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

Schirawski, Jan; Unden, Gottfried

doi:10.1046/j.1432-1327.1998.2570210.x

Cited by 115 publications

(107 citation statements)

References 23 publications

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“…Other reports (24,39,42) tion of terminal oxidase activity, which in turn inhibits Pho induction, then deletion of a gene responsible for the production of an Na ϩ /H ϩ antiporter should improve respiration, leading to increased activity of the terminal oxidases causing hyperinduction of Pho induction, as was reported in the nhaC deletion strain.…”

Section: Discussionmentioning

confidence: 86%

Terminal Oxidases Are Essential To Bypass the Requirement for ResD for Full Pho Induction in Bacillus subtilis

2004

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The Bacillus subtilis Pho signal transduction network, which regulates the cellular response to phosphate starvation, integrates the activity of three signal transduction systems to regulate the level of the Pho response. This signal transduction network includes a positive feedback loop between the PhoP/PhoR and ResD/ResE two-component systems. Within this network, ResD is responsible for 80% of the Pho response. To date, the role of ResD in the generation of the Pho response has not been understood. Expression of two terminal oxidases requires ResD function, and expression of at least one terminal oxidase is needed for the wild-type Pho response. Previously, our investigators have shown that strains bearing mutations in resD are impaired for growth and acquire secondary mutations which compensate for the loss of the a-type terminal oxidases by allowing production of cytochrome bd. We report here that the expression of cytochrome bd in a ⌬resDE background is sufficient to compensate for the loss of ResD for full Pho induction. A ctaA mutant strain, deficient in the production of heme A, has the same Pho induction phenotype as a ⌬resDE strain. This demonstrates that the production of a-type terminal oxidases is the basis for the role of ResD in Pho induction. Terminal oxidases affect the redox state of the quinone pool. Reduced quinones inhibit PhoR autophosphorylation in vitro, consistent with a requirement for terminal oxidases for full Pho induction in vivo.The Bacillus subtilis phosphate starvation response (Pho response) is under the control of a complex regulatory network that allows the cell to respond to the level of inorganic phosphate (P i ) in the environment. This system is critical to survival because phosphate is the limiting nutrient in soil (33), the natural environment for B. subtilis.Central to the B. subtilis Pho response is the PhoP/PhoR two-component signal transduction system. The phoPR operon (23, 43) is subject to activation by PhoP under phosphate starvation conditions (34). PhoP/PhoR directly regulates the expression of genes involved in the cellular response to phosphate starvation. The histidine kinase, PhoR, is autophosphorylated in response to an environmental signal and then phosphorylates its cognate response regulator, PhoP. PhoPϳP activates the transcription of the alkaline phosphatases (19), phoA (formerly phoAIV) (20), and phoB (formerly phoAIII) (7); phosphodiesterases, phoD (11), and glpQ (1); a high-affinity phosphate transport system, pstS (37); teichuronic acid synthetic genes (teichuronic acid is a cell wall polymer lacking phosphate), tuaABCDEFGH (27, 46); and a gene encoding a 60-residue peptide of unknown function, ykoL (38). PhoPϳP has been shown to repress the expression of the tagAB and tagDEF genes responsible for the production of teichoic acid (a cell wall polymer containing phosphate) (26). The collective action of these products allows the cell to scavenge extracellular phosphate and to release additional P i from the cell wall.The regulation of the Pho respon...

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Section: Discussionmentioning

confidence: 86%

Terminal Oxidases Are Essential To Bypass the Requirement for ResD for Full Pho Induction in Bacillus subtilis

2004

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“…In B. subtilis, the succinate dehydrogenase is orthologous to FrdCAB from G. sulfurreducens, and the membrane-bound electron carrier is also menaquinone (9). Dissipation of the membrane potential has been proposed to drive succinate oxidation in B. subtilis (34,35). In G. sulfurreducens, a succinate dehydrogenase that dissipates the membrane potential could explain the increases in cell yield and growth rate seen when the succinate dehydrogenase is bypassed (Fig.…”

Section: Resultsmentioning

confidence: 99%

Genetic Characterization of a Single Bifunctional Enzyme for Fumarate Reduction and Succinate Oxidation in Geobacter sulfurreducens and Engineering of Fumarate Reduction in Geobacter metallireducens

et al. 2006

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The mechanism of fumarate reduction in Geobacter sulfurreducens was investigated. The genome contained genes encoding a heterotrimeric fumarate reductase, FrdCAB, with homology to the fumarate reductase of Wolinella succinogenes and the succinate dehydrogenase of Bacillus subtilis. Mutation of the putative catalytic subunit of the enzyme resulted in a strain that lacked fumarate reductase activity and was unable to grow with fumarate as the terminal electron acceptor. The mutant strain also lacked succinate dehydrogenase activity and did not grow with acetate as the electron donor and Fe(III) as the electron acceptor. The mutant strain could grow with acetate as the electron donor and Fe(III) as the electron acceptor if fumarate was provided to alleviate the need for succinate dehydrogenase activity in the tricarboxylic acid cycle. The growth rate of the mutant strain under these conditions was faster and the cell yields were higher than for wild type grown under conditions requiring succinate dehydrogenase activity, suggesting that the succinate dehydrogenase reaction consumes energy. An orthologous frdCAB operon was present in Geobacter metallireducens, which cannot grow with fumarate as the terminal electron acceptor. When a putative dicarboxylic acid transporter from G. sulfurreducens was expressed in G. metallireducens, growth with fumarate as the sole electron acceptor was possible. These results demonstrate that, unlike previously described organisms, G. sulfurreducens and possibly G. metallireducens use the same enzyme for both fumarate reduction and succinate oxidation in vivo.

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“…As illustrated in Fig. 4c, this enzyme used the transmembrane ⌬p to drive the succinate oxidation by menaquinone, an endergonic reaction under standard conditions, in a manner similar to that proposed for the SQR of Gram-positive positive bacteria, e.g., Bacillus subtilis (37,38), and very different from that of mitochondrial complex II, which reduces ubiquinone (Fig. 4d).…”

Section: Discussionmentioning

confidence: 95%

Experimental support for the “E pathway hypothesis” of coupled transmembrane e ^– and H ⁺ transfer in dihemic quinol:fumarate reductase

Lancaster

Sauer

Groß

et al. 2005

Proc. Natl. Acad. Sci. U.S.A.

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Reconciliation of apparently contradictory experimental results obtained on the quinol:fumarate reductase, a diheme-containing respiratory membrane protein complex from Wolinella succinogenes, was previously obtained by the proposal of the so-called ''E pathway hypothesis.'' According to this hypothesis, transmembrane electron transfer via the heme groups is strictly coupled to cotransfer of protons via a transiently established pathway thought to contain the side chain of residue Glu-C180 as the most prominent component. Here we demonstrate that, after replacement of Glu-C180 with Gln or Ile by site-directed mutagenesis, the resulting mutants are unable to grow on fumarate, and the membrane-bound variant enzymes lack quinol oxidation activity. Upon solubilization, however, the purified enzymes display Ϸ1͞10 of the specific quinol oxidation activity of the wild-type enzyme and unchanged quinol Michaelis constants, K m. The refined x-ray crystal structures at 2.19 Å and 2.76 Å resolution, respectively, rule out major structural changes to account for these experimental observations. Changes in the oxidation-reduction heme midpoint potential allow the conclusion that deprotonation of Glu-C180 in the wild-type enzyme facilitates the reoxidation of the reduced high-potential heme. Comparison of solvent isotope effects indicates that a rate-limiting proton transfer step in the wild-type enzyme is lost in the Glu-C180 3 Gln variant. The results provide experimental evidence for the validity of the E pathway hypothesis and for a crucial functional role of Glu-C180.anaerobic respiration ͉ atomic model ͉ bioenergetics ͉ membrane protein ͉ succinate:quinone oxidoreductase A ccording to Peter Mitchell's chemiosmotic theory (1), the energy released upon the oxidation of electron donor substrates in both aerobic and anaerobic respiration is transiently stored in the form of an electrochemical proton potential (⌬p) across the energy-transducing membranes, which can then be used by the ATP synthase for ADP phosphorylation with inorganic phosphate. Fundamentally, there are two mechanisms by which integral membrane proteins can act as catalysts in this coupling of electron transfer reactions to the generation of a transmembrane ⌬p: the redox loop mechanism and the proton pump mechanism (2). The redox loop mechanism essentially involves transmembrane electron transfer. Reduction reactions on one side of the energytransducing membrane are associated with proton binding, whereas oxidation reactions on the opposite side of the membrane are associated with proton release. In a simple form, this mechanism is represented by the formate dehydrogenase (3) and membranebound nitrate reductase (4) enzymes of anaerobic respiration and, in a more complicated form, by the Q-cycle of the cytochrome bc 1

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

Cited by 115 publications

References 23 publications

Terminal Oxidases Are Essential To Bypass the Requirement for ResD for Full Pho Induction in Bacillus subtilis

Terminal Oxidases Are Essential To Bypass the Requirement for ResD for Full Pho Induction in Bacillus subtilis

Genetic Characterization of a Single Bifunctional Enzyme for Fumarate Reduction and Succinate Oxidation in Geobacter sulfurreducens and Engineering of Fumarate Reduction in Geobacter metallireducens

Experimental support for the “E pathway hypothesis” of coupled transmembrane e ^– and H ⁺ transfer in dihemic quinol:fumarate reductase

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

Cited by 115 publications

References 23 publications

Terminal Oxidases Are Essential To Bypass the Requirement for ResD for Full Pho Induction in Bacillus subtilis

Terminal Oxidases Are Essential To Bypass the Requirement for ResD for Full Pho Induction in Bacillus subtilis

Genetic Characterization of a Single Bifunctional Enzyme for Fumarate Reduction and Succinate Oxidation in Geobacter sulfurreducens and Engineering of Fumarate Reduction in Geobacter metallireducens

Experimental support for the “E pathway hypothesis” of coupled transmembrane e – and H + transfer in dihemic quinol:fumarate reductase

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Experimental support for the “E pathway hypothesis” of coupled transmembrane e ^– and H ⁺ transfer in dihemic quinol:fumarate reductase