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EcoSal Plus

Domain 3:

Metabolism

Oxygen as Acceptor

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  • Authors: Vitaliy B. Borisov1, and Michael I. Verkhovsky2,3
  • Editor: Valley Stewart4
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Department of Molecular Energetics of Microorganisms, Belozersky Institute of Physico-Chemical Biology, Lomonosov Moscow State University, Moscow 119991, Russia; 2: Deceased 4 October 2011; 3: Helsinki Bioenergetics Group, Institute of Biotechnology, University of Helsinki, 00014, Helsinki, Finland; 4: University of California—Davis, Davis, CA
  • Received 19 August 2015 Accepted 14 September 2015 Published 23 October 2015
  • Address correspondence to Vitaliy B. Borisov, bor@genebee.msu.su
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  • Abstract:

    Like most bacteria, has a flexible and branched respiratory chain that enables the prokaryote to live under a variety of environmental conditions, from highly aerobic to completely anaerobic. In general, the bacterial respiratory chain is composed of dehydrogenases, a quinone pool, and reductases. Substrate-specific dehydrogenases transfer reducing equivalents from various donor substrates (NADH, succinate, glycerophosphate, formate, hydrogen, pyruvate, and lactate) to a quinone pool (menaquinone, ubiquinone, and dimethylmenoquinone). Then electrons from reduced quinones (quinols) are transferred by terminal reductases to different electron acceptors. Under aerobic growth conditions, the terminal electron acceptor is molecular oxygen. A transfer of electrons from quinol to O is served by two major oxidoreductases (oxidases), cytochrome encoded by and cytochrome encoded by . Terminal oxidases of aerobic respiratory chains of bacteria, which use O as the final electron acceptor, can oxidize one of two alternative electron donors, either cytochrome or quinol. This review compares the effects of different inhibitors on the respiratory activities of cytochrome and cytochrome in . It also presents a discussion on the genetics and the prosthetic groups of cytochrome and cytochrome . The membrane contains three types of quinones that all have an octaprenyl side chain (C). It has been proposed that the oxidase can have two ubiquinone-binding sites with different affinities.

    : The revised article comprises additional information about subunit composition of cytochrome and its role in bacterial resistance to nitrosative and oxidative stresses. Also, we present the novel data on the electrogenic function of -encoded cytochrome -II, a second -type oxidase that had been thought not to contribute to generation of a proton motive force in , although its spectral properties closely resemble those of -encoded cytochrome .

  • Citation: Borisov V, Verkhovsky M. 2015. Oxygen as Acceptor, EcoSal Plus 2015; doi:10.1128/ecosalplus.ESP-0012-2015

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295. journal-id:
ecosalplus.ESP-0012-2015.citations
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/content/journal/ecosalplus/10.1128/ecosalplus.ESP-0012-2015
2015-10-23
2017-11-21

Abstract:

Like most bacteria, has a flexible and branched respiratory chain that enables the prokaryote to live under a variety of environmental conditions, from highly aerobic to completely anaerobic. In general, the bacterial respiratory chain is composed of dehydrogenases, a quinone pool, and reductases. Substrate-specific dehydrogenases transfer reducing equivalents from various donor substrates (NADH, succinate, glycerophosphate, formate, hydrogen, pyruvate, and lactate) to a quinone pool (menaquinone, ubiquinone, and dimethylmenoquinone). Then electrons from reduced quinones (quinols) are transferred by terminal reductases to different electron acceptors. Under aerobic growth conditions, the terminal electron acceptor is molecular oxygen. A transfer of electrons from quinol to O is served by two major oxidoreductases (oxidases), cytochrome encoded by and cytochrome encoded by . Terminal oxidases of aerobic respiratory chains of bacteria, which use O as the final electron acceptor, can oxidize one of two alternative electron donors, either cytochrome or quinol. This review compares the effects of different inhibitors on the respiratory activities of cytochrome and cytochrome in . It also presents a discussion on the genetics and the prosthetic groups of cytochrome and cytochrome . The membrane contains three types of quinones that all have an octaprenyl side chain (C). It has been proposed that the oxidase can have two ubiquinone-binding sites with different affinities.

: The revised article comprises additional information about subunit composition of cytochrome and its role in bacterial resistance to nitrosative and oxidative stresses. Also, we present the novel data on the electrogenic function of -encoded cytochrome -II, a second -type oxidase that had been thought not to contribute to generation of a proton motive force in , although its spectral properties closely resemble those of -encoded cytochrome .

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Figures

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Figure 1

The two NADH-quinone oxidoreductases called NDH-I and NDH-II and succinate-quinone oxidoreductase (SQR) transfer reducing equivalents to ubiquinone-8 (UQ-8) to yield reduced UQ-8, ubiquinol-8. Three quinol-oxygen oxidoreductases, cytochrome (CyoABCD), cytochrome (CydABX), and cytochrome -II (AppBCX), oxidize ubiquinol-8 and reduce O to 2HO. CydABX and possibly AppBCX oxidize menaquinol-8. NDH-I, CyoABCD, CydABX, and AppBCX are coupled (Δ generators); NDH-II and SQR are uncoupled (no Δ generation). The energetic efficiency of each enzyme is indicated as the number of protons delivered to the periplasmic side of the membrane per electron (H/ ratio). doi:10.1128/ecosalplus.ESP-0012-2015.f1

Citation: Borisov V, Verkhovsky M. 2015. Oxygen as Acceptor, EcoSal Plus 2015; doi:10.1128/ecosalplus.ESP-0012-2015
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Figure 2

Structures of ubiquinone-8, the reduced ubiquinone-8 (ubiquinol-8), menaquinone-8, and the reduced menaquinone-8 (menaquinol-8). doi:10.1128/ecosalplus.ESP-0012-2015.f2

Citation: Borisov V, Verkhovsky M. 2015. Oxygen as Acceptor, EcoSal Plus 2015; doi:10.1128/ecosalplus.ESP-0012-2015
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Figure 3

Structures of heme (protoheme IX), heme , and heme (chlorin), which are redox cofactors of cytochrome and/or cytochrome from . doi:10.1128/ecosalplus.ESP-0012-2015.f3

Citation: Borisov V, Verkhovsky M. 2015. Oxygen as Acceptor, EcoSal Plus 2015; doi:10.1128/ecosalplus.ESP-0012-2015
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Figure 4

Only two main subunits are shown: subunit I in gray and subunit II in yellow. Hemes are shown in red (heme on the right and heme on the left). The cyan sphere near heme represents the Cu center. The amino acid residues of possible proton-conducting pathways, the D (red-tag) and K (blue-tag) channels, in subunit I are shown. The most likely position of the membrane is depicted by the gray background. doi:10.1128/ecosalplus.ESP-0012-2015.f4

Citation: Borisov V, Verkhovsky M. 2015. Oxygen as Acceptor, EcoSal Plus 2015; doi:10.1128/ecosalplus.ESP-0012-2015
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Figure 5

The axial ligands of heme (H19) and heme (H186 and M393) in the CydA subunit are shown in purple and red, respectively. The protein sequence data have been taken from information available at http://genolist.pasteur.fr/Colibri/. The alignment has been made by using the TOPO2 program available at http://www.sacs.ucsf.edu/TOPO2. The model is very similar to that reported in reference 27 . doi:10.1128/ecosalplus.ESP-0012-2015.f5

Citation: Borisov V, Verkhovsky M. 2015. Oxygen as Acceptor, EcoSal Plus 2015; doi:10.1128/ecosalplus.ESP-0012-2015
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Figure 6

There are two protonatable groups, X and X, redox coupled to the heme -heme active site. A highly conserved residue, E445, was proposed to be either the X group or the gateway in a channel that connects X with the cytoplasm or the periplasm ( 52 ). A strictly conserved E107 residue is a part of the channel mediating proton transfer to X from the cytoplasm ( 54 ). X, a group at the periplasmic side of the membrane that picks up and releases a proton as heme , is reduced and oxidized. doi:10.1128/ecosalplus.ESP-0012-2015.f6

Citation: Borisov V, Verkhovsky M. 2015. Oxygen as Acceptor, EcoSal Plus 2015; doi:10.1128/ecosalplus.ESP-0012-2015
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Figure 7

The three rhombuses represent hemes , , and , respectively. The minus signs and red backgrounds in the rhombuses denote that the heme is in the ferrous state. R-CO, R, A, P, F, O are fully ferrous CO bound, fully ferrous unligated, fully ferrous O bound, peroxy, oxoferryl, and fully ferric species, respectively. Transient peroxy species (P) discovered by Belevich et al. ( 53 ) is shown as a true peroxy complex of ferric heme . It is possible, however, that P is an oxoferryl form with a π-cation radical on the porphyrin ring of heme ( 285 , 286 ). doi:10.1128/ecosalplus.ESP-0012-2015.f7

Citation: Borisov V, Verkhovsky M. 2015. Oxygen as Acceptor, EcoSal Plus 2015; doi:10.1128/ecosalplus.ESP-0012-2015
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Tables

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Table 1

Properties of cytochrome and cytochrome in

Citation: Borisov V, Verkhovsky M. 2015. Oxygen as Acceptor, EcoSal Plus 2015; doi:10.1128/ecosalplus.ESP-0012-2015
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Table 2

Effects of inhibitors on quinol oxidase activities of cytochrome and cytochrome in

Citation: Borisov V, Verkhovsky M. 2015. Oxygen as Acceptor, EcoSal Plus 2015; doi:10.1128/ecosalplus.ESP-0012-2015
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Table 3

Extinction coefficients used for determination of the cytochrome concentration

Citation: Borisov V, Verkhovsky M. 2015. Oxygen as Acceptor, EcoSal Plus 2015; doi:10.1128/ecosalplus.ESP-0012-2015
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Table 4

Kinetic and thermodynamic parameters for the reaction of cytochrome with O, CO, and NO at room temperature

Citation: Borisov V, Verkhovsky M. 2015. Oxygen as Acceptor, EcoSal Plus 2015; doi:10.1128/ecosalplus.ESP-0012-2015

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