Abstract
Ubihydroquinone: cytochrome (cyt)c oxidoreductase, or cyt bc 1, is a widespread, membrane integral enzyme that plays a crucial role during photosynthesis and respiration. It is one of the major contributors of the electrochemical proton gradient, which is subsequently used for ATP synthesis. The simplest form of the cyt bc 1 is found in bacteria, and it contains only the three ubiquitously conserved catalytic subunits: the Fe–S protein, cyt b and cyt c 1. Here we present a preliminary X-ray structure of Rhodobacter capsulatus cyt bc 1 at 3.8 Å and compare it to the available structures of its homologues from mitochondria and chloroplast. Using the bacterial enzyme structure, we highlight the structural similarities and differences that are found among the three catalytic subunits between the members of this family of enzymes. In addition, we discuss the locations of currently known critical mutations, and their implications in terms of the cyt bc 1 catalysis.
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Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W and Lipman DJ (1997) Gapped BLAST and PSIBLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389–3402
Ambler RP (1982) The structure and classification of cytochrome c. In: Kaplan NO and Robinson A (eds) From Cyclotrons to Cytochromes, pp 263–282. Academic Press, New York
Berry EA, Huang LS and DeRose VJ (1991) Ubiquinolcytochrome c oxidoreductase of higher plants. Isolation and characterization of the bc1 complex from potato tuber mitochondria. J Biol Chem 266: 9064–9077
Berry EA, Huang LS, Zhang ZL and Kim SH (1999) Structure of the avian mitochondrial cytochrome bc(1) complex. J Bioenerg Biomemb 31: 177–190
Berry EA, Guergova-Kuras M, Huang LS and Crofts AR (2000) Structure and function of cytochrome bc complexes. Ann Rev of Biochem 69: 1005–1075
Berry EA, Huang LS, Cobessi D, Cromartie TH, Crowley P and Pon NG (2003) Crystallographic studies of inhibitor and substrate binding in the vertebrate cytochrome bc1 complex at up to 2.1 angstrom resoluton. Biophys J 84: 150A–150A
Brasseur G, Saribas AS and Daldal F (1996) A compilation of mutations located in the cytochrome b subunit of the bacterial and mitochondrial bc1 complex. Biochim Biophys Acta 1275: 61–69
Brunger AT (1992) The Free R value: a novel statistical quantity for assessing the accuracy of crystal structures. Nature 355: 472–474
Brunger AT, Adams PD, Clore GM, DeLano WL, Gros P, Grosse-Kunstleve RW, Jiang JS, Kuszewski J, Nilges M, Pannu NS, Read RJ, Rice LM, Simonson T and Warren GL (1998) Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr D Biol Crystallogr 54: 905–921
Carrell CJ, Zhang HM, Cramer WA and Smith JL (1997) Biological identity and diversity in photosynthesis and respiration: structure of the lumen-side domain of the chloroplast Rieske protein. Structure 5: 1613–1625
Collaborative Computational Project (1994) The CCP4 Suite: Programs for Protein Crystallography. Acta Crystallography. D D50: 760–763
Combet C, Blanchet C, Geourjon C and Deleage G (2000)NPS@: network protein sequence analysis. Trends Biochem Sci 25: 147–150
Cooley JW, Roberts AG, Bowman MK, Kramer DM and Daldal F (2004) The raised midpoint potential of the [2Fe2S] cluster of cytochrome bc1 is mediated by both the Qo site occupants and the head domain position of the Fe-S protein subunit. Biochemistry 43: 2217–2227
Cramer WA, Soriano GM, Ponomarev M, Huang D, Zhang H, Martinez SE and Smith JL (1996) Some new structural aspects and old controversies concerning the cytochrome b6f complex of oxygenic photosynthesis. Annu Rev Plant Physiol Plant Mol Biol 47: 477–508
Cramer WA, Zhang H, Yan JS, Kurisu G and Smith JL (2004) Evolution of photosynthesis: time-independent structure of the cytochrome b 6 f complex of oxygenic photosynthesis. Biochemistry 43: 5921–5929
Crofts AR, Guergova-Kuras M, Kuras R, Ugulava N, Li JY and Hong SJ (2000) Proton-coupled electron transfer at the Q(o) site:whattype ofmechanismcanaccountfor the high activation barrier? Biochim Biophys Acta Bioenerg 1459: 456–466
Crofts AR and Meinhardt SW (1982) A Q-cycle mechanism for the cyclic electron-transfer chain of Rhodopseudomonas sphaeroides. Biochem Soc Trans 10: 201–203
Crowley PB, Vintonenko N, Bullerjahn GS and Ubbink M (2002) Plastocyanin-cytochrome f interactions: the influence of hydrophobic patch mutations studied by NMR spectroscopy. Biochemistry 41: 15698–15705
Crofts AR, Meinhardt SW, Jones KR and SnozziM(1983) The role of the quinone pool in the cyclic electron-transfer chain on Rhodopseudomonas sphaeroides-a modified Q-cycle mechanism. Biochim Biophys Acta 723: 202–218
Darrouzet E, Valkova-Valchanova M, Moser CC, Dutton PL and Daldal F (2000) Uncovering the 2Fe2S domain movement in cytochrome bc(1) and its implications for energy conversion. Proc Natl Acad Sci USA 97: 4567–4572
Darrouzet E, Moser CC, Dutton PL and Daldal F (2001) Large scale domain movement in cytochrome bc(1): a new device for electron transfer in proteins. Trends Biochem Sci 26: 445–451
Darrouzet E, Cooley JW and Daldal F (2004) The cytochrome bc(1) complex and its homologue the b6f complex: similarities and differences. Photosynth Res 79: 25–44
Degli Esposti M, De Vries S, Crimi M, Ghelli A, Patarnello T and Meyer A (1993) Mitochondrial cytochrome b: evolution and structure of the protein. Biochim Biophys Acta 1143: 243–271
di Rago JP, Sohm F, Boccia C, Dujardin G, Trumpower BL and Slonimski PP (1997) A point mutation in the mitochondrial cytochrome b gene obviates the requirement for the nuclear encoded core protein 2 subunit in the cytochrome bc1 complex in Saccharomyces cerevisiae. J Biol Chem 272: 4699–4704.
Diederichs K and Karplus PA (1997) Improved R-factors for diffraction data analysis in macromolecular crystallography. Nat Struct Biol 4: 269–275
Dutton PL, Moser CC, Sled VD, Daldal F and Ohnishi T (1998) A reductant-induced oxidation mechanism for complex I. Biochim Biophys Acta 1364: 245–257
Gao X, Wen X, Esser L, Quinn B, Yu L, Yu CA and Xia D (2003) Structural basis for the quinone reduction in the bc(1) complex: a comparative analysis of crystal structures of mitochondrial cytochrome bc(1) with bound substrate and inhibitors at the Q(i) site. Biochemistry 42: 9067–9080
Hochkoeppler A, Zannoni D, Ciurli S, Meyer TE, Cusanovich MA and Tollin G (1996) Kinetics of photo-induced electron transfer from high-potential iron-sulfur protein to the photosynthetic reaction center of the purple phototroph Rhodoferax fermentans. Proc Natl Acad Sci USA 93: 6998–7002
Hunsicker-Wang LM, Heine A, Chen Y, Luna EP, Todaro T, Zhang YM, Williams PA, McRee DE, Hirst J, Stout CD and Fee JA (2003) High-resolution structure of the soluble, respiratory-type Rieske protein from Thermus thermophilus: analysis and comparison. Biochemistry 42: 7303–7317
Hunte C, Koepke J, Lange C, Rossmanith Tand MichelH(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 Fold Des 8: 669–684
Iwata S, Saynovits M, Link TA and Michel H (1996) Structure of a water soluble fragment of the 'Rieske' iron-sulfur protein of the bovine heart mitochondrial cytochrome bc1 complex determined by MAD phasing at 1.5 Å resolution. Structure 4: 567–579
Iwata S, Lee JW, Okada K, Lee JK, Iwata M, Rasmussen B, Link TA, Ramaswamy S and Jap BK (1998) Complete structure of the 11-subunit bovine mitochondrial cytochrome bc1 complex. Science 281: 64–71
Jenney FE and Daldal F (1993) A novel membrane-associated C-type cytochrome, cyt cy, can mediate the photosynthetic growth of Rhodobacter capsulatus and Rhodobacter sphaeroides. EMBO J 12: 1283–1292
Jenney FE, Prince RC Daldal F (1994) Roles of the soluble cytochrome C(2) and membrane-associated cytochrome C(Y) of Rhodobacter capsulatus in photosynthetic electron-transfer. Biochemistry 33: 2496–2502
Jones TA, Zhou J-Y, Cowan SW and Kjeldgaard M (1991) Improved methods for building protein models in electron density maps and the location of errors on these models. Acta Crystallogr A47: 110–119
Kerfeld CA, Chan C, Hirasawa M, KleisSanFrancisco S, Yeates TO and Knaff DB (1996) Isolation and characterization of soluble electron transfer proteins from Chromatium purpuratum. Biochemistry 35: 7812–7818
Kleywegt GJ and Jones TA (1994) Convenient single and multiple crystal real-space... CCP4 Newsletter: 59–66
Kraulis PJ (1991) MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J Appl Crystallogr 24: 946–950
Kuras R, Guergova-Kuras M and Crofts AR (1998) Steps toward constructing a cytochrome b6 f complex in the purple bacterium Rhodobacter sphaeroides: an example of the structural plasticity of a membrane cytochrome. Biochemistry 37: 16280–16288
Kurisu G, Zhang HM, Smith JL and Cramer WA (2003) Structure of the cytochrome b 6 f complex of oxygenic photosynthesis: tuning the cavity. Science 302: 1009–1014
Kurowski B and Ludwig B (1987) The genes of the Paracoccus denitrificans-bc 1 complex-nucleotide-sequence and homologies between bacterial and mitochondrial subunits. J Biol Chem 262: 13805–13811
Lange C and Hunte C (2002) Crystal structure of the yeast cytochrome bc 1complex with its bound substrate cytochrome c. Proc Natl Acad Sci USA 99: 2800–2805
Martinez SE, Huang D, Szczepaniak A, Cramer WA and Smith JL (1994) Crystal structure of chloroplast cytochrome f reveals a novel cytochrome fold and unexpected heme ligation. Structure 2: 95–105
McFadden DC, Tomavo S, Berry EA and Boothroyd JC (2000) Characterization of cytochrome b from Toxoplasma gondii and Q(o) domain mutations as a mechanism of atovaquoneresistance. Mol Biochem Parasitol 108: 1–12
Mitchell P (1976) Possible molecular mechanisms of the protonmotive function of cytochrome systems. J Theor Biol 62: 327–367
Muller F, Crofts AR and Kramer DM (2002) Multiple Q-cycle bypass reactions at the Q(o) site of the cytochiome bc(1) complex. Biochemistry 41: 7866–7874
Navaza J (1994) AMoRe: an automated package for molecular replacement. Acta Crystallogr A50: 157–163
Osyczka A, Dutton PL, Moser CC, Darrouzet E and Daldal F (2001) Controlling the functionality of cytochrome c1 redox potentials in the Rhodobacter capsulatus bc 1complex through disulfide anchoring of a loop and a beta-branched amino acid near the heme-ligating methionine. Biochemistry 40: 14547–14556
Osyczka A, Moser CC, Daldal F and Dutton PL (2004) Reversible redox energy coupling in electron transfer chains. Nature 427: 607–612
Otwinowski Z, Borek D, Majewski W and Minor W (2003) Multiparametric scaling of diffraction intensities. Acta Crystallogr A 59: 228–234
Palsdottir H, Lojero CG, Trumpower BL and Hunte C (2003) Structure of the yeast cytochrome bc1 complex with a hydroxyquinone anion Qo site inhibitor bound. J Biol Chem 278: 31303–31311
Rieske JS, Maclennan DH and Coleman R (1964) Isolation + Properties of iron-protein from beef heart mitochondria. Fed Proc 23: 323
Robertson DE, Ding HG, Chelminski PR, Slaughter C, Hsu J, Moomaw C, Tokito M, Daldal F and Dutton PL (1993) Hydroubiquinone cytochrome-c2 oxidoreductase from Rhodobacter capsulatus-definition of a minimal, functional isolated preparation. Biochemistry 32: 1310–1317
Saraste M (1999) Oxidative phosphorylation at the fin de siecle. Science 283: 1488–1493
Saribas AS, Mandaci S and Daldal F (1999) An engineered cytochrome b6c1 complex with a split cytochrome b is able to support photosynthetic growth of Rhodobacter capsulatus. J Bacteriol 181: 5365–5372
Sayle RA and Milner-White EJ (1995) RASMOL: biomolecular graphics for all. Trends Biochem Sci 20: 374
Schagger H, Brandt U, Gencic S and von Jagow G (1995) Ubiquinol-cytochrome-c reductase from human and bovine mitochondria. Methods Enzymol 260: 82–96
Soriano GM, Ponamarev MV, Carrell CJ, Xia D, Smith JL and Cramer WA (1999) Comparison of the cytochrome bc1 complex with the anticipated structure of the cytochrome b6 f complex: de plus ç a change de plus c'est la me` me chose. J Bioenerg Biomembr 31: 201–213
Stonehuerner J, Obrien P, Geren L, Millett F, Steidl J, Yu L and Yu CA (1985) Identification of the binding-site on cytochrome c1 for cytochrome c. J Biol Chem 260: 5392-5398 Stroebel D, Choquet Y, Popot JL and Picot D (2003) An atypical haem in the cytochrome b6f complex. Nature 426: 413–418
Trumpower BL (2002) A concerted, alternating sites mechanism of ubiquinol oxidation by the dimeric cytochrome bc1 complex. Biochim Biophys Acta-Bioenerg 1555: 166–173
Xia D, Yu CA, Kim H, Xian JZ, Kachurin AM, Zhang L, Yu L and Deisenhofer J (1997) Crystal structure of the cytochrome bc 1complex from bovine heart mitochondria. Science277: 60–66
Xiao KH, Liu XY, Yu CA and Yu L (2004) The extra fragment of the iron-sulfur protein (residues 96-107) of Rhodobacter sphaeroides cytochrome bc 1complex is required for protein stability. Biochemistry 43: 1488–1495
Yang XH and Trumpower BL (1986) Purification of a threesubunit ubiquinol-cytochrome c oxidoreductase complex from Paracoccus denitrificans. J Biol Chem 261: 12282–12209 [published erratum appears in J Biol Chem 1986 Nov 25; 261(33): 15813]
Yun CH, Crofts AR and Gennis RB (1991) Assignment of the histidine axial ligands to the cytochrome bH and cytochrome b l components of the bc 1complex from Rhodobacter sphaeroides by site-directed mutagenesis. Biochemistry 30: 6747–6754
Zara V, Palmisano I, Conte L and Trumpower BL (2004) Further insights into the assembly of the yeast cytochrome bc1 complex based on analysis of single and double deletion mutants lacking supernumerary subunits and cytochrome b. Eur J Biochem 271: 1209–1218
Zhang Z, Huang L, Shulmeister VM, Chi YI, Kim KK, Hung LW, Crofts AR, Berry EA and Kim SH (1998) Electron transfer by domain movement in cytochrome bc1. Nature 392: 677–684
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Berry, E.A., Huang, LS., Saechao, L.K. et al. X-Ray Structure of Rhodobacter Capsulatus Cytochrome bc 1: Comparison with its Mitochondrial and Chloroplast Counterparts. Photosynthesis Research 81, 251–275 (2004). https://doi.org/10.1023/B:PRES.0000036888.18223.0e
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DOI: https://doi.org/10.1023/B:PRES.0000036888.18223.0e