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Ton motor conformational switch and peptidoglycan role in bacterial nutrient uptake

Author

Listed:
  • Maximilian Zinke

    (Institut Pasteur, Université Paris Cité, CNRS UMR3528, Bacterial Transmembrane Systems Unit)

  • Maylis Lejeune

    (Institut Pasteur, Université Paris Cité, CNRS UMR3528, Bacterial Transmembrane Systems Unit)

  • Ariel Mechaly

    (Institut Pasteur, Université Paris Cité, CNRS UMR3528, Crystallography Platform)

  • Benjamin Bardiaux

    (Institut Pasteur, Université Paris Cité, CNRS UMR3528, Bacterial Transmembrane Systems Unit)

  • Ivo Gomperts Boneca

    (Institut Pasteur, Université Paris Cité, CNRS UMR6047, INSERM U1306, Unité de Biologie et génétique de la paroi bactérienne)

  • Philippe Delepelaire

    (Laboratoire de Biologie Physico-Chimique des Protéines Membranaires, Université Paris Cité, UMR7099 CNRS
    Institut de Biologie Physico-Chimique)

  • Nadia Izadi-Pruneyre

    (Institut Pasteur, Université Paris Cité, CNRS UMR3528, Bacterial Transmembrane Systems Unit)

Abstract

Active nutrient uptake is fundamental for survival and pathogenicity of Gram-negative bacteria, which operate a multi-protein Ton system to transport essential nutrients like metals and vitamins. This system harnesses the proton motive force at the inner membrane to energize the import through the outer membrane, but the mechanism of energy transfer remains enigmatic. Here, we study the periplasmic domain of ExbD, a crucial component of the proton channel of the Ton system. We show that this domain is a dynamic dimer switching between two conformations representing the proton channel’s open and closed states. By in vivo phenotypic assays we demonstrate that this conformational switch is essential for the nutrient uptake by bacteria. The open state of ExbD triggers a disorder to order transition of TonB, enabling TonB to supply energy to the nutrient transporter. We also reveal the anchoring role of the peptidoglycan layer in this mechanism. Herein, we propose a mechanistic model for the Ton system, emphasizing ExbD duality and the pivotal catalytic role of peptidoglycan. Sequence analysis suggests that this mechanism is conserved in other systems energizing gliding motility and membrane integrity. Our study fills important gaps in understanding bacterial motor mechanism and proposes novel antibacterial strategies.

Suggested Citation

  • Maximilian Zinke & Maylis Lejeune & Ariel Mechaly & Benjamin Bardiaux & Ivo Gomperts Boneca & Philippe Delepelaire & Nadia Izadi-Pruneyre, 2024. "Ton motor conformational switch and peptidoglycan role in bacterial nutrient uptake," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-023-44606-z
    DOI: 10.1038/s41467-023-44606-z
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    References listed on IDEAS

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    1. Joanna Szczepaniak & Peter Holmes & Karthik Rajasekar & Renata Kaminska & Firdaus Samsudin & Patrick George Inns & Patrice Rassam & Syma Khalid & Seán M. Murray & Christina Redfield & Colin Kleanthous, 2020. "The lipoprotein Pal stabilises the bacterial outer membrane during constriction by a mobilisation-and-capture mechanism," Nature Communications, Nature, vol. 11(1), pages 1-14, December.
    2. Hervé Celia & Nicholas Noinaj & Stanislav D. Zakharov & Enrica Bordignon & Istvan Botos & Monica Santamaria & Travis J. Barnard & William A. Cramer & Roland Lloubes & Susan K. Buchanan, 2016. "Structural insight into the role of the Ton complex in energy transduction," Nature, Nature, vol. 538(7623), pages 60-65, October.
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