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The semiquinone swing in the bifurcating electron transferring flavoprotein/butyryl-CoA dehydrogenase complex from Clostridium difficile.

Demmer JK, Pal Chowdhury N, Selmer T, Ermler U, Buckel W
Nat Commun 8 1577 (2017)
Cited: 48 times
EuropePMC logo PMID: 29146947

Abstract

The electron transferring flavoprotein/butyryl-CoA dehydrogenase (EtfAB/Bcd) catalyzes the reduction of one crotonyl-CoA and two ferredoxins by two NADH within a flavin-based electron-bifurcating process. Here we report on the X-ray structure of the Clostridium difficile (EtfAB/Bcd)4 complex in the dehydrogenase-conducting D-state, α-FAD (bound to domain II of EtfA) and δ-FAD (bound to Bcd) being 8 Å apart. Superimposing Acidaminococcus fermentans EtfAB onto C. difficile EtfAB/Bcd reveals a rotation of domain II of nearly 80°. Further rotation by 10° brings EtfAB into the bifurcating B-state, α-FAD and β-FAD (bound to EtfB) being 14 Å apart. This dual binding mode of domain II, substantiated by mutational studies, resembles findings in non-bifurcating EtfAB/acyl-CoA dehydrogenase complexes. In our proposed mechanism, NADH reduces β-FAD, which bifurcates. One electron goes to ferredoxin and one to α-FAD, which swings over to reduce δ-FAD to the semiquinone. Repetition affords a second reduced ferredoxin and δ-FADH-, which reduces crotonyl-CoA.

Articles - 5ol2 mentioned but not cited (6)

  1. The semiquinone swing in the bifurcating electron transferring flavoprotein/butyryl-CoA dehydrogenase complex from Clostridium difficile. Demmer JK, Pal Chowdhury N, Selmer T, Ermler U, Buckel W. Nat Commun 8 1577 (2017)
  2. Structure-based electron-confurcation mechanism of the Ldh-EtfAB complex. Kayastha K, Katsyv A, Himmrich C, Welsch S, Schuller JM, Ermler U, Müller V. Elife 11 e77095 (2022)
  3. Spectral deconvolution of redox species in the crotonyl-CoA-dependent NADH:ferredoxin oxidoreductase from Megasphaera elsdenii. A flavin-dependent bifurcating enzyme. Vigil W, Niks D, Franz-Badur S, Chowdhury N, Buckel W, Hille R. Arch Biochem Biophys 701 108793 (2021)
  4. The reductive half-reaction of two bifurcating electron-transferring flavoproteins: Evidence for changes in flavin reduction potentials mediated by specific conformational changes. Vigil W, Tran J, Niks D, Schut GJ, Ge X, Adams MWW, Hille R. J Biol Chem 298 101927 (2022)
  5. Characterization of the Membrane-Associated Electron-Bifurcating Flavoenzyme EtfABCX from the Hyperthermophilic Bacterium Thermotoga maritima. Ge X, Schut GJ, Tran J, Poole Ii FL, Niks D, Menjivar K, Hille R, Adams MWW. Biochemistry 62 3554-3567 (2023)
  6. Rapid-reaction kinetics of the butyryl-CoA dehydrogenase component of the electron-bifurcating crotonyl-CoA-dependent NADH:ferredoxin oxidoreductase from Megasphaera elsdenii. Vigil W, Nguyen D, Niks D, Hille R. J Biol Chem 299 104853 (2023)


Reviews citing this publication (10)

  1. Flavin-Based Electron Bifurcation, Ferredoxin, Flavodoxin, and Anaerobic Respiration With Protons (Ech) or NAD+ (Rnf) as Electron Acceptors: A Historical Review. Buckel W, Thauer RK. Front Microbiol 9 401 (2018)
  2. Electron Bifurcation: A Long-Hidden Energy-Coupling Mechanism. Müller V, Chowdhury NP, Basen M. Annu Rev Microbiol 72 331-353 (2018)
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  6. Distribution, Evolution, Catalytic Mechanism, and Physiological Functions of the Flavin-Based Electron-Bifurcating NADH-Dependent Reduced Ferredoxin: NADP+ Oxidoreductase. Liang J, Huang H, Wang S. Front Microbiol 10 373 (2019)
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  2. Metatranscriptomic and Thermodynamic Insights into Medium-Chain Fatty Acid Production Using an Anaerobic Microbiome. Scarborough MJ, Lawson CE, Hamilton JJ, Donohue TJ, Noguera DR. mSystems 3 e00221-18 (2018)
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  5. Letter Molecular basis of the flavin-based electron-bifurcating caffeyl-CoA reductase reaction. Demmer JK, Bertsch J, Öppinger C, Wohlers H, Kayastha K, Demmer U, Ermler U, Müller V. FEBS Lett 592 332-342 (2018)
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  9. Universal free-energy landscape produces efficient and reversible electron bifurcation. Yuly JL, Zhang P, Lubner CE, Peters JW, Beratan DN. Proc Natl Acad Sci U S A 117 21045-21051 (2020)
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  12. Cryoelectron microscopy structure and mechanism of the membrane-associated electron-bifurcating flavoprotein Fix/EtfABCX. Feng X, Schut GJ, Lipscomb GL, Li H, Adams MWW, Adams MWW. Proc Natl Acad Sci U S A 118 e2016978118 (2021)
  13. Structure and electron transfer pathways of an electron-bifurcating NiFe-hydrogenase. Feng X, Schut GJ, Haja DK, Adams MWW, Li H. Sci Adv 8 eabm7546 (2022)
  14. Dynamics and Complexity of Dark Fermentation Microbial Communities Producing Hydrogen From Sugar Beet Molasses in Continuously Operating Packed Bed Reactors. Detman A, Laubitz D, Chojnacka A, Wiktorowska-Sowa E, Piotrowski J, Salamon A, Kaźmierczak W, Błaszczyk MK, Barberan A, Chen Y, Łupikasza E, Yang F, Sikora A. Front Microbiol 11 612344 (2020)
  15. Purification and structural characterization of the Na+-translocating ferredoxin: NAD+ reductase (Rnf) complex of Clostridium tetanomorphum. Vitt S, Prinz S, Eisinger M, Ermler U, Buckel W. Nat Commun 13 6315 (2022)
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  19. Molecular and Low-Resolution Structural Characterization of the Na+-Translocating Glutaconyl-CoA Decarboxylase From Clostridium symbiosum. Vitt S, Prinz S, Hellwig N, Morgner N, Ermler U, Buckel W. Front Microbiol 11 480 (2020)
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  24. Correlating Conformational Equilibria with Catalysis in the Electron Bifurcating EtfABCX of Thermotoga maritima. Murray DT, Ge X, Schut GJ, Rosenberg DJ, Hammel M, Bierma JC, Hille R, Adams MWW, Hura GL. Biochemistry 63 128-140 (2024)
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