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Peptidoglycan maturation controls outer membrane protein assembly

Author

Listed:
  • Gideon Mamou

    (South Parks Road, University of Oxford)

  • Federico Corona

    (Newcastle University
    European Molecular Biology Laboratory)

  • Ruth Cohen-Khait

    (South Parks Road, University of Oxford)

  • Nicholas G. Housden

    (South Parks Road, University of Oxford)

  • Vivian Yeung

    (South Parks Road, University of Oxford)

  • Dawei Sun

    (Genentech)

  • Pooja Sridhar

    (University of Birmingham)

  • Manuel Pazos

    (Newcastle University
    Autonomous University of Madrid)

  • Timothy J. Knowles

    (University of Birmingham)

  • Colin Kleanthous

    (South Parks Road, University of Oxford)

  • Waldemar Vollmer

    (Newcastle University)

Abstract

Linkages between the outer membrane of Gram-negative bacteria and the peptidoglycan layer are crucial for the maintenance of cellular integrity and enable survival in challenging environments1–5. The function of the outer membrane is dependent on outer membrane proteins (OMPs), which are inserted into the membrane by the β-barrel assembly machine6,7 (BAM). Growing Escherichia coli cells segregate old OMPs towards the poles by a process known as binary partitioning, the basis of which is unknown8. Here we demonstrate that peptidoglycan underpins the spatiotemporal organization of OMPs. Mature, tetrapeptide-rich peptidoglycan binds to BAM components and suppresses OMP foldase activity. Nascent peptidoglycan, which is enriched in pentapeptides and concentrated at septa9, associates with BAM poorly and has little effect on its activity, leading to preferential insertion of OMPs at division sites. The synchronization of OMP biogenesis with cell wall growth results in the binary partitioning of OMPs as cells divide. Our study reveals that Gram-negative bacteria coordinate the assembly of two major cell envelope layers by rendering OMP biogenesis responsive to peptidoglycan maturation, a potential vulnerability that could be exploited in future antibiotic design.

Suggested Citation

  • Gideon Mamou & Federico Corona & Ruth Cohen-Khait & Nicholas G. Housden & Vivian Yeung & Dawei Sun & Pooja Sridhar & Manuel Pazos & Timothy J. Knowles & Colin Kleanthous & Waldemar Vollmer, 2022. "Peptidoglycan maturation controls outer membrane protein assembly," Nature, Nature, vol. 606(7916), pages 953-959, June.
    • Handle: RePEc:nat:nature:v:606:y:2022:i:7916:d:10.1038_s41586-022-04834-7
    DOI: 10.1038/s41586-022-04834-7
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    Cited by:

    1. Matthew Herdman & Buse Isbilir & Andriko Kügelgen & Ulrike Schulze & Alan Wainman & Tanmay A. M. Bharat, 2024. "Cell cycle dependent coordination of surface layer biogenesis in Caulobacter crescentus," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    2. Rei Nakamoto & Sarp Bamyaci & Karin Blomqvist & Staffan Normark & Birgitta Henriques-Normark & Lok-To Sham, 2023. "The divisome but not the elongasome organizes capsule synthesis in Streptococcus pneumoniae," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    3. Caroline Servais & Victoria Vassen & Audrey Verhaeghe & Nina Küster & Elodie Carlier & Léa Phégnon & Aurélie Mayard & Nicolas Auberger & Stéphane Vincent & Xavier De Bolle, 2023. "Lipopolysaccharide biosynthesis and traffic in the envelope of the pathogen Brucella abortus," Nature Communications, Nature, vol. 14(1), pages 1-13, December.

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