IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-50278-0.html
   My bibliography  Save this article

FlhE functions as a chaperone to prevent formation of periplasmic flagella in Gram-negative bacteria

Author

Listed:
  • Manuel Halte

    (Humboldt-Universität zu Berlin)

  • Ekaterina P. Andrianova

    (The Ohio State University)

  • Christian Goosmann

    (Max Planck Institute for Infection Biology)

  • Fabienne F. V. Chevance

    (University of Utah)

  • Kelly T. Hughes

    (University of Utah)

  • Igor B. Zhulin

    (The Ohio State University)

  • Marc Erhardt

    (Humboldt-Universität zu Berlin
    Max Planck Unit for the Science of Pathogens)

Abstract

The bacterial flagellum, which facilitates motility, is composed of ~20 structural proteins organized into a long extracellular filament connected to a cytoplasmic rotor-stator complex via a periplasmic rod. Flagellum assembly is regulated by multiple checkpoints that ensure an ordered gene expression pattern coupled to the assembly of the various building blocks. Here, we use epifluorescence, super-resolution, and transmission electron microscopy to show that the absence of a periplasmic protein (FlhE) prevents proper flagellar morphogenesis and results in the formation of periplasmic flagella in Salmonella enterica. The periplasmic flagella disrupt cell wall synthesis, leading to a loss of normal cell morphology resulting in cell lysis. We propose that FlhE functions as a periplasmic chaperone to control assembly of the periplasmic rod, thus preventing formation of periplasmic flagella.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-50278-0
    DOI: 10.1038/s41467-024-50278-0
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-50278-0
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-024-50278-0?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. Koji Yonekura & Saori Maki-Yonekura & Keiichi Namba, 2003. "Complete atomic model of the bacterial flagellar filament by electron cryomicroscopy," Nature, Nature, vol. 424(6949), pages 643-650, August.
    2. Yukihiro Akeda & Jorge E. Galán, 2005. "Chaperone release and unfolding of substrates in type III secretion," Nature, Nature, vol. 437(7060), pages 911-915, October.
    3. 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.
    4. 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. William R Taylor & Teige R S Matthews-Palmer & Morgan Beeby, 2016. "Molecular Models for the Core Components of the Flagellar Type-III Secretion Complex," PLOS ONE, Public Library of Science, vol. 11(11), pages 1-33, November.
    3. 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.
    4. 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.
    5. 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.
    6. Vidhyavathi Raman & Clemencia M. Rojas & Balaji Vasudevan & Kevin Dunning & Jaydeep Kolape & Sunhee Oh & Jianfei Yun & Lishan Yang & Guangming Li & Bikram D. Pant & Qingzhen Jiang & Kirankumar S. Myso, 2022. "Agrobacterium expressing a type III secretion system delivers Pseudomonas effectors into plant cells to enhance transformation," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    7. Xiaojiao Yang & Yanzhi Guo & Jiesi Luo & Xuemei Pu & Menglong Li, 2013. "Effective Identification of Gram-Negative Bacterial Type III Secreted Effectors Using Position-Specific Residue Conservation Profiles," PLOS ONE, Public Library of Science, vol. 8(12), pages 1-12, December.
    8. Dominic Gilzer & Madeleine Schreiner & Hartmut H. Niemann, 2022. "Direct interaction of a chaperone-bound type III secretion substrate with the export gate," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    9. Jessie Lynda Fields & Hua Zhang & Nathan F. Bellis & Holly A. Petersen & Sajal K. Halder & Shane T. Rich-New & Mart Krupovic & Hui Wu & Fengbin Wang, 2024. "Structural diversity and clustering of bacterial flagellar outer domains," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    10. Nicholas M Thomson & Josie L Ferreira & Teige R Matthews-Palmer & Morgan Beeby & Mark J Pallen, 2018. "Giant flagellins form thick flagellar filaments in two species of marine γ-proteobacteria," PLOS ONE, Public Library of Science, vol. 13(11), pages 1-12, November.

    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:15:y:2024:i:1:d:10.1038_s41467-024-50278-0. 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.