ATP-driven succinate oxidation in the catabolism of Desulfuromonas acetoxidans

Paulsen, Jens; Kröger, Achim; Thauer, Rudolf K.

doi:10.1007/bf00454960

Cited by 58 publications

(43 citation statements)

References 12 publications

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“…The oxidation of the fatty acids occurs via a modified citric-acid cycle or the methylmalonyl-CoA pathway and involves the function of Sdh using MK as an electron acceptor. Succinate oxidation with S is strongly endergonic (succinate ϩ S → fumarate ϩ H 2S ; ∆G′ 0.1 ϭ ϩ47 kJ/mol S) and was the first endergonic catabolic reaction clearly shown to depend on reversed electron transport [26,31]. It was suggested that the endergonic reaction from menaquinol to S (S/HS Ϫ ; E°′ ϭ Ϫ260 mV) requires reversed electron transport for function [26,27].…”

Section: Discussionmentioning

confidence: 99%

Menaquinone‐dependent succinate dehydrogenase of bacteria catalyzes reversed electron transport driven by the proton potential

Schirawski

Unden

1998

European Journal of Biochemistry

114

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Succinate dehydrogenases from bacteria and archaea using menaquinone (MK) as an electron acceptor (succinate/menaquinone oxidoreductases) contain, or are predicted to contain, two heme-B groups in the membrane-anchoring protein(s), located close to opposite sides of the membrane. All succinate/ubiquinone oxidoreductases, however, contain only one heme-B molecule. In Bacillus subtilis and other bacteria that use MK as the respiratory quinone, the succinate oxidase activity (succinate→O 2 ), and the succinate/ menaquinone oxidoreductase activity were specifically inhibited by uncoupler (CCCP, carbonyl cyanide m-chlorophenylhydrazone) or by agents dissipating the membrane potential (valinomycin). Other parts of the respiratory chains were not affected by the agents. Succinate oxidase or succinate/ubiquinone oxidoreductase from bacteria using ubiquinone as an acceptor were not inhibited. We propose that the endergonic electron transport from succinate (E°′ ϭ ϩ30 mV) to MK (E°′ Х Ϫ80 mV) in succinate/menaquinone oxidoreductase includes a reversed electron transport across the cytoplasmic membrane from the inner (negative) to the outer (positive) side via the two heme-B groups. The reversed electron transport is driven by the proton or electrical potential, which provides the driving force for MK reduction.

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Section: Discussionmentioning

confidence: 99%

Menaquinone‐dependent succinate dehydrogenase of bacteria catalyzes reversed electron transport driven by the proton potential

Schirawski

Unden

1998

European Journal of Biochemistry

114

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“…With the exception of the terminal electron acceptor all other reactants are given in the reduced form. Numbers in brackets: E" in mV; X, unidentified electron carrier, probably a cytochrome [49,761 bound succinate : menaquinone oxidoreductase and a NADdependent malate dehydrogenase. The average redox potential of the electron acceptors is -279 mV (NADP, -324 mV; ferredoxin, -400 mV [24]; menaquinone, -74 mV; and NAD, -320 mV) which is only 13 mV more positive than the E" = -291 mV of the 2 C02/acetate couple.…”

Section: Acetate Oxidation To C 0 2 In Desulfuromonas Acetoxidans : Imentioning

confidence: 99%

“…acetoxiduns contains, membrane-bound, a reduced ferredoxin dehydrogenase, an NADH dehydrogenase, a succinate: menaquinone oxidoreductase, a sulfur reductase, and a proton-translocating ATPase [49]. The membrane fraction catalyzes the reduction of sulfur with ferredoxin and NADH, of fumarate with NADH and H2S, and an ATP-dependent reduction of sulfur and of NAD with succinate.…”

Section: H2smentioning

confidence: 99%

“…The observation that the membrane fraction catalyzes an ATP-dependent reduction of So with succinate was the clue to how endergonic succinate oxidation (E" = + 32 mV) with S" (E" = -240 mV) in D. acetoxidans proceeds. It was found [49] that the reaction was inhibited by the H + -translocating ATPase inhibitor dicyclohexylcarbodiimide and by protonophores indicating that So reduction with succinate is driven by the electrochemical proton potential LIP,,+, probably 2 protons ( A 2/3 mol ATP) being consumed per 2 electrons pushed uphill from menaquinone (E"' = -74 mV) to So. Thus reversed-electron transport is the trick which makes the operation of the citric-acid cycle in D. acetoxiduns possible [80].…”

Section: H2smentioning

confidence: 99%

“…It was, therefore, not considered very likely that in these organisms the citricacid cycle operates as pathway of terminal respiration [24]. Surprisingly, the first two anaerobic bacteria analyzed in this respect, Desulfobacter postgatei [41-471 and Desulfuromonas acetoxidans (48,491, were found to use the cycle, each with a different trick to overcome the redox potential difference between the terminal electron acceptor and succinate [45,49]. However, all the other anaerobes investigated to date turned out to degrade acetate by an alternative pathway [50, 511 (Schauder, R. and Fuchs, G., unpublished results).…”

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Citric‐acid cycle, 50 years on

Thauer

1988

European Journal of Biochemistry

Self Cite

158

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Many anaerobic bacteria can completely oxidize organic matter to C 0 2 with either sulfur, sulfate, or protons as electron acceptor. The sulfur-reducing bacteria and one genus of sulfate reducers use a modified citric-acid cycle with a novel anaplerotic sequence as pathway of terminal respiration. All other anaerobes use an alternative pathway, in which carbon monoxide dehydrogenase is a key enzyme and in which acetyl-CoA is cleaved into two C1 units at the oxidation level of CH30H and CO. Thus almost 50 years after the discovery of the citric acid cycle by Hans Krebs in 1937, a second pathway for acetyl-CoA oxidation was found.1987 marked the 50th anniversary of the discovery of the citric acid cycle. In 1937 Hans Krebs summarized the evidence for a cyclic sequence of reactions that explained the complete oxidation, by pigeon breast muscle, of an unidentified 'triose' derived from glycolysis. The paper was entitled " [11][12][13][14], and intracellular organization [15, 161. The book contains excellent up-to-date treatises of these topics which therefore will not be dealt within the following review.Until recently it was believed that the citric acid cycle operates only in aerobic organisms in a few denitrifiers (reduce NO, to N,) [20, 211, and in some phototrophic purple non-sulfur bacteria [22, 231. Under anaerobic conditions all other known chemotrophic organisms, in pure culture, were incapable of complete oxidation of organic matter. And there was also a theory to explain this observation: the oxidation of succinate to fumarate in the citric-acid cycle requires a terminal electron acceptor with a redox potential (E"') more positive than that of the fumarate/ succinate couple (+32 mV). Only O2 ( 0 2 / H 2 0 : E" = f 8 1 8 mV), NO; (NO;/NO;: E"' = +433 mV) and NO; (NO;/N2: E"' = +970 mV), rather than the electron acceptors used by anaerobes, appeared to meet these conditions The above consideration ignored that there was, in the literature, evidence for a mineralization of organic matter in anaerobic biotopes. Hoppe-Seyler, already in 1886, described the complete oxidation of cellulose in anaerobic sediments supplemented with CaSO,. The reducing equivalents were quantitatively recovered as H2S [25]. Later Jerrgensen Martens and Berner [30], and Winfrey and Zeikus [31] reported that in marine sediments carbohydrates, proteins, and fatty acids were mineralized in the absence of O2 and that sulfate, elemental sulfur, and thiosulfate [29] were the major electron acceptors used. Sterilized sediments did not mediate the conversion. It was, therefore, evident that an anaerobic pathway of terminal respiration must exist.Pfennig and collaborators were then the first to isolate one of these organisms. In 1976 Pfennig and Biebl [32] described ~4 1 .

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