Cytochrome <italic toggle="yes">bd</italic>-Dependent Bioenergetics and Antinitrosative Defenses in <italic toggle="yes">Salmonella</italic> Pathogenesis

ABSTRACT In the course of an infection, Salmonella enterica occupies diverse anatomical sites with various concentrations of oxygen (O2) and nitric oxide (NO). These diatomic gases compete for binding to catalytic metal groups of quinol oxidases. Enterobacteriaceae express two evolutionarily distinc...

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Autores principales:	Jessica Jones-Carson, Maroof Husain, Lin Liu, David J. Orlicky, Andrés Vázquez-Torres
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2016
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/c753637443f6408291a031610070c678
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spelling	oai:doaj.org-article:c753637443f6408291a031610070c6782021-11-15T15:50:15ZCytochrome <italic toggle="yes">bd</italic>-Dependent Bioenergetics and Antinitrosative Defenses in <italic toggle="yes">Salmonella</italic> Pathogenesis10.1128/mBio.02052-162150-7511https://doaj.org/article/c753637443f6408291a031610070c6782016-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02052-16https://doaj.org/toc/2150-7511ABSTRACT In the course of an infection, Salmonella enterica occupies diverse anatomical sites with various concentrations of oxygen (O2) and nitric oxide (NO). These diatomic gases compete for binding to catalytic metal groups of quinol oxidases. Enterobacteriaceae express two evolutionarily distinct classes of quinol oxidases that differ in affinity for O2 and NO as well as stoichiometry of H+ translocated across the cytoplasmic membrane. The investigations presented here show that the dual function of bacterial cytochrome bd in bioenergetics and antinitrosative defense enhances Salmonella virulence. The high affinity of cytochrome bd for O2 optimizes respiratory rates in hypoxic cultures, and thus, this quinol oxidase maximizes bacterial growth under O2-limiting conditions. Our investigations also indicate that cytochrome bd, rather than cytochrome bo, is an intrinsic component of the adaptive antinitrosative toolbox of Salmonella. Accordingly, induction of cytochrome bd helps Salmonella grow and respire in the presence of inhibitory NO. The combined antinitrosative defenses of cytochrome bd and the flavohemoglobin Hmp account for a great part of the adaptations that help Salmonella recover from the antimicrobial activity of NO. Moreover, the antinitrosative defenses of cytochrome bd and flavohemoglobin Hmp synergize to promote Salmonella growth in systemic tissues. Collectively, our investigations indicate that cytochrome bd is a critical means by which Salmonella resists the nitrosative stress that is engendered in the innate response of mammalian hosts while it concomitantly allows for proper O2 utilization in tissue hypoxia. IMPORTANCE It is becoming quite apparent that metabolism is critically important to the virulence potential of pathogenic microorganisms. Bacterial cells use a variety of terminal electron acceptors to power electron transport chains and metabolic processes. Of all the electron acceptors available to bacteria, utilization of O2 yields the most energy while diversifying the type of substrates that a pathogen can use. Recent investigations have demonstrated important roles for bd-type quinol oxidases with high affinity for O2 in bacterial pathogenesis. The investigations presented here have revealed that cytochrome bd potentiates virulence of a clinically relevant bacterial pathogen by fueling bioenergetics of prokaryotic cells while protecting the respiratory chain against NO toxicity. The adaptive antinitrosative defenses afforded by cytochrome bd synergize with other NO-detoxifying systems to preserve cellular bioenergetics, thereby promoting bacterial virulence in tissue hypoxia.Jessica Jones-CarsonMaroof HusainLin LiuDavid J. OrlickyAndrés Vázquez-TorresAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 7, Iss 6 (2016)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Jessica Jones-Carson Maroof Husain Lin Liu David J. Orlicky Andrés Vázquez-Torres Cytochrome <italic toggle="yes">bd</italic>-Dependent Bioenergetics and Antinitrosative Defenses in <italic toggle="yes">Salmonella</italic> Pathogenesis
description	ABSTRACT In the course of an infection, Salmonella enterica occupies diverse anatomical sites with various concentrations of oxygen (O2) and nitric oxide (NO). These diatomic gases compete for binding to catalytic metal groups of quinol oxidases. Enterobacteriaceae express two evolutionarily distinct classes of quinol oxidases that differ in affinity for O2 and NO as well as stoichiometry of H+ translocated across the cytoplasmic membrane. The investigations presented here show that the dual function of bacterial cytochrome bd in bioenergetics and antinitrosative defense enhances Salmonella virulence. The high affinity of cytochrome bd for O2 optimizes respiratory rates in hypoxic cultures, and thus, this quinol oxidase maximizes bacterial growth under O2-limiting conditions. Our investigations also indicate that cytochrome bd, rather than cytochrome bo, is an intrinsic component of the adaptive antinitrosative toolbox of Salmonella. Accordingly, induction of cytochrome bd helps Salmonella grow and respire in the presence of inhibitory NO. The combined antinitrosative defenses of cytochrome bd and the flavohemoglobin Hmp account for a great part of the adaptations that help Salmonella recover from the antimicrobial activity of NO. Moreover, the antinitrosative defenses of cytochrome bd and flavohemoglobin Hmp synergize to promote Salmonella growth in systemic tissues. Collectively, our investigations indicate that cytochrome bd is a critical means by which Salmonella resists the nitrosative stress that is engendered in the innate response of mammalian hosts while it concomitantly allows for proper O2 utilization in tissue hypoxia. IMPORTANCE It is becoming quite apparent that metabolism is critically important to the virulence potential of pathogenic microorganisms. Bacterial cells use a variety of terminal electron acceptors to power electron transport chains and metabolic processes. Of all the electron acceptors available to bacteria, utilization of O2 yields the most energy while diversifying the type of substrates that a pathogen can use. Recent investigations have demonstrated important roles for bd-type quinol oxidases with high affinity for O2 in bacterial pathogenesis. The investigations presented here have revealed that cytochrome bd potentiates virulence of a clinically relevant bacterial pathogen by fueling bioenergetics of prokaryotic cells while protecting the respiratory chain against NO toxicity. The adaptive antinitrosative defenses afforded by cytochrome bd synergize with other NO-detoxifying systems to preserve cellular bioenergetics, thereby promoting bacterial virulence in tissue hypoxia.
format	article
author	Jessica Jones-Carson Maroof Husain Lin Liu David J. Orlicky Andrés Vázquez-Torres
author_facet	Jessica Jones-Carson Maroof Husain Lin Liu David J. Orlicky Andrés Vázquez-Torres
author_sort	Jessica Jones-Carson
title	Cytochrome <italic toggle="yes">bd</italic>-Dependent Bioenergetics and Antinitrosative Defenses in <italic toggle="yes">Salmonella</italic> Pathogenesis
title_short	Cytochrome <italic toggle="yes">bd</italic>-Dependent Bioenergetics and Antinitrosative Defenses in <italic toggle="yes">Salmonella</italic> Pathogenesis
title_full	Cytochrome <italic toggle="yes">bd</italic>-Dependent Bioenergetics and Antinitrosative Defenses in <italic toggle="yes">Salmonella</italic> Pathogenesis
title_fullStr	Cytochrome <italic toggle="yes">bd</italic>-Dependent Bioenergetics and Antinitrosative Defenses in <italic toggle="yes">Salmonella</italic> Pathogenesis
title_full_unstemmed	Cytochrome <italic toggle="yes">bd</italic>-Dependent Bioenergetics and Antinitrosative Defenses in <italic toggle="yes">Salmonella</italic> Pathogenesis
title_sort	cytochrome <italic toggle="yes">bd</italic>-dependent bioenergetics and antinitrosative defenses in <italic toggle="yes">salmonella</italic> pathogenesis
publisher	American Society for Microbiology
publishDate	2016
url	https://doaj.org/article/c753637443f6408291a031610070c678
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Cytochrome <italic toggle="yes">bd</italic>-Dependent Bioenergetics and Antinitrosative Defenses in <italic toggle="yes">Salmonella</italic> Pathogenesis

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