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Terminal Oxidase Cytochrome bd Protects Bacteria Against Hydrogen Sulfide Toxicity

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Abstract

Hydrogen sulfide (H2S) is often called the third gasotransmitter (after nitric oxide and carbon monoxide), or endogenous gaseous signaling molecule. This compound plays important roles in organisms from different taxonomic groups, from bacteria to animals and humans. In mammalian cells, H2S has a cytoprotective effect at nanomolar concentrations, but becomes cytotoxic at higher concentrations. The primary target of H2S is mitochondria. At submicromolar concentrations, H2S inhibits mitochondrial heme-copper cytochrome c oxidase, thereby blocking aerobic respiration and oxidative phosphorylation and eventually leading to cell death. Since the concentration of H2S in the gut is extremely high, the question arises – how can gut bacteria maintain the functioning of their oxygen-dependent respiratory electron transport chains under such conditions? This review provides an answer to this question and discusses the key role of non-canonical bd-type terminal oxidases of the enterobacterium Escherichia coli, a component of the gut microbiota, in maintaining aerobic respiration and growth in the presence of toxic concentrations of H2S in the light of recent experimental data.

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Abbreviations

3-MST:

3-mercaptopyruvate sulfurtransferase

CBS:

cystathionine β-synthase

CSE:

cystathionine γ-lyase

DTT:

dithiothreitol

EhOASS:

O-acetylserine sulfhydrylase from Entamoeba histolytica

OASS:

O-acetylserine sulfhydrylase

Q1 :

2,3-dimethoxy-5-methyl-6-(3-methyl-2-butenyl)-1,4-benzoquinone

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Acknowledgements

V. B. Borisov thanks V. P. Skulachev and A. D. Vinogradov for their interest in this work and useful discussion. V. B. Borisov would also like to express his deepest gratitude to A. A. Konstantinov (passed away May 1, 2020), who in 1993 suggested the author (then a PhD student) to study cytochrome bd.

Funding

This work was supported by the Russian Science Foundation (project no. 19-14-00063).

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  1. Belozersky Institute of Physico-Chemical Biology, Lomonosov Moscow State University, 119991, Moscow, Russia

    Vitaliy B. Borisov

  2. Department of Biochemical Sciences, Sapienza University of Rome, I-00185, Rome, Italy

    Elena Forte

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Borisov, V.B., Forte, E. Terminal Oxidase Cytochrome bd Protects Bacteria Against Hydrogen Sulfide Toxicity. Biochemistry Moscow 86, 22–32 (2021). https://doi.org/10.1134/S000629792101003X

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