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Preparations of Terminal Oxidase Cytochrome bd-II Isolated from Escherichia coli Reveal Significant Hydrogen Peroxide Scavenging Activity

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Abstract

Cytochrome bd-II is one of the three terminal quinol oxidases of the aerobic respiratory chain of Escherichia coli. Preparations of the detergent-solubilized untagged bd-II oxidase isolated from the bacterium were shown to scavenge hydrogen peroxide (H2O2) with high rate producing molecular oxygen (O2). Addition of H2O2 to the same buffer that does not contain enzyme or contains thermally denatured cytochrome bd-II does not lead to any O2 production. The latter observation rules out involvement of adventitious transition metals bound to the protein. The H2O2-induced O2 production is not susceptible to inhibition by N-ethylmaleimide (the sulfhydryl binding compound), antimycin A (the compound that binds specifically to a quinol binding site), and CO (diatomic gas that binds specifically to the reduced heme d). However, O2 formation is inhibited by cyanide (IC50 = 4.5 ± 0.5 µM) and azide. Addition of H2O2 in the presence of dithiothreitol and ubiquinone-1 does not inactivate cytochrome bd-II and apparently does not affect the O2 reductase activity of the enzyme. The ability of cytochrome bd-II to detoxify H2O2 could play a role in bacterial physiology by conferring resistance to the peroxide-mediated stress.

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Abbreviations

DTT:

dithiothreitol

Q1 :

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

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Acknowledgments

The authors are grateful to M. Bekker (University of Amsterdam, Amsterdam, The Netherlands) for providing the strain of E. coli MB37 and to R. B. Gennis (University of Illinois, Urbana, Illinois, USA) for the strain of E. coli GO105/pTK1. V. B. Borisov would also like to express his deepest gratitude to A. D. Vinogradov (untimely departed), the author’s teacher from the student bench to the defense of the doctoral dissertation.

Funding

This work was supported by the Russian Science Foundation (project no. 22-24-00045, https://rscf.ru/en/project/22-24-00045/).

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Authors and Affiliations

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

    Elena Forte & Martina R. Nastasi

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

    Vitaliy B. Borisov

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  1. Elena Forte
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  2. Martina R. Nastasi
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Contributions

E.F. and V.B.B. conceived the study, designed the experimental plan and wrote the paper. E.F., M.R.N., and V.B.B. performed and analyzed the experiments. All authors reviewed the results, contributed to data interpretation and critical revision of the manuscript, and approved the final version of the manuscript.

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Correspondence to Vitaliy B. Borisov.

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The authors declare no conflicts of interests in financial or any other sphere. This article does not contain any studies with human participants or animal performed by any of the authors.

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Forte, E., Nastasi, M.R. & Borisov, V.B. Preparations of Terminal Oxidase Cytochrome bd-II Isolated from Escherichia coli Reveal Significant Hydrogen Peroxide Scavenging Activity. Biochemistry Moscow 87, 720–730 (2022). https://doi.org/10.1134/S0006297922080041

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