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Plasticity within the barrel domain of BamA mediates a hybrid-barrel mechanism by BAM

Author

Listed:
  • Runrun Wu

    (Purdue University)

  • Jeremy W. Bakelar

    (Purdue University
    Dixie State University)

  • Karl Lundquist

    (School of Physics, Georgia Institute of Technology
    Purdue University)

  • Zijian Zhang

    (School of Physics, Georgia Institute of Technology)

  • Katie M. Kuo

    (Georgia Institute of Technology)

  • David Ryoo

    (Georgia Institute of Technology)

  • Yui Tik Pang

    (School of Physics, Georgia Institute of Technology)

  • Chen Sun

    (Purdue University)

  • Tommi White

    (University of Missouri)

  • Thomas Klose

    (Purdue University
    Purdue University)

  • Wen Jiang

    (Purdue University
    Purdue University
    Purdue University
    Purdue University)

  • James C. Gumbart

    (School of Physics, Georgia Institute of Technology
    Georgia Institute of Technology)

  • Nicholas Noinaj

    (Purdue University
    Purdue University
    Purdue University)

Abstract

In Gram-negative bacteria, the biogenesis of β-barrel outer membrane proteins is mediated by the β-barrel assembly machinery (BAM). The mechanism employed by BAM is complex and so far- incompletely understood. Here, we report the structures of BAM in nanodiscs, prepared using polar lipids and native membranes, where we observe an outward-open state. Mutations in the barrel domain of BamA reveal that plasticity in BAM is essential, particularly along the lateral seam of the barrel domain, which is further supported by molecular dynamics simulations that show conformational dynamics in BAM are modulated by the accessory proteins. We also report the structure of BAM in complex with EspP, which reveals an early folding intermediate where EspP threads from the underside of BAM and incorporates into the barrel domain of BamA, supporting a hybrid-barrel budding mechanism in which the substrate is folded into the membrane sequentially rather than as a single unit.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-27449-4
    DOI: 10.1038/s41467-021-27449-4
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    References listed on IDEAS

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    1. Anatol Luther & Matthias Urfer & Michael Zahn & Maik Müller & Shuang-Yan Wang & Milon Mondal & Alessandra Vitale & Jean-Baptiste Hartmann & Timothy Sharpe & Fabio Lo Monte & Harsha Kocherla & Elizabet, 2019. "Author Correction: Chimeric peptidomimetic antibiotics against Gram-negative bacteria," Nature, Nature, vol. 576(7786), pages 5-5, December.
    2. 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.
    3. 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.
    4. Nicholas Noinaj & Nicole C. Easley & Muse Oke & Naoko Mizuno & James Gumbart & Evzen Boura & Ashley N. Steere & Olga Zak & Philip Aisen & Emad Tajkhorshid & Robert W. Evans & Andrew R. Gorringe & Anne, 2012. "Structural basis for iron piracy by pathogenic Neisseria," Nature, Nature, vol. 483(7387), pages 53-58, March.
    5. 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.
    6. Anatol Luther & Matthias Urfer & Michael Zahn & Maik Müller & Shuang-Yan Wang & Milon Mondal & Alessandra Vitale & Jean-Baptiste Hartmann & Timothy Sharpe & Fabio Lo Monte & Harsha Kocherla & Elizabet, 2019. "Chimeric peptidomimetic antibiotics against Gram-negative bacteria," Nature, Nature, vol. 576(7787), pages 452-458, December.
    7. Yinghong Gu & Huanyu Li & Haohao Dong & Yi Zeng & Zhengyu Zhang & Neil G. Paterson & Phillip J. Stansfeld & Zhongshan Wang & Yizheng Zhang & Wenjian Wang & Changjiang Dong, 2016. "Structural basis of outer membrane protein insertion by the BAM complex," Nature, Nature, vol. 531(7592), pages 64-69, March.
    8. Timm Maier & Bernard Clantin & Fabian Gruss & Frédérique Dewitte & Anne-Sophie Delattre & Françoise Jacob-Dubuisson & Sebastian Hiller & Vincent Villeret, 2015. "Conserved Omp85 lid-lock structure and substrate recognition in FhaC," Nature Communications, Nature, vol. 6(1), pages 1-9, November.
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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. 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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