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Research Article | Molecular Biology and Physiology

Clustering as a Means To Control Nitrate Respiration Efficiency and Toxicity in Escherichia coli

Suzy Bulot, Stéphane Audebert, Laetitia Pieulle, Farida Seduk, Emilie Baudelet, Leon Espinosa, Marie-Camille Pizay, Luc Camoin, Axel Magalon
Markus W. Ribbe, Editor
Suzy Bulot
aAix-Marseille Université, CNRS, Laboratoire de Chimie Bactérienne (UMR7283), IMM, Marseille, France
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Stéphane Audebert
bAix-Marseille Université, Inserm, CNRS, Institut Paoli-Calmettes, CRCM, Marseille Protéomique, Marseille, France
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Laetitia Pieulle
aAix-Marseille Université, CNRS, Laboratoire de Chimie Bactérienne (UMR7283), IMM, Marseille, France
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Farida Seduk
aAix-Marseille Université, CNRS, Laboratoire de Chimie Bactérienne (UMR7283), IMM, Marseille, France
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Emilie Baudelet
bAix-Marseille Université, Inserm, CNRS, Institut Paoli-Calmettes, CRCM, Marseille Protéomique, Marseille, France
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Leon Espinosa
aAix-Marseille Université, CNRS, Laboratoire de Chimie Bactérienne (UMR7283), IMM, Marseille, France
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Marie-Camille Pizay
aAix-Marseille Université, CNRS, Laboratoire de Chimie Bactérienne (UMR7283), IMM, Marseille, France
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Luc Camoin
bAix-Marseille Université, Inserm, CNRS, Institut Paoli-Calmettes, CRCM, Marseille Protéomique, Marseille, France
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Axel Magalon
aAix-Marseille Université, CNRS, Laboratoire de Chimie Bactérienne (UMR7283), IMM, Marseille, France
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Markus W. Ribbe
University of California, Irvine
Roles: Editor
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DOI: 10.1128/mBio.01832-19
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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.

  • Copyright © 2019 Bulot et al.

This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license.

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Clustering as a Means To Control Nitrate Respiration Efficiency and Toxicity in Escherichia coli
Suzy Bulot, Stéphane Audebert, Laetitia Pieulle, Farida Seduk, Emilie Baudelet, Leon Espinosa, Marie-Camille Pizay, Luc Camoin, Axel Magalon
mBio Oct 2019, 10 (5) e01832-19; DOI: 10.1128/mBio.01832-19

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Clustering as a Means To Control Nitrate Respiration Efficiency and Toxicity in Escherichia coli
Suzy Bulot, Stéphane Audebert, Laetitia Pieulle, Farida Seduk, Emilie Baudelet, Leon Espinosa, Marie-Camille Pizay, Luc Camoin, Axel Magalon
mBio Oct 2019, 10 (5) e01832-19; DOI: 10.1128/mBio.01832-19
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KEYWORDS

cellular respiration
fluorescence microscopy
metalloprotein
nitric oxide

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