Clustering as a Means To Control Nitrate Respiration Efficiency and Toxicity in <named-content content-type="genus-species">Escherichia coli</named-content>

ABSTRACT Respiration is a fundamental process that has to optimally respond to metabolic demand and environmental changes. We previously showed that nitrate respiration, crucial for gut colonization by enterobacteria, is controlled by polar clustering of the nitrate reductase increasing the electron...

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Autores principales:	Suzy Bulot, Stéphane Audebert, Laetitia Pieulle, Farida Seduk, Emilie Baudelet, Leon Espinosa, Marie-Camille Pizay, Luc Camoin, Axel Magalon
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	cellular respiration fluorescence microscopy metalloprotein nitric oxide Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/4534ee1c0ffd430f8395f74878c75774
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spelling	oai:doaj.org-article:4534ee1c0ffd430f8395f74878c757742021-11-15T15:59:40ZClustering as a Means To Control Nitrate Respiration Efficiency and Toxicity in <named-content content-type="genus-species">Escherichia coli</named-content>10.1128/mBio.01832-192150-7511https://doaj.org/article/4534ee1c0ffd430f8395f74878c757742019-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01832-19https://doaj.org/toc/2150-7511ABSTRACT Respiration is a fundamental process that has to optimally respond to metabolic demand and environmental changes. We previously showed that nitrate respiration, crucial for gut colonization by enterobacteria, is controlled by polar clustering of the nitrate reductase increasing the electron flux through the complex. Here, we show that the formate dehydrogenase electron-donating complex, FdnGHI, also clusters at the cell poles under nitrate-respiring conditions. Its proximity to the nitrate reductase complex was confirmed by its identification in the interactome of the latter, which appears to be specific to the nitrate-respiring condition. Interestingly, we have identified a multiprotein complex dedicated to handle nitric oxide resulting from the enhanced activity of the electron transport chain terminated by nitrate reductase. We demonstrated that the cytoplasmic NADH-dependent nitrite reductase NirBD and the hybrid cluster protein Hcp are key contributors to regulation of the nitric oxide level during nitrate respiration. Thus, gathering of actors involved in respiration and NO homeostasis seems to be critical to balancing maximization of electron flux and the resulting toxicity. IMPORTANCE Most bacteria rely on the redox activity of respiratory complexes embedded in the cytoplasmic membrane to gain energy in the form of ATP and of an electrochemical gradient established across the membrane. Nevertheless, production of harmful and toxic nitric oxide by actively growing bacteria as either an intermediate or side-product of nitrate respiration challenges how homeostasis control is exerted. Here, we show that components of the nitrate electron transport chain are clustered, likely influencing the kinetics of the process. Nitric oxide production from this respiratory chain is controlled and handled through a multiprotein complex, including detoxifying systems. These findings point to an essential role of compartmentalization of respiratory components in bacterial cell growth.Suzy BulotStéphane AudebertLaetitia PieulleFarida SedukEmilie BaudeletLeon EspinosaMarie-Camille PizayLuc CamoinAxel MagalonAmerican Society for Microbiologyarticlecellular respirationfluorescence microscopymetalloproteinnitric oxideMicrobiologyQR1-502ENmBio, Vol 10, Iss 5 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	cellular respiration fluorescence microscopy metalloprotein nitric oxide Microbiology QR1-502
spellingShingle	cellular respiration fluorescence microscopy metalloprotein nitric oxide Microbiology QR1-502 Suzy Bulot Stéphane Audebert Laetitia Pieulle Farida Seduk Emilie Baudelet Leon Espinosa Marie-Camille Pizay Luc Camoin Axel Magalon Clustering as a Means To Control Nitrate Respiration Efficiency and Toxicity in <named-content content-type="genus-species">Escherichia coli</named-content>
description	ABSTRACT Respiration is a fundamental process that has to optimally respond to metabolic demand and environmental changes. We previously showed that nitrate respiration, crucial for gut colonization by enterobacteria, is controlled by polar clustering of the nitrate reductase increasing the electron flux through the complex. Here, we show that the formate dehydrogenase electron-donating complex, FdnGHI, also clusters at the cell poles under nitrate-respiring conditions. Its proximity to the nitrate reductase complex was confirmed by its identification in the interactome of the latter, which appears to be specific to the nitrate-respiring condition. Interestingly, we have identified a multiprotein complex dedicated to handle nitric oxide resulting from the enhanced activity of the electron transport chain terminated by nitrate reductase. We demonstrated that the cytoplasmic NADH-dependent nitrite reductase NirBD and the hybrid cluster protein Hcp are key contributors to regulation of the nitric oxide level during nitrate respiration. Thus, gathering of actors involved in respiration and NO homeostasis seems to be critical to balancing maximization of electron flux and the resulting toxicity. IMPORTANCE Most bacteria rely on the redox activity of respiratory complexes embedded in the cytoplasmic membrane to gain energy in the form of ATP and of an electrochemical gradient established across the membrane. Nevertheless, production of harmful and toxic nitric oxide by actively growing bacteria as either an intermediate or side-product of nitrate respiration challenges how homeostasis control is exerted. Here, we show that components of the nitrate electron transport chain are clustered, likely influencing the kinetics of the process. Nitric oxide production from this respiratory chain is controlled and handled through a multiprotein complex, including detoxifying systems. These findings point to an essential role of compartmentalization of respiratory components in bacterial cell growth.
format	article
author	Suzy Bulot Stéphane Audebert Laetitia Pieulle Farida Seduk Emilie Baudelet Leon Espinosa Marie-Camille Pizay Luc Camoin Axel Magalon
author_facet	Suzy Bulot Stéphane Audebert Laetitia Pieulle Farida Seduk Emilie Baudelet Leon Espinosa Marie-Camille Pizay Luc Camoin Axel Magalon
author_sort	Suzy Bulot
title	Clustering as a Means To Control Nitrate Respiration Efficiency and Toxicity in <named-content content-type="genus-species">Escherichia coli</named-content>
title_short	Clustering as a Means To Control Nitrate Respiration Efficiency and Toxicity in <named-content content-type="genus-species">Escherichia coli</named-content>
title_full	Clustering as a Means To Control Nitrate Respiration Efficiency and Toxicity in <named-content content-type="genus-species">Escherichia coli</named-content>
title_fullStr	Clustering as a Means To Control Nitrate Respiration Efficiency and Toxicity in <named-content content-type="genus-species">Escherichia coli</named-content>
title_full_unstemmed	Clustering as a Means To Control Nitrate Respiration Efficiency and Toxicity in <named-content content-type="genus-species">Escherichia coli</named-content>
title_sort	clustering as a means to control nitrate respiration efficiency and toxicity in <named-content content-type="genus-species">escherichia coli</named-content>
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/4534ee1c0ffd430f8395f74878c75774
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Clustering as a Means To Control Nitrate Respiration Efficiency and Toxicity in <named-content content-type="genus-species">Escherichia coli</named-content>

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