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Ton Motor Conformational Switch and Peptidoglycan Role in Bacterial Nutrient Uptake
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 o...
Autores principales: | , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Cold Spring Harbor Laboratory
2023
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10441417/ https://www.ncbi.nlm.nih.gov/pubmed/37609138 http://dx.doi.org/10.1101/2023.08.11.552980 |
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author | Zinke, Maximilian Lejeune, Maylis Mechaly, Ariel Bardiaux, Benjamin Boneca, Ivo Gomperts Delepelaire, Philippe Izadi-Pruneyre, Nadia |
author_facet | Zinke, Maximilian Lejeune, Maylis Mechaly, Ariel Bardiaux, Benjamin Boneca, Ivo Gomperts Delepelaire, Philippe Izadi-Pruneyre, Nadia |
author_sort | Zinke, Maximilian |
collection | PubMed |
description | 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. |
format | Online Article Text |
id | pubmed-10441417 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2023 |
publisher | Cold Spring Harbor Laboratory |
record_format | MEDLINE/PubMed |
spelling | pubmed-104414172023-08-22 Ton Motor Conformational Switch and Peptidoglycan Role in Bacterial Nutrient Uptake Zinke, Maximilian Lejeune, Maylis Mechaly, Ariel Bardiaux, Benjamin Boneca, Ivo Gomperts Delepelaire, Philippe Izadi-Pruneyre, Nadia bioRxiv Article 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. Cold Spring Harbor Laboratory 2023-08-11 /pmc/articles/PMC10441417/ /pubmed/37609138 http://dx.doi.org/10.1101/2023.08.11.552980 Text en https://creativecommons.org/licenses/by-nc-nd/4.0/This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (https://creativecommons.org/licenses/by-nc-nd/4.0/) , which allows reusers to copy and distribute the material in any medium or format in unadapted form only, for noncommercial purposes only, and only so long as attribution is given to the creator. |
spellingShingle | Article Zinke, Maximilian Lejeune, Maylis Mechaly, Ariel Bardiaux, Benjamin Boneca, Ivo Gomperts Delepelaire, Philippe Izadi-Pruneyre, Nadia Ton Motor Conformational Switch and Peptidoglycan Role in Bacterial Nutrient Uptake |
title | Ton Motor Conformational Switch and Peptidoglycan Role in Bacterial Nutrient Uptake |
title_full | Ton Motor Conformational Switch and Peptidoglycan Role in Bacterial Nutrient Uptake |
title_fullStr | Ton Motor Conformational Switch and Peptidoglycan Role in Bacterial Nutrient Uptake |
title_full_unstemmed | Ton Motor Conformational Switch and Peptidoglycan Role in Bacterial Nutrient Uptake |
title_short | Ton Motor Conformational Switch and Peptidoglycan Role in Bacterial Nutrient Uptake |
title_sort | ton motor conformational switch and peptidoglycan role in bacterial nutrient uptake |
topic | Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10441417/ https://www.ncbi.nlm.nih.gov/pubmed/37609138 http://dx.doi.org/10.1101/2023.08.11.552980 |
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