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Inter-domain dynamics in the chaperone SurA and multi-site binding to its outer membrane protein clients

Author

Listed:
  • Antonio N. Calabrese

    (University of Leeds)

  • Bob Schiffrin

    (University of Leeds)

  • Matthew Watson

    (University of Leeds)

  • Theodoros K. Karamanos

    (University of Leeds
    National Institutes of Health)

  • Martin Walko

    (University of Leeds
    University of Leeds)

  • Julia R. Humes

    (University of Leeds)

  • Jim E. Horne

    (University of Leeds)

  • Paul White

    (University of Leeds)

  • Andrew J. Wilson

    (University of Leeds
    University of Leeds)

  • Antreas C. Kalli

    (University of Leeds)

  • Roman Tuma

    (University of Leeds
    University of South Bohemia)

  • Alison E. Ashcroft

    (University of Leeds)

  • David J. Brockwell

    (University of Leeds)

  • Sheena E. Radford

    (University of Leeds)

Abstract

The periplasmic chaperone SurA plays a key role in outer membrane protein (OMP) biogenesis. E. coli SurA comprises a core domain and two peptidylprolyl isomerase domains (P1 and P2), but its mechanisms of client binding and chaperone function have remained unclear. Here, we use chemical cross-linking, hydrogen-deuterium exchange mass spectrometry, single-molecule FRET and molecular dynamics simulations to map the client binding site(s) on SurA and interrogate the role of conformational dynamics in OMP recognition. We demonstrate that SurA samples an array of conformations in solution in which P2 primarily lies closer to the core/P1 domains than suggested in the SurA crystal structure. OMP binding sites are located primarily in the core domain, and OMP binding results in conformational changes between the core/P1 domains. Together, the results suggest that unfolded OMP substrates bind in a cradle formed between the SurA domains, with structural flexibility between domains assisting OMP recognition, binding and release.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:natcom:v:11:y:2020:i:1:d:10.1038_s41467-020-15702-1
    DOI: 10.1038/s41467-020-15702-1
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    Cited by:

    1. 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.
    2. Paul David Harris & Alessandra Narducci & Christian Gebhardt & Thorben Cordes & Shimon Weiss & Eitan Lerner, 2022. "Multi-parameter photon-by-photon hidden Markov modeling," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    3. Parthasarathi Rath & Adrian Hermann & Ramona Schaefer & Elia Agustoni & Jean-Marie Vonach & Martin Siegrist & Christian Miscenic & Andreas Tschumi & Doris Roth & Christoph Bieniossek & Sebastian Hille, 2023. "High-throughput screening of BAM inhibitors in native membrane environment," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    4. Bob Schiffrin & Joel A. Crossley & Martin Walko & Jonathan M. Machin & G. Nasir Khan & Iain W. Manfield & Andrew J. Wilson & David J. Brockwell & Tomas Fessl & Antonio N. Calabrese & Sheena E. Radford, 2024. "Dual client binding sites in the ATP-independent chaperone SurA," Nature Communications, Nature, vol. 15(1), pages 1-16, December.

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