IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v12y2021i1d10.1038_s41467-021-27449-4.html
   My bibliography  Save this article

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
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-021-27449-4
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-021-27449-4?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. 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.
    2. 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.
    3. 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.
    4. 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.
    5. 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.
    6. 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.
    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.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. 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.
    2. Christopher Jonkergouw & Ngong Kodiah Beyeh & Ekaterina Osmekhina & Katarzyna Leskinen & S. Maryamdokht Taimoory & Dmitrii Fedorov & Eduardo Anaya-Plaza & Mauri A. Kostiainen & John F. Trant & Robin H, 2023. "Repurposing host-guest chemistry to sequester virulence and eradicate biofilms in multidrug resistant Pseudomonas aeruginosa and Acinetobacter baumannii," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    3. Mathieu Botte & Dongchun Ni & Stephan Schenck & Iwan Zimmermann & Mohamed Chami & Nicolas Bocquet & Pascal Egloff & Denis Bucher & Matilde Trabuco & Robert K. Y. Cheng & Janine D. Brunner & Markus A. , 2022. "Cryo-EM structures of a LptDE transporter in complex with Pro-macrobodies offer insight into lipopolysaccharide translocation," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
    4. Nick Middleton & Utchang Kang, 2017. "Sand and Dust Storms: Impact Mitigation," Sustainability, MDPI, vol. 9(6), pages 1-22, June.
    5. Yunmin Yang & Binbin Chu & Jiayi Cheng & Jiali Tang & Bin Song & Houyu Wang & Yao He, 2022. "Bacteria eat nanoprobes for aggregation-enhanced imaging and killing diverse microorganisms," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    6. Chih-Wei Chen & Nadja Leimer & Egor A. Syroegin & Clémence Dunand & Zackery P. Bulman & Kim Lewis & Yury S. Polikanov & Maxim S. Svetlov, 2023. "Structural insights into the mechanism of overcoming Erm-mediated resistance by macrolides acting together with hygromycin-A," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    7. Zhenyan Zhang & Qi Zhang & Tingzhang Wang & Nuohan Xu & Tao Lu & Wenjie Hong & Josep Penuelas & Michael Gillings & Meixia Wang & Wenwen Gao & Haifeng Qian, 2022. "Assessment of global health risk of antibiotic resistance genes," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    8. Matteo Tassinari & Marta Rudzite & Alain Filloux & Harry H. Low, 2023. "Assembly mechanism of a Tad secretion system secretin-pilotin complex," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    9. Anaïs Menny & Marie V. Lukassen & Emma C. Couves & Vojtech Franc & Albert J. R. Heck & Doryen Bubeck, 2021. "Structural basis of soluble membrane attack complex packaging for clearance," Nature Communications, Nature, vol. 12(1), pages 1-11, December.
    10. Ruihuan Yang & Qing Shi & Tingting Huang & Yichao Yan & Shengzhang Li & Yuan Fang & Ying Li & Linlin Liu & Longyu Liu & Xiaozheng Wang & Yongzheng Peng & Jiangbo Fan & Lifang Zou & Shuangjun Lin & Gon, 2023. "The natural pyrazolotriazine pseudoiodinine from Pseudomonas mosselii 923 inhibits plant bacterial and fungal pathogens," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    11. Ana Teresa López-Jiménez & Serge Mostowy, 2021. "Emerging technologies and infection models in cellular microbiology," Nature Communications, Nature, vol. 12(1), pages 1-13, December.
    12. Yuqing Li & Yeying Ma & Yinzheng Xia & Tao Zhang & Shuaishuai Sun & Jiangtao Gao & Hongwei Yao & Huan Wang, 2023. "Discovery and biosynthesis of tricyclic copper-binding ribosomal peptides containing histidine-to-butyrine crosslinks," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    13. Shan Wang & Sixing Lin & Qing Fang & Roland Gyampoh & Zhou Lu & Yingli Gao & David J. Clarke & Kewen Wu & Laurent Trembleau & Yi Yu & Kwaku Kyeremeh & Bruce F. Milne & Jioji Tabudravu & Hai Deng, 2022. "A ribosomally synthesised and post-translationally modified peptide containing a β-enamino acid and a macrocyclic motif," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    14. Sijia Guo & Shu Wang & Suze Ma & Zixin Deng & Wei Ding & Qi Zhang, 2022. "Radical SAM-dependent ether crosslink in daropeptide biosynthesis," Nature Communications, Nature, vol. 13(1), pages 1-9, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-27449-4. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.