IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-39723-8.html
   My bibliography  Save this article

On the mechanisms of lysis triggered by perturbations of bacterial cell wall biosynthesis

Author

Listed:
  • Yoshikazu Kawai

    (Newcastle University
    University of Sydney)

  • Maki Kawai

    (Newcastle University
    University of Sydney)

  • Eilidh Sohini Mackenzie

    (Newcastle University)

  • Yousef Dashti

    (University of Sydney)

  • Bernhard Kepplinger

    (University of Wrocław)

  • Kevin John Waldron

    (Newcastle University
    Polish Academy of Sciences)

  • Jeff Errington

    (Newcastle University
    University of Sydney)

Abstract

Inhibition of bacterial cell wall synthesis by antibiotics such as β-lactams is thought to cause explosive lysis through loss of cell wall integrity. However, recent studies on a wide range of bacteria have suggested that these antibiotics also perturb central carbon metabolism, contributing to death via oxidative damage. Here, we genetically dissect this connection in Bacillus subtilis perturbed for cell wall synthesis, and identify key enzymatic steps in upstream and downstream pathways that stimulate the generation of reactive oxygen species through cellular respiration. Our results also reveal the critical role of iron homeostasis for the oxidative damage-mediated lethal effects. We show that protection of cells from oxygen radicals via a recently discovered siderophore-like compound uncouples changes in cell morphology normally associated with cell death, from lysis as usually judged by a phase pale microscopic appearance. Phase paling appears to be closely associated with lipid peroxidation.

Suggested Citation

  • Yoshikazu Kawai & Maki Kawai & Eilidh Sohini Mackenzie & Yousef Dashti & Bernhard Kepplinger & Kevin John Waldron & Jeff Errington, 2023. "On the mechanisms of lysis triggered by perturbations of bacterial cell wall biosynthesis," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-39723-8
    DOI: 10.1038/s41467-023-39723-8
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-39723-8
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-023-39723-8?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. M. Leaver & P. Domínguez-Cuevas & J. M. Coxhead & R. A. Daniel & J. Errington, 2009. "Life without a wall or division machine in Bacillus subtilis," Nature, Nature, vol. 457(7231), pages 849-853, February.
    2. Alexander J. Meeske & Eammon P. Riley & William P. Robins & Tsuyoshi Uehara & John J. Mekalanos & Daniel Kahne & Suzanne Walker & Andrew C. Kruse & Thomas G. Bernhardt & David Z. Rudner, 2016. "SEDS proteins are a widespread family of bacterial cell wall polymerases," Nature, Nature, vol. 537(7622), pages 634-638, September.
    3. M. Leaver & P. Domínguez-Cuevas & J. M. Coxhead & R. A. Daniel & J. Errington, 2009. "Erratum: Life without a wall or division machine in Bacillus subtilis," Nature, Nature, vol. 460(7254), pages 538-538, July.
    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. Renée Kapteijn & Shraddha Shitut & Dennis Aschmann & Le Zhang & Marit Beer & Deniz Daviran & Rona Roverts & Anat Akiva & Gilles P. Wezel & Alexander Kros & Dennis Claessen, 2022. "Endocytosis-like DNA uptake by cell wall-deficient bacteria," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    2. Simone Pelliciari & Salomé Bodet-Lefèvre & Stepan Fenyk & Daniel Stevens & Charles Winterhalter & Frederic D. Schramm & Sara Pintar & Daniel R. Burnham & George Merces & Tomas T. Richardson & Yumiko T, 2023. "The bacterial replication origin BUS promotes nucleobase capture," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    3. Miloš Tišma & Florian Patrick Bock & Jacob Kerssemakers & Hammam Antar & Aleksandre Japaridze & Stephan Gruber & Cees Dekker, 2024. "Direct observation of a crescent-shape chromosome in expanded Bacillus subtilis cells," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    4. Manuel Halte & Ekaterina P. Andrianova & Christian Goosmann & Fabienne F. V. Chevance & Kelly T. Hughes & Igor B. Zhulin & Marc Erhardt, 2024. "FlhE functions as a chaperone to prevent formation of periplasmic flagella in Gram-negative bacteria," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    5. Rie Nygaard & Chris L. B. Graham & Meagan Belcher Dufrisne & Jonathan D. Colburn & Joseph Pepe & Molly A. Hydorn & Silvia Corradi & Chelsea M. Brown & Khuram U. Ashraf & Owen N. Vickery & Nicholas S. , 2023. "Structural basis of peptidoglycan synthesis by E. coli RodA-PBP2 complex," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    6. Huan Zhang & Srutha Venkatesan & Emily Ng & Beiyan Nan, 2023. "Coordinated peptidoglycan synthases and hydrolases stabilize the bacterial cell wall," Nature Communications, Nature, vol. 14(1), pages 1-9, December.
    7. Shailab Shrestha & Najwa Taib & Simonetta Gribaldo & Aimee Shen, 2023. "Diversification of division mechanisms in endospore-forming bacteria revealed by analyses of peptidoglycan synthesis in Clostridioides difficile," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    8. Irina Shlosman & Elayne M. Fivenson & Morgan S. A. Gilman & Tyler A. Sisley & Suzanne Walker & Thomas G. Bernhardt & Andrew C. Kruse & Joseph J. Loparo, 2023. "Allosteric activation of cell wall synthesis during bacterial growth," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    9. Michael D. Sacco & Shaohui Wang & Swamy R. Adapa & Xiujun Zhang & Eric M. Lewandowski & Maura V. Gongora & Dimitra Keramisanou & Zachary D. Atlas & Julia A. Townsend & Jean R. Gatdula & Ryan T. Morgan, 2022. "A unique class of Zn2+-binding serine-based PBPs underlies cephalosporin resistance and sporogenesis in Clostridioides difficile," Nature Communications, Nature, vol. 13(1), pages 1-13, 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:14:y:2023:i:1:d:10.1038_s41467-023-39723-8. 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.