Skip to main content
Log in

Kinetics of Electron Transfer within Cytochrome bc 1 and Between Cytochrome bc 1 and Cytochrome c

  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

In this minireview an overview is presented of the kinetics of electron transfer within the cytochrome bc 1 complex, as well as from cytochrome bc 1 to cytochrome c. The cytochrome bc 1 complex (ubiquinone:cytochrome c oxidoreductase) is an integral membrane protein found in the mitochondrial respiratory chain as well as the electron transfer chains of many respiratory and photosynthetic bacteria. Experiments on both mitochondrial and bacterial cyatochrome bc 1 have provided detailed kinetic information supporting a Q-cycle mechanism for electron transfer within the complex. On the basis of X-ray crystallographic studies of cytochrome bc 1, it has been proposed that the Rieske iron–sulfur protein undergoes large conformational changes as it transports electrons from ubiquinol to cytochrome c 1. A new method was developed to study electron transfer within cytochrome bc 1 using a binuclear ruthenium complex to rapidly photooxidize cytochrome c 1. The rate constant for electron transfer from the iron–sulfur center to cytochrome c 1 was found to be 80,000 s−1, and is controlled by the dynamics of conformational changes in the iron–sulfur protein. Moreover, a linkage between the conformation of the ubiquinol binding site and the conformational dynamics of the iron–sulfur protein has been discovered which could play a role in the bifurcated oxidation of ubiquinol. A ruthenium photoexcitation method has also been developed to measure electron transfer from cytochrome c 1 to cytochrome c. The kinetics of electron transfer are interpreted in light of a new X-ray crystal structure for the complex between cytochrome bc 1 and cytochrome c.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Ahmed AJ, Smith HT, Smith MB and Millett F (1978) Effect of speci c lysine modi cation on the reduction of cytochrome c by succinate–cytochrome c reductase. Biochemistry 17: 2479–2483

    Article  PubMed  CAS  Google Scholar 

  • Axelrod HL, Abresch EC, Okamura MY, Yey AP, Rees DC and Feher G (2002) X-ray structure determination of the cytochrome c 2: reaction center electron transfer complex from Rhodobacter sphaeroides. J Mol Biol 319: 501–515

    Article  PubMed  CAS  Google Scholar 

  • Bartoschek S, Johansson M, Geierstanger BH, Okun JG, Lancaster CR, Humpfer E, Yu L, Yu CA, Griesinger C and Brandt U (2001) Three molecules of ubiquinone bind speci cally to mitochondrial cytochrome bc 1 complex. J Biol Chem 276: 35231–35234

    Article  PubMed  CAS  Google Scholar 

  • Beratan DN, Betts JN and Onuchic JN (1991) Protein electron transfer rates set by the bridging secondary and tertiary structure. Science 252: 1285–1288

    PubMed  CAS  Google Scholar 

  • Bowyer JR and Crofts AR (1981) Inhitibion of electron transport in R. capsulatus by a ubiquinone analogue. In: Dutton PL, Leigh J and Scarpa A (eds) Frontiers of Biological Energetics, Vol I, pp 326–333. Academic Press, New York

    Google Scholar 

  • Bowyer JR and Trumpower BL (1981) Pathways of electron transfer in the cytochrome bc 1 complexes of mitochondria and photosynthetic bacteria. In: Skulachev BP and Hinkle PC (eds) Chemiosmotic Proton Circuits in Biologial membranes, pp 105–122. Addison-Wesley, Reading, Massachusetts

    Google Scholar 

  • Brandt U (1996) Energy conservation by bifurcated electron-transfer in the cytochrome bc 1 complex. Biochim Biophys Acta 1275: 41–46

    Article  PubMed  Google Scholar 

  • Brandt U (1998) The chemistry and mechanics of ubihydro-quinone oxidation at center P (Qo )of the cytochrome bc 1 complex. Biochim Biophys Acta 1365: 261–268

    Article  PubMed  CAS  Google Scholar 

  • Broger C, Salardi S and Azzi A (1983) Interaction between isolated cytochrome c 1 and cytochrome c. Eur J Biochem 131: 349–352

    Article  PubMed  CAS  Google Scholar 

  • Brugna M, Rodgers S, Schricker A, Montoya G, Kazmeier M, Nitschike W and Sinning I (2000) A spectroscopic method for observing the domain movement of the Rieske iron–sulfur protein. Proc Natl Acad Sci USA 97: 2069–2074

    Article  PubMed  CAS  Google Scholar 

  • Crofts AR and Meinhardt SW (1982) A Q-cycle mechanism for the cyclic electron transfer chain of Rp. sphaeroides. Biochem Soc Trans 10: 210–203

    Google Scholar 

  • Crofts AR and Wang Z (1989) How rapid are the internal reactions of the ubiquinol: cytochrome c 2 oxidoreductase? Photosynth Res 22: 69–87

    Article  CAS  Google Scholar 

  • Crofts AR, Guergova-Kuras M, Huang L, Kuras R, Zhang Z and Berry EA (1999) Mechanism of ubiquinol oxidation by the bc 1 complex: role of the iron–sulfur protein and its mobility. Biochemistry 38: 15791–15806

    Article  PubMed  CAS  Google Scholar 

  • Crofts AR, Guergova-Kuras M, Duras R, Ugulava N, Li J and Hong S (2000) Proton-coupled electron transfer at the Qo site: what type of mechanism can account for the high activation barrier? Biochim Biophys Acta 1459: 456–466

    Article  PubMed  CAS  Google Scholar 

  • Darrouzet E and Daldal F (2002)Movement of the iron–sulfur subunit beyond the ef loop of cytochrome b is required for multiple turnovers of the bc 1 complex but not for a single turnover Qo site catalysis. J Biol Chem 277: 3471–3476

    Article  PubMed  CAS  Google Scholar 

  • Darrouzet E, Valkova-Valchanova M and Daldal R (2000) Probing the role of the Fe–S subunit hinge region during Qo site catalysis in Rhodobacter capsulatus bc 1 complex. Biochemistry 39: 15475–15483

    Article  PubMed  CAS  Google Scholar 

  • Darrouzet E, Valkova-Valchanova M and Daldal F (2002) The [2Fe–2S ]cluster E m as an indicator of the iron–sulfur subunit position in the ubihydroquinone oxidation site of the cytochrome bc 1 complex. J Biol Chem 277: 3464–3470

    Article  PubMed  CAS  Google Scholar 

  • Darrouzet E, Cooley JW and Daldal F (2004) The cytochrome bc 1 complex and its homologue the b 6 f complex: similarities and differences. Photosynth Res 79: 25–44

    Article  PubMed  CAS  Google Scholar 

  • Davidson V (1996) Unraveling the kinetic complexity of interprotein electron transfer reactions. Biochemistry 35: 14035–14039

    Article  PubMed  CAS  Google Scholar 

  • De Vries S, Albracht SPJ, Berden JA and Slater EC (1982) The pathway of electron through QH2 cytochrome c oxidoreductase studied by pre-steady-state kinetics. Biochim Biophys Acta 681: 41–53

    Article  PubMed  CAS  Google Scholar 

  • Ding H, Robertson DE, Daldal F and Dutton PL (1992) Cytochrome bc 1 complex [2Fe–2S ]cluster and its interaction with ubiquinone and ubihydroquinone at the Qo site: a double-occupancy Qo site model. Biochemistry 31: 3144–3158

    Article  PubMed  CAS  Google Scholar 

  • Ding H, Moser CC, Robertson DE, Tokito MK, Daldal F and Dutton PL (1995) Ubiquinone pair in the Qo site central to the primary energy conversion reactions of cytochrome bc 1 complex. Biochemistry 24: 15979–15996

    Article  Google Scholar 

  • Engstrom G, Xiao K, Yu C-A, Yu L, Durham B and Millett F (2002) Photoinduced electron transfer between the Rieske iron–sulfur protein and cytochrome c 1 in the Rhodobacter sphaeroides cytochrome bc 1 complex: effects of pH, temperature, and driving force. J Biol Chem 277: 31072–31078

    Article  PubMed  CAS  Google Scholar 

  • Engstrom G, Rajagukguk R, Saunders AJ, Patel C, Raja-gukguk S, Merbitz-Zahradnik T, Xiao K, Pielak G, Trum-power B, Yu C-A, Gu L, Durham B and Millett F (2003) Design of a ruthenium-labeled cytochrome c derivative to study electron transfer with the cytochrome bc 1 complex. Biochemistry 42: 2816–2824

    Article  PubMed  CAS  Google Scholar 

  • Gao X, Wen X, Yu C-A, Esser L, Tsao S, Quinn B, Zhang L, Yu L and Xia D (2002) The crystal structure of mitochon-drial cytochrome bc 1 in complex with famoxadone: the role of aromatic–aromatic interaction in inhibition. Biochemistry 41: 11692–11702

    Article  PubMed  CAS  Google Scholar 

  • Ghosh M, Wang C, Ebert E, Vadlamuri S and Beattie DS (2001) Substituting leucine for alanine-86 in the tether region of the iron–sulfur protein of the cytochrome bc 1 complex affects the mobility of the [2Fe–2S ]Domain. Biochemistry 40: 327–335

    Article  PubMed  CAS  Google Scholar 

  • Gutweniger HE, Grassi C and Bisson C (1983) Interaction between cytochrome c and ubiquinone–cytochrome c oxido-reductase: a study with water-soluble carbodiimides. Biochem Biophys Res Comm 116: 272–283

    Article  PubMed  CAS  Google Scholar 

  • Hansen KC, Schultz BE, Wang F Chan SI (2000) Reaction of E. coli cytochrome bo 3 and mitochondrial cytochrome bc 1 with a photoreleasable decylubiquinol. Biochim Biophys Acta 1456: 121–137

    Article  PubMed  CAS  Google Scholar 

  • Hong S, Ugulava N, Guergova-Kuras M and Crofts AR (1999) The energy landscape for ubihydroquinone oxidation at the Qo site of the bc 1 complex in Rhodobacter sphaeroides. J Biol Chem 274: 33931–33944

    Article  PubMed  CAS  Google Scholar 

  • Hunte C, Koepke J, Lange C, Rossmanith T and Michel H (2000) Structure at 2. 3 Å resolution of the cytochrome bc 1 complex from the yeast Saccharomyces cerevisiae co crystallized with an antibody Fv fragment. Struct (London) Fold Des 8: 669–684

    Article  CAS  Google Scholar 

  • Hunte C, Solmaz S and Lange C (2002) Electron transfer between yeast cytochrome bc 1 complex and cytochrome c: a structural analysis. Biochim Biophys Acta 1555: 21–28

    Article  PubMed  CAS  Google Scholar 

  • Iwata S, Lee JW, Okada K, Lee JK, Wata M, Rasmussen B, Link TA, Ramaswamy S and Jap BK (1998) Complete structure of the 11-subunit bovine mitochondrial cytochrome bc 1 complex. Science 281: 64–71

    Article  PubMed  CAS  Google Scholar 

  • Jordan DB, Livingston RS, Bisaha JJ, Duncan KE, Pember SO, Picollelli MA, Schwartz RS, Sternberg JA and Tang XS (1999) Oxazolidinediones: a new chemical class of fungicides and inhibitors of mitochondrial cytochrome bc 1 function. Extended summaries: IUPAC Conference. Pestic Sci 55: 197–218

    Article  Google Scholar 

  • Kim H, Xia D, Yu C-A, Xia J-Z, Kachurin AM, Zhang L Yu L and Deisenhofer J (1998) Inhibitor binding changes domain mobility in the iron–sulfur protein of the mitochondrial bc 1 complex from bovine heart. Proc Natl Acad Sci USA 95: 8026–8033

    Article  PubMed  CAS  Google Scholar 

  • King TE, Yu C-A, Yu L and Chiang Y (1975) An examination of the components, sequence, mechanism and their uncertainties involved in mitochondrial electron transport from succinate to cytochrome c. In: Quagliariello E, Papa S, Palmieri F, Slater EC and Sliprandi N (eds) Electron Transfer Chains and Oxidatitve Phosphorylation, pp 105–118. North-Holland Publishing, Amsterdam

    Google Scholar 

  • Konig BW, Oshero. N, Wilms J, Muijsers AO, Dekker HL, and Margoliash E (1980) Mapping of the interaction domain for puri ed cytochrome c 1 on cytochrome c. FEBS Lett 111: 359–398

    Google Scholar 

  • Kurisu G, Zhang H, Smith JL and Cramer WA (2003) Structure of the cytochrome b 6 f complex of oxygenic photosynthesis: tuning the cavity. Science 302: 1009–1014

    Article  PubMed  CAS  Google Scholar 

  • Lange C and Hunte C (2002) Crystal structure of the yeast cytochrome bc 1 complex with its bound substrate cytochrome c. Proc Natl Acad Sci USA 99: 2800–2805

    Article  PubMed  CAS  Google Scholar 

  • Li J, Osyczka A, Conover RC, Johnson MK, Qin H, Daldal F and Knaff DB (2003) Role of acidic and aromatic amino acids in Rb. capsulatus cytochrome c 1. A site-directed mutagenesis study. Biochemistry 42: 8818–8830

    Article  PubMed  CAS  Google Scholar 

  • Link TA (1994) Two p K values of the oxidized Rieske [2Fe–2S ] cluster observed by CD spectroscopy. Biochim Biophys Acta 1185: 81–84

    Article  CAS  Google Scholar 

  • Marcus RA (1956) On the theory of oxidation–reduction reactions involving electron transfer. J Chem Phys 24: 966–978

    Article  CAS  Google Scholar 

  • Meinhardt SW and Crofts AR (1982a) The site and mechanism of action of myxothiazol as an inhibitor of electron transport in Rp. Sphaeroides FEBS Lett 149: 223–227

    Article  CAS  Google Scholar 

  • Meinhardt SW and Crofts AR (1982b) Kinetic and thermodynamic resolution of cytochrome c 1 and cytochrome c 2 from Rhodopseudomonas sphaeroides. FEBS Lett 149: 223–227

    Article  CAS  Google Scholar 

  • Mitchell P (1975) Proton motice redox mechanism of the cytochrome bc 1 complex in the respiratory chain: proton motive ubiquinone cycle. FEBS Lett 56: 1–6

    Article  PubMed  CAS  Google Scholar 

  • Moore GR and Pettigrew GW (1990) Cytochromes c: Evolutionary, Structural and Physicochemical Aspects. Springer-Verlag, New York

    Google Scholar 

  • Moser CC, Keske JM, Warncke K, Farid RS and Dutton PL (1992) Nature of biological electron transfer. Nature 355: 796–802

    Article  PubMed  CAS  Google Scholar 

  • Nett JH, Hunte C and Trumpower BL (2000) Changes to the length of the flexible linker region of the Rieske protein impair the interaction of ubiquinol with the cytochrome bc 1 complex. Eur J Biochem 267: 5777–5782

    Article  PubMed  CAS  Google Scholar 

  • Pelletier H and Kraut J (1992) Crystal structure of a complex between electron transfer partners, cytochrome c peroxidase and cytochrome c. Science 258: 1748–1755

    PubMed  CAS  Google Scholar 

  • Sadoski RC, Engstrom G, Tian H, Zhang L, Yu CA, Y, L, Durham B and Millett F (2000) Use of a photoactivated ruthenium dimer complex to measure electron transfer between the Rieske iron–sulfur protein and cytochrome c 1 in the cytochrome bc 1 complex. Biochemistry 39: 4231–4236

    Article  PubMed  CAS  Google Scholar 

  • Shinkarev VP, Crofts AR and Wraight CA (2001) The electric eld generated by photosynthetic reaction center induces rapid reversed electron transfer in the bc 1 complex. Biochem-istry 40: 12584–12590

    Article  CAS  Google Scholar 

  • Slater EC and De Vries S (1980) Identification of the BAL-labile factor. Nature 288: 717–718

    Article  PubMed  CAS  Google Scholar 

  • Smith HT, Ahmed A and Millett F (1981) Electrostatic interaction of cytochrome c with cytochrome c 1 and cyto-chrome oxidase J Biol Chem 256: 4984–4990

    PubMed  CAS  Google Scholar 

  • Snyder CH, Guierrez-Cirlos EB and Trumpower BL (2000) Evidence for a concerted mechanism of ubiquinol oxidation by the cytochrome bc 1 complex. J Biol Chem 275: 13555–13541

    Article  Google Scholar 

  • Speck SH, Ferguson-Miller S, Oshero. N and Margoliash E (1979) Definition of cytochrome c binding domains by chemical modi cation: kinetics of reaction with beef mitochondrial reductase. Proc Natl Acad Sci USA 76: 155–160

    Article  PubMed  CAS  Google Scholar 

  • Stonehuerner J, OBrien P, Geren L, Millett F, Steidl J, Yu L and Yu C-A (1983) Identification of the binding site on cytochrome c 1 for cytochrome c. J Biol Chem 260: 5392–5398

    Google Scholar 

  • Stroebel D, Choquet Y, Popot JL and Picot D (2003) An atypical heme in the cytochrome b 6 f complex. Nature 426: 413–418

    Article  PubMed  CAS  Google Scholar 

  • Tian H, Yu L, Mather MW and Yu C-A (1998) Flexibility of the neck region of the Rieske iron–sulfur protein is functionally important in the cytochrome bc 1 complex. J Biol Chem 273: 27953–27959

    Article  PubMed  CAS  Google Scholar 

  • Tian H, White S, Yu L and Yu C-A (1999) Evidence for the head domain movement of the Rieske iron–sulfur protein in electron transfer reaction of the cytochrome bc 1 complex. J Biol Chem 274: 7146–7152

    Article  PubMed  CAS  Google Scholar 

  • Tian H, Sadoski R, Zhang L, Yu C-A, Yu L, Durham B and Millett F (2000) Definition of the interaction domain for cytochrome c on the cytochrome bc 1 complex. Steady-state and rapid kinetic analysis of electron transfer between cytochrome c and Rhodobacter sphaeroides cytochrome bc 1 surface mutants. J Biol Chem 275: 9587–9595

    Article  PubMed  CAS  Google Scholar 

  • Trumpower BL (1981) Function of the iron–sulfur protein of the cytochrome bc 1 segment of the respiratory chain. Biochim Biophys Acta 639: 129–155

    PubMed  CAS  Google Scholar 

  • Trumpower BL (1990) The protonmotive Q cycle. Energy transduction by coupling of proton translocation to electron transfer by the cytochrome bc 1 complex. J Biol Chem 265: 11409–11412

    PubMed  CAS  Google Scholar 

  • Trumpower BL (2002) A concerted, alternating sites mechanism of ubiquinol oxidation by the dimeric cytochrome bc 1 complex. Biochim Biophys Acta 1555: 166–173

    Article  PubMed  CAS  Google Scholar 

  • Trumpower BL and Gennis RB (1994) Energy transduction by cytochrome complexes in mitochondrial and bacterial respiration: the enzymology of coupling electron transfer reactions to transmembrane proton translocation. Annu Rev Biochem 63: 675–716

    PubMed  CAS  Google Scholar 

  • T'sai A, Olson JS and Palmer G (1983) The oxidation of yeast complex III: evidence for a very rapid electron equilibrium between cytochrome c 1 and the iron–sulfur center. J Biol Chem 258: 2122–2125

    Google Scholar 

  • Ugulava NB and Crofts AR (1998) CD-monitored redox titration of the Rieske Fe–S protein of Rb. sphaeroides: pH dependence of the midpoint potential in isolated bc 1 complex and in membranes. FEBS Lett 440: 409–413

    Article  PubMed  CAS  Google Scholar 

  • Valkova-Valchanova MB, Saribas AS, Gibney BR, Dutton PL and Daldal F (1998) Isolation and characterization of a two-subunit cytochrome b–c 1 subcomplex from Rhodobacter capsulatus and reconstitution of its ubihydroquinone oxidation (Qo )site with puri ed Fe–S protein subunit. Biochem-istry 37: 16242–16251

    Article  CAS  Google Scholar 

  • Wang K, Mei H, Geren L, Miller MA, Saunders A, Wang X, Waldner JL, Pielak GJ, Durham B and Millett F (1996) Design of a ruthenium cytochrome c derivative to measure electron transfer to the radical cation and the oxyferryl heme in cytochrome c peroxidase. Biochemistry 35: 15107–15119

    Article  PubMed  CAS  Google Scholar 

  • Wang K, Zhen Y, Sadoski R, Grinnell S, Geren L, Ferguson-Miller S, Durham B and Millett F (1999) Definition of the interaction domain for cytochrome c on cytochrome c oxidase: II. Rapid kinetic analysis of electron transfer from cytochrome c to Rhodobacter sphaeroides cytochrome oxidase surface mutants. J Biol Chem 274: 38042–38050

    Article  PubMed  CAS  Google Scholar 

  • Wikstrom MKF and Berden J (1972) Oxidoreduction of cytochrome b in the presence of antimycin. Biochim Biophys Acta 283: 403–420

    Article  PubMed  CAS  Google Scholar 

  • Xia D, Yu C-A, Kim H, Xia J-Z, Kachurin AM, Zhang L Yu L and Desienhofer J (1997) Crystal structure of the cytochrome bc 1 complex from bovine heart mitochondria science 277: 60–66

    CAS  Google Scholar 

  • Xiao K, Engstrom G, Rajagukguk S, Yu C-A, Yu L, Durham B and Millett F (2003) Effect of famoxadone on photo-induced electron transfer between the iron–sulfur center and cytochrome c 1 in the cytochrome bc 1 Complex. J Biol Chem 278: 11419–11426

    Article  PubMed  CAS  Google Scholar 

  • Yu CA, Yu L and King TE (1973) Kinetics of electron transfer between cardiac cytochrome c 1 and c. J Biol Chem 248: 528–533

    PubMed  CAS  Google Scholar 

  • Zhang Z, Huang L, Shulmeister VM, Chi Y-I, Kim KK, Hung L-W, Crofts AR, Berry EA and Kim S-H (1998) Electron transfer by domain movement in cytochrome bc 1 Nature 392: 677–684

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Millett, F., Durham, B. Kinetics of Electron Transfer within Cytochrome bc 1 and Between Cytochrome bc 1 and Cytochrome c . Photosynthesis Research 82, 1–16 (2004). https://doi.org/10.1023/B:PRES.0000040434.77061.ca

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/B:PRES.0000040434.77061.ca

Navigation