Nitrite Derived from Endogenous Bacterial Nitric Oxide Synthase Activity Promotes Aerobic Respiration

ABSTRACT Macrophage-derived nitric oxide (NO·) is a crucial effector against invading pathogens. Yet, paradoxically, several bacterial species, including some pathogens, are known to endogenously produce NO· via nitric oxide synthase (NOS) activity, despite its apparent cytotoxicity. Here, we reveal...

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Autores principales:	Sujata S. Chaudhari, Minji Kim, Shulei Lei, Fareha Razvi, Abdulelah A. Alqarzaee, Elizabeth H. Hutfless, Robert Powers, Matthew C. Zimmerman, Paul D. Fey, Vinai C. Thomas
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2017
Materias:	Staphylococcus aureus TCA cycle cytochrome bo oxidase nitric oxide synthase nitrite quinol oxidase Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/093ff564b67d4755b634791f586c6334
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spelling	oai:doaj.org-article:093ff564b67d4755b634791f586c63342021-11-15T15:51:43ZNitrite Derived from Endogenous Bacterial Nitric Oxide Synthase Activity Promotes Aerobic Respiration10.1128/mBio.00887-172150-7511https://doaj.org/article/093ff564b67d4755b634791f586c63342017-09-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00887-17https://doaj.org/toc/2150-7511ABSTRACT Macrophage-derived nitric oxide (NO·) is a crucial effector against invading pathogens. Yet, paradoxically, several bacterial species, including some pathogens, are known to endogenously produce NO· via nitric oxide synthase (NOS) activity, despite its apparent cytotoxicity. Here, we reveal a conserved role for bacterial NOS in activating aerobic respiration. We demonstrate that nitrite generated from endogenous NO· decomposition stimulates quinol oxidase activity in Staphylococcus aureus and increases the rate of cellular respiration. This not only supports optimal growth of this organism but also prevents a dysbalance in central metabolism. Further, we also show that activity of the SrrAB two-component system alleviates the physiological defects of the nos mutant. Our findings suggest that NOS and SrrAB constitute two distinct but functionally redundant routes for controlling staphylococcal respiration during aerobic growth. IMPORTANCE Despite its potential autotoxic effects, several bacterial species, including pathogenic staphylococcal species, produce NO· endogenously through nitric oxide synthase (NOS) activity. Therefore, how endogenous NO· influences bacterial fitness remains unclear. Here we show that the oxidation of NO· to nitrite increases aerobic respiration and consequently optimizes central metabolism to favor growth. Importantly, we also demonstrate that cells have a “fail-safe” mechanism that can maintain respiratory activity through the SrrAB two-component signaling regulon should NOS-derived nitrite levels decrease. These findings identify NOS and SrrAB as critical determinants of staphylococcal respiratory control and highlight their potential as therapeutic targets.Sujata S. ChaudhariMinji KimShulei LeiFareha RazviAbdulelah A. AlqarzaeeElizabeth H. HutflessRobert PowersMatthew C. ZimmermanPaul D. FeyVinai C. ThomasAmerican Society for MicrobiologyarticleStaphylococcus aureusTCA cyclecytochrome bo oxidasenitric oxide synthasenitritequinol oxidaseMicrobiologyQR1-502ENmBio, Vol 8, Iss 4 (2017)
institution	DOAJ
collection	DOAJ
language	EN
topic	Staphylococcus aureus TCA cycle cytochrome bo oxidase nitric oxide synthase nitrite quinol oxidase Microbiology QR1-502
spellingShingle	Staphylococcus aureus TCA cycle cytochrome bo oxidase nitric oxide synthase nitrite quinol oxidase Microbiology QR1-502 Sujata S. Chaudhari Minji Kim Shulei Lei Fareha Razvi Abdulelah A. Alqarzaee Elizabeth H. Hutfless Robert Powers Matthew C. Zimmerman Paul D. Fey Vinai C. Thomas Nitrite Derived from Endogenous Bacterial Nitric Oxide Synthase Activity Promotes Aerobic Respiration
description	ABSTRACT Macrophage-derived nitric oxide (NO·) is a crucial effector against invading pathogens. Yet, paradoxically, several bacterial species, including some pathogens, are known to endogenously produce NO· via nitric oxide synthase (NOS) activity, despite its apparent cytotoxicity. Here, we reveal a conserved role for bacterial NOS in activating aerobic respiration. We demonstrate that nitrite generated from endogenous NO· decomposition stimulates quinol oxidase activity in Staphylococcus aureus and increases the rate of cellular respiration. This not only supports optimal growth of this organism but also prevents a dysbalance in central metabolism. Further, we also show that activity of the SrrAB two-component system alleviates the physiological defects of the nos mutant. Our findings suggest that NOS and SrrAB constitute two distinct but functionally redundant routes for controlling staphylococcal respiration during aerobic growth. IMPORTANCE Despite its potential autotoxic effects, several bacterial species, including pathogenic staphylococcal species, produce NO· endogenously through nitric oxide synthase (NOS) activity. Therefore, how endogenous NO· influences bacterial fitness remains unclear. Here we show that the oxidation of NO· to nitrite increases aerobic respiration and consequently optimizes central metabolism to favor growth. Importantly, we also demonstrate that cells have a “fail-safe” mechanism that can maintain respiratory activity through the SrrAB two-component signaling regulon should NOS-derived nitrite levels decrease. These findings identify NOS and SrrAB as critical determinants of staphylococcal respiratory control and highlight their potential as therapeutic targets.
format	article
author	Sujata S. Chaudhari Minji Kim Shulei Lei Fareha Razvi Abdulelah A. Alqarzaee Elizabeth H. Hutfless Robert Powers Matthew C. Zimmerman Paul D. Fey Vinai C. Thomas
author_facet	Sujata S. Chaudhari Minji Kim Shulei Lei Fareha Razvi Abdulelah A. Alqarzaee Elizabeth H. Hutfless Robert Powers Matthew C. Zimmerman Paul D. Fey Vinai C. Thomas
author_sort	Sujata S. Chaudhari
title	Nitrite Derived from Endogenous Bacterial Nitric Oxide Synthase Activity Promotes Aerobic Respiration
title_short	Nitrite Derived from Endogenous Bacterial Nitric Oxide Synthase Activity Promotes Aerobic Respiration
title_full	Nitrite Derived from Endogenous Bacterial Nitric Oxide Synthase Activity Promotes Aerobic Respiration
title_fullStr	Nitrite Derived from Endogenous Bacterial Nitric Oxide Synthase Activity Promotes Aerobic Respiration
title_full_unstemmed	Nitrite Derived from Endogenous Bacterial Nitric Oxide Synthase Activity Promotes Aerobic Respiration
title_sort	nitrite derived from endogenous bacterial nitric oxide synthase activity promotes aerobic respiration
publisher	American Society for Microbiology
publishDate	2017
url	https://doaj.org/article/093ff564b67d4755b634791f586c6334
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Nitrite Derived from Endogenous Bacterial Nitric Oxide Synthase Activity Promotes Aerobic Respiration

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