, December.
    9. David Tomasek & Shaun Rawson & James Lee & Joseph S. Wzorek & Stephen C. Harrison & Zongli Li & Daniel Kahne, 2020. "Structure of a nascent membrane protein as it folds on the BAM complex," Nature, Nature, vol. 583(7816), pages 473-478, July.
    10. Matthew G. Iadanza & Anna J. Higgins & Bob Schiffrin & Antonio N. Calabrese & David J. Brockwell & Alison E. Ashcroft & Sheena E. Radford & Neil A. Ranson, 2016. "Lateral opening in the intact β-barrel assembly machinery captured by cryo-EM," Nature Communications, Nature, vol. 7(1), pages 1-12, November.
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