Impact of Hydrogen Sulfide on Mitochondrial and Bacterial Bioenergetics

This review focuses on the effects of hydrogen sulfide (H<sub>2</sub>S) on the unique bioenergetic molecular machines in mitochondria and bacteria—the protein complexes of electron transport chains and associated enzymes. H<sub>2</sub>S, along with nitric oxide and carbon mon...

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Main Authors: Vitaliy B. Borisov, Elena Forte
Format: Article
Language:English
Published: MDPI AG 2021-11-01
Series:International Journal of Molecular Sciences
Subjects:
Online Access:https://www.mdpi.com/1422-0067/22/23/12688
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author Vitaliy B. Borisov
Elena Forte
author_facet Vitaliy B. Borisov
Elena Forte
author_sort Vitaliy B. Borisov
collection DOAJ
description This review focuses on the effects of hydrogen sulfide (H<sub>2</sub>S) on the unique bioenergetic molecular machines in mitochondria and bacteria—the protein complexes of electron transport chains and associated enzymes. H<sub>2</sub>S, along with nitric oxide and carbon monoxide, belongs to the class of endogenous gaseous signaling molecules. This compound plays critical roles in physiology and pathophysiology. Enzymes implicated in H<sub>2</sub>S metabolism and physiological actions are promising targets for novel pharmaceutical agents. The biological effects of H<sub>2</sub>S are biphasic, changing from cytoprotection to cytotoxicity through increasing the compound concentration. In mammals, H<sub>2</sub>S enhances the activity of F<sub>o</sub>F<sub>1</sub>-ATP (adenosine triphosphate) synthase and lactate dehydrogenase via their <i>S</i>-sulfhydration, thereby stimulating mitochondrial electron transport. H<sub>2</sub>S serves as an electron donor for the mitochondrial respiratory chain via sulfide quinone oxidoreductase and cytochrome <i>c</i> oxidase at low H<sub>2</sub>S levels. The latter enzyme is inhibited by high H<sub>2</sub>S concentrations, resulting in the reversible inhibition of electron transport and ATP production in mitochondria. In the branched respiratory chain of <i>Escherichia coli</i>, H<sub>2</sub>S inhibits the <i>bo</i><sub>3</sub> terminal oxidase but does not affect the alternative <i>bd</i>-type oxidases. Thus, in <i>E. coli</i> and presumably other bacteria, cytochrome <i>bd</i> permits respiration and cell growth in H<sub>2</sub>S-rich environments. A complete picture of the impact of H<sub>2</sub>S on bioenergetics is lacking, but this field is fast-moving, and active ongoing research on this topic will likely shed light on additional, yet unknown biological effects.
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spelling doaj.art-b5fa8fb6528248989f7450d86d8eba4d2023-11-23T02:26:26ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672021-11-0122231268810.3390/ijms222312688Impact of Hydrogen Sulfide on Mitochondrial and Bacterial BioenergeticsVitaliy B. Borisov0Elena Forte1Belozersky Institute of Physico-Chemical Biology, Lomonosov Moscow State University, Leninskie Gory, 119991 Moscow, RussiaDepartment of Biochemical Sciences, Sapienza University of Rome, 00185 Rome, ItalyThis review focuses on the effects of hydrogen sulfide (H<sub>2</sub>S) on the unique bioenergetic molecular machines in mitochondria and bacteria—the protein complexes of electron transport chains and associated enzymes. H<sub>2</sub>S, along with nitric oxide and carbon monoxide, belongs to the class of endogenous gaseous signaling molecules. This compound plays critical roles in physiology and pathophysiology. Enzymes implicated in H<sub>2</sub>S metabolism and physiological actions are promising targets for novel pharmaceutical agents. The biological effects of H<sub>2</sub>S are biphasic, changing from cytoprotection to cytotoxicity through increasing the compound concentration. In mammals, H<sub>2</sub>S enhances the activity of F<sub>o</sub>F<sub>1</sub>-ATP (adenosine triphosphate) synthase and lactate dehydrogenase via their <i>S</i>-sulfhydration, thereby stimulating mitochondrial electron transport. H<sub>2</sub>S serves as an electron donor for the mitochondrial respiratory chain via sulfide quinone oxidoreductase and cytochrome <i>c</i> oxidase at low H<sub>2</sub>S levels. The latter enzyme is inhibited by high H<sub>2</sub>S concentrations, resulting in the reversible inhibition of electron transport and ATP production in mitochondria. In the branched respiratory chain of <i>Escherichia coli</i>, H<sub>2</sub>S inhibits the <i>bo</i><sub>3</sub> terminal oxidase but does not affect the alternative <i>bd</i>-type oxidases. Thus, in <i>E. coli</i> and presumably other bacteria, cytochrome <i>bd</i> permits respiration and cell growth in H<sub>2</sub>S-rich environments. A complete picture of the impact of H<sub>2</sub>S on bioenergetics is lacking, but this field is fast-moving, and active ongoing research on this topic will likely shed light on additional, yet unknown biological effects.https://www.mdpi.com/1422-0067/22/23/12688hydrogen sulfidedonorsgasotransmittersmolecular bioenergeticsinhibitionelectron transport chain
spellingShingle Vitaliy B. Borisov
Elena Forte
Impact of Hydrogen Sulfide on Mitochondrial and Bacterial Bioenergetics
International Journal of Molecular Sciences
hydrogen sulfide
donors
gasotransmitters
molecular bioenergetics
inhibition
electron transport chain
title Impact of Hydrogen Sulfide on Mitochondrial and Bacterial Bioenergetics
title_full Impact of Hydrogen Sulfide on Mitochondrial and Bacterial Bioenergetics
title_fullStr Impact of Hydrogen Sulfide on Mitochondrial and Bacterial Bioenergetics
title_full_unstemmed Impact of Hydrogen Sulfide on Mitochondrial and Bacterial Bioenergetics
title_short Impact of Hydrogen Sulfide on Mitochondrial and Bacterial Bioenergetics
title_sort impact of hydrogen sulfide on mitochondrial and bacterial bioenergetics
topic hydrogen sulfide
donors
gasotransmitters
molecular bioenergetics
inhibition
electron transport chain
url https://www.mdpi.com/1422-0067/22/23/12688
work_keys_str_mv AT vitaliybborisov impactofhydrogensulfideonmitochondrialandbacterialbioenergetics
AT elenaforte impactofhydrogensulfideonmitochondrialandbacterialbioenergetics