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The outer membrane is an essential load-bearing element in Gram-negative bacteria

Author

Listed:
  • Enrique R. Rojas

    (Stanford University
    Stanford University School of Medicine
    Stanford University School of Medicine)

  • Gabriel Billings

    (Stanford University)

  • Pascal D. Odermatt

    (Stanford University
    University of California San Francisco)

  • George K. Auer

    (University of Wisconsin-Madison)

  • Lillian Zhu

    (Stanford University)

  • Amanda Miguel

    (Stanford University)

  • Fred Chang

    (University of California San Francisco)

  • Douglas B. Weibel

    (University of Wisconsin-Madison
    University of Wisconsin-Madison
    University of Wisconsin-Madison)

  • Julie A. Theriot

    (Stanford University School of Medicine
    Stanford University School of Medicine
    Howard Hughes Medical Institute
    Stanford University)

  • Kerwyn Casey Huang

    (Stanford University
    Stanford University School of Medicine
    Stanford University
    Chan Zuckerberg Biohub)

Abstract

Gram-negative bacteria possess a complex cell envelope that consists of a plasma membrane, a peptidoglycan cell wall and an outer membrane. The envelope is a selective chemical barrier1 that defines cell shape2 and allows the cell to sustain large mechanical loads such as turgor pressure3. It is widely believed that the covalently cross-linked cell wall underpins the mechanical properties of the envelope4,5. Here we show that the stiffness and strength of Escherichia coli cells are largely due to the outer membrane. Compromising the outer membrane, either chemically or genetically, greatly increased deformation of the cell envelope in response to stretching, bending and indentation forces, and induced increased levels of cell lysis upon mechanical perturbation and during L-form proliferation. Both lipopolysaccharides and proteins contributed to the stiffness of the outer membrane. These findings overturn the prevailing dogma that the cell wall is the dominant mechanical element within Gram-negative bacteria, instead demonstrating that the outer membrane can be stiffer than the cell wall, and that mechanical loads are often balanced between these structures.

Suggested Citation

  • Enrique R. Rojas & Gabriel Billings & Pascal D. Odermatt & George K. Auer & Lillian Zhu & Amanda Miguel & Fred Chang & Douglas B. Weibel & Julie A. Theriot & Kerwyn Casey Huang, 2018. "The outer membrane is an essential load-bearing element in Gram-negative bacteria," Nature, Nature, vol. 559(7715), pages 617-621, July.
  • Handle: RePEc:nat:nature:v:559:y:2018:i:7715:d:10.1038_s41586-018-0344-3
    DOI: 10.1038/s41586-018-0344-3
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    Cited by:

    1. Augustinas Silale & Yiling Zhu & Jerzy Witwinowski & Robert E. Smith & Kahlan E. Newman & Satya P. Bhamidimarri & Arnaud Baslé & Syma Khalid & Christophe Beloin & Simonetta Gribaldo & Bert Berg, 2023. "Dual function of OmpM as outer membrane tether and nutrient uptake channel in diderm Firmicutes," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    2. Xiangfeng Lai & Mei-Ling Han & Yue Ding & Seong Hoong Chow & Anton P. Brun & Chun-Ming Wu & Phillip J. Bergen & Jhih-hang Jiang & Hsien-Yi Hsu & Benjamin W. Muir & Jacinta White & Jiangning Song & Jia, 2022. "A polytherapy based approach to combat antimicrobial resistance using cubosomes," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    3. Han Gao & Yongmao Jiang & Lihua Wang & Guandong Wang & Wenqian Hu & Ling Dong & Sibao Wang, 2023. "Outer membrane vesicles from a mosquito commensal mediate targeted killing of Plasmodium parasites via the phosphatidylcholine scavenging pathway," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    4. Irina V. Mikheyeva & Jiawei Sun & Kerwyn Casey Huang & Thomas J. Silhavy, 2023. "Mechanism of outer membrane destabilization by global reduction of protein content," Nature Communications, Nature, vol. 14(1), pages 1-9, December.
    5. Yuqian Qiao & Yingde Xu & Xiangmei Liu & Yufeng Zheng & Bo Li & Yong Han & Zhaoyang Li & Kelvin Wai Kwok Yeung & Yanqin Liang & Shengli Zhu & Zhenduo Cui & Shuilin Wu, 2022. "Microwave assisted antibacterial action of Garcinia nanoparticles on Gram-negative bacteria," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    6. Kerry R. Buchholz & Mike Reichelt & Matthew C. Johnson & Sarah J. Robinson & Peter A. Smith & Steven T. Rutherford & John G. Quinn, 2024. "Potent activity of polymyxin B is associated with long-lived super-stoichiometric accumulation mediated by weak-affinity binding to lipid A," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    7. 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.
    8. Henri Voedts & Sean P. Kennedy & Guennadi Sezonov & Michel Arthur & Jean-Emmanuel Hugonnet, 2022. "Genome-wide identification of genes required for alternative peptidoglycan cross-linking in Escherichia coli revealed unexpected impacts of β-lactams," Nature Communications, Nature, vol. 13(1), pages 1-14, December.

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