The cytochrome bc1 complex and its homologue the b6f complex: Similarities and differences

Photosynthesis Research

Volumn 79, Issue 1, 2004, Pages 25-44

  Darrouzet, Elisabeth ^a   Cooley, Jason W ^b   Daldal, Fevzi ^b  

^a CEA Marcoule   (France)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Cytochrome bc1 and b6f complexes; Electron transfer; Proton translocation; Respiration and photosynthesis; Ubihydroquinone:cytochrome c and plastohydroquinone:plastocyanin oxidoreductases

Indexed keywords

ALGAE; BACTERIA (MICROORGANISMS); CYANOBACTERIA; EUKARYOTA;

EID: 0442329855     PISSN: 01668595     EISSN: None     Source Type: Journal    
DOI: 10.1023/B:PRES.0000011926.47778.4e     Document Type: Review

References (167)

1. Anemüller S and Schäfer G (1990) Cytochrome 003 from Sulfolobus acidocaldarius, a single-subunit, quinol oxidizing archaebacterial terminal oxidase. Eur J Biochem 191: 297-305
2. H heme. Arch Biochem Biophys 354: 206-214
3. Axelrod HL, Abresch EC, Okamura MY, Yeh AP, Rees DC and Feher G (2002) X-ray structure determination of the cytochromes C2: reaction center electron transfer complex from Rhodobacter sphaeroides. J Mol Biol 319: 501-515
4. 6f complex: evidence for the existence of two binding pockets in the lumenal site. Biochemistry 38: 12814-12821
5. 1 complex from Rhodobacter capsulatus. Biochemistry 38: 188-199
6. Bernhard M, Friedrich B and Siddiqui RA (2000) Ralstonia eutropha TF93 is blocked in Tat-mediated protein export. J Bacteriol 182: 581-588
7. 3 complexes. J Biol Chem 260: 2458-2467
8. Berry EA, Guergova-Kuras M, Huang LS and Crofts AR (2000) Structure and function of cytochrome be complexes. Annu Rev Biochem 69: 1005-1075
9. 1 segment of the mitochondrial respiratory chain. J Biol Chem 257: 8321-8330
10. 1 complex by proton-gated charge transfer. FEBS Lett 387: 1-6
11. 1 complex. Biochim Biophys Acta 1275: 61-69
12. 1 complex. Biochemistry 36: 11685-11696
13. 1 complex? Biochim Biophys Acta 1555: 37-43
14. 6f complex induced by inhibitor binding. J Biol Chem 275: 13195-13201
15. 1 complex. Biochim Biophys Acta 1459: 467-474
16. Brugna M, Albouy D and Nitschke W (1998) Diversity of cytochrome be complexes: example of the Rieske protein in green sulfur bacteria. J Bacteriol 180: 3719-3723
17. Brugna M, Rodgers S, Schricker A, Montoya G, Kazmeier M, Nitschke 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
18. Carrell CJ, Zhang H, 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
19. 1 complex and reconstitution of recombinant protein with three-subunit core complex. J Biol Chem 271: 2057-2062
20. Choquet Y, Stern DB, Wostrikoff K, Kuras R, Girard-Bascou J and Wollman FA (1998) Translation of cytochrome f is autoregulated through the 5′ untranslated region of petA mRNA in Chlamydomonas chloroplasts. Proc Natl Acad Sci USA 95: 4380-4385
21. 1 complex. FEBS Lett 456: 37-40
22. Cramer W, Soriano G, Ponomarev M, Huang D, Zhang H, Martinez S and Smith J (1996) Some new structural aspects and old controversies concerning the cytochrome b(6)f complex of oxygenic photosynthesis. Annu Rev Plant Physiol 47: 477-508
23. 1 complex of mitochondria and photosynthetic bacteria. Curr Opin Struct Biol 8: 501-509
24. Crofts AR, Meinhardt SW, Jones KR and Snozzi M (1983) The role of the quinone pool in the cyclic electron-transfer chain of Rhodopseudomonas sphaeroides: a modified Q-cycle mechanism. Biochim Biophys Acta 723: 202-218
25. 1 complex: different domains of the quinol binding pocket and their role in the mechanism and binding of inhibitors. Biochemistry 38: 15807-15826
26. 1 complex. Proc Natl Acad Sci USA 96: 10021-10026
27. 1 and cytochrome c oxidase complexes associate to form a single supra complex in yeast mitochondria. J Biol Chem 275: 18093-18098
28. 1 complex of Rhodobacter capsulatus. EMBO J 8: 3951-3961
29. o site catalysis. J Biol Chem 277: 3471-3476
30. 1 complex. Biochemistry 42: 1499-1507
31. 1 complex. Biochemistry 39: 15475-15483
32. 1 and its implications for energy conversion Proc Natl Acad Sci USA 97: 4567-4572
33. 1: a new device for electron transfer in proteins. Trends Biochem Sci 26: 445-451
34. 1 complex. J Biol Chem 277: 3464-3470
35. 1 complex of Rhodobacter capsulatus probed by site-directed mutagenesis. Biochemistry 31: 3342-3351
36. 1 sub complex with an intact quinone reduction site. Biochemistry 31: 3351-3358
37. Degli-Esposti M, deVries S, Crimi M, Ghelli A, Paternello T and Meyer A (1993) Mitochondrial cytochrome b: evolution and structure of the protein. Biochim Biophys Acta 1143: 243-271
38. 1 complex from bovine heart mitochondria. J Biol Chem 33: 20752-20757
39. 6f turnovers from the study of H/D substitution effects on the electrogenicity and electron transfer reactions. Biochemistry 39: 3304-3310
40. Denke E, Merbitz-Zahradnik T, Hatzfeld OM, Snyder CH, Link TA and Trumpower BL (1998) Alteration of the midpoint potential and catalytic activity of the Rieske iron-sulfur protein by changes of amino acids forming hydrogen bonds to the iron-sulfur cluster. J Biol Chem 273: 9085-9093
41. de Vitry C, Finazzi G, Baymann F and Kallas T (1999) Analysis of the nucleus-encoded and chloroplast-targeted Rieske protein by classic and site-directed mutagenesis of Chlamydomonas. Plant Cell 11: 2031-2044
42. o site model. Biochemistry 31: 3144-3158
43. 1 complex. Biochemistry 34: 15979-15996
44. di Rago JP, Netter P, Slonimski PP (1990) Intragenic suppressors reveal long distance interactions between inactivating and reactivating amino acid replacements generating three-dimensional constraints in the structure of mitochondrial cytochrome b. J Biol Chem 265: 15750-15757
45. Dutton PL, Ohnishi T, Darrouzet E, Leonard MA, Sharp RE, Gibney BR, Daldal F and Moser CC (2000) Coenzyme Q oxidation reduction reactions in mitochondrial electron transport. In: Kagan VE and Quinn PJ (eds) Coenzyme Q: Molecular Mechanisms in Health and Disease, pp 65-82. CRC Press LLC, New York
46. 6f complex can bypass cytochrome f. J Biol Chem 276: 30598-30607
47. o site occupancy in LHC II kinase activation. J Biol Chem 276: 9770-9774
48. 6 in situ. Biochemistry 28: 8990-8998
49. 1 subunits between prokaryotes, mitochondria, and chloroplasts. J Bioenerg Biomembr 20: 59-83
50. 1 in complex with famoxadone: the role of aromatic-aromatic interaction in inhibition. Biochemistry 41: 11692-11702
51. 1 complexes of Rhodobacter sphaeroides and Rhodobacter capsulatus. J Bioenerg Biomembr 25: 195-209
52. 1 complex in plants. J Bioenerg Biomembr 31: 259-274
53. 1. Biochemistry 38: 9031-9038
54. 1 complex of Rhodobacter capsulatus: ubiquinol oxidation in a dimeric Q-cycle? FEBS Lett 431: 291-296
55. 1 complexes. In: Blankenship RE, Madigan MT and Bauer C (eds) Anoxygenic Photosynthetic Bacteria, pp 747-774. Kluwer Academic Publishers, Dordrecht, The Netherlands
56. 1 complex. Biochemistry 33: 723-733
57. 6f complex activity. J Biol Chem 264: 4506-4512
58. 1 complex. Biochemistry 39: 7436-7444
59. 6f complex undergoes reversible phosphorylation upon state transition. J Biol Chem 275: 17072-17079
60. Hauska G, Hurt E, Gabellini N and Lockau W (1983) Comparative aspects of quinol-cytochrome c/plastocyanin oxidoreductases. Biochim Biophys Acta 726: 97-133
61. Heimann S, Klughammer C and Schreiber U (1998) Two distinct states of the thylakoid bf complex. FEBS Lett 426: 126-130
62. 6f complex. Biochemistry 39: 2692-2699
63. 6f complex as a structural and functional dimer. Biochemistry 33: 4401-4409
64. 1 complex from the yeast Saccharomyces cerevisiae co-crystallized with an antibody Fv-fragment. Structure 8: 669-684
65. 1 complex determined by MAD phasing at 1. 5 Å resolution. Structure 4: 567-579
66. 1 complex. Science 281: 64-71
67. 1 complex. Biophys J 77: 1753-1768
68. Joliot P and Joliot A (1994) Mechanism of electron transfer in the cytochrome b/f complex of algae: evidence for a semiquinone cycle. Proc Natl Acad Sci USA 91: 1034-1038
69. Joliot P and Joliot A (2001) Electrogenic events associated with electron and proton transfers within the cytochrome b6/f complex. Biochim Biophys Acta 1503: 367-376
70. Jones RW and Whitmarsh J (1986) The electrogenic reaction and proton release during quinol oxidation by the cytochrome b/f complex. In: Biggins J (ed) Proceedings VII International Congress on Photosynthesis, pp 101-106. Martinus Nijhoff, The Hague, The Netherlands
71. Kallas T, Spiller S and Malkin R (1988) Characterization of two operons encoding the cytochrome b6-f complex of the cyanobacterium Nostoc PCC 7906. Highly conserved sequences but different gene organization than in chloroplasts. J Biol Chem 263: 14334-14342
72. 1 complex from bovine heart. Proc Natl Acad Sci USA 95: 8026-8033
73. 1 complex. J Biol Chem 266: 14270-14276
74. Kramer DM and Crofts AR (1994) Re-examination of the properties and function of the b cytochromes of the thylakoid cytochrome bf complex. Biochim Biophys Acta 1184: 193-201
75. 6 protein from a fusion protein expressed in Escherichia coli. Biochim Biophys Acta 1598: 177-184
76. 6f complexes: an approach using genetic transformation of the green alga Chlamydomonas reinhardtii. EMBO J 13: 1019-1027
77. Kuras R, de Vitry C, Choquet Y, Girard-Bascou J, Culler D, Buschlen S, Merchant S and Wollman FA (1997) Molecular genetic identification of a pathway for heme binding to cytochrome b6. J Biol Chem 272: 32427-32435
78. 6f complex in the purple bacterium Rhodobacter sphaeroides: an example of the structural plasticity of a membrane cytochrome. Biochemistry 37: 16280-16288
79. 1 complex structure. EMBO J 20: 6591-6600
80. 1 complex with its bound substrate cytochrome c. Proc Natl Acad Sci USA 99: 2800-2805
81. 6) in Synechococcus sp. PCC 7002. Biochim Biophys Acta 1504: 235-247
82. 1 and its M183K and M183H variants. Biochim Biophys Acta 1556: 175-186
83. Liebl U, Pezennec S, Riedel A, Kellner E and Nitschke W (1992) The Rieske FeS center from the Gram-positive bacterium PS3 and its interaction with the menaquinone pool studied by EPR. J Biol Chem 267: 14068-14072
84. 1 complex are essential for protein structure, properties of the [2Fe-2S] cluster, and communication with the quinone pool. Biochemistry 36: 11675-11684
85. 1 complex. FEBS Lett 412: 257-264
86. Link TA (1999) The structures of Rieske and Rieske-type proteins. Adv Inorg Chem 47: 213-287
87. 6/f complex of spinach chloroplasts. FEBS Lett 131: 169-172
88. Malkin R (1986) Interactions of stigmatellin and DNP-INT with the Rieske iron-sulfur center of the chloroplast cytochrome b6-f complex. FEBS Lett 208: 317-320
89. 6f complex in Synechocystis sp. 6803. FEBS Lett 519: 82-86
90. 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
91. Matsuno-Yagi A and Hatefi Y (1999) Ubiquinol:cytochrome c oxidoreductase. Effects of inhibitors on reverse electron transfer from the iron-sulfur protein to cytochrome b. J Biol Chem 274: 9283-9288
92. Metzger SU, Cramer WA and Whitmarsh J (1997) Critical analysis of the extinction coefficient of cytochrome f. Biochim Biophys Acta 1319: 233-241
93. Mitchell P (1961) Coupling of phosphorylation to electron and hydrogen transfer by chemiosmotic type of mechanism. Nature 191: 144-148
94. Mitchell P (1975) The protonmotive Q cycle: a general formulation. FEBS Lett 59: 137-139
95. 6/f complex in chloroplasts. Missing link in the evolution of protein transport pathways in chloroplasts? J Biol Chem 276: 42761-4276
96. 1 complex from Rhodovulum sulfidophilum is a dimer with six quinones per monomer and an additional 6-kDa component. Eur J Biochem 259: 709-718
97. 1 of Euglena gracilis mitochondrial complex III. Eur J Biochem 178: 649-656
98. 1 complex. Biochemistry 41: 7866-7874
99. 1 complex. Eur J Biochem 267: 5777-5782
100. Neupert W (1997) Protein import into mitochondria. Annu Rev Biochem 66: 863-917
101. 1. J Biol Chem 278: 4339-4346
102. 6f complexes. Biochim Biophys Acta 974: 223-226
103. 6f complex (the 'Rieske centre'). Biochim Biophys Acta 1102: 266-268
104. 1 complex of yeast mitochondria. Biochim Biophys Acta 1457: 36-44
105. 1 redox potential in the Rhodobacter capsulants bc1 complex through disulfide anchoring of a loop and a β-branched amino acid near the heme ligating methionine. Biochemistry 40: 14547-14556
106. 1 complex. J Bacteriol 184: 3815-3822
107. 1 complex of purple non-sulfur bacterium Rhodosprillum rubrum. In: Murata N (ed) Research in Photosynthesis, Vol II, pp 761-764. Kluwer Academic Publishers, Dordrecht, The Netherlands
108. Pereira MM, Carita JN and Teixeira M (1999) Membrane-bound electron transfer of the thermohalophilic bacterium Rhodothermus marinus: a novel multihemic cytochrome bc, a new complex III. Biochemistry 38: 1268-1275
109. 6f complex from Chlamydomonas reinhardtii. J Biol Chem 270: 29342-29349
110. 6. Biochemistry 37: 17199-17208
111. 1. J Biol Chem 267: 20188-20195
112. Prince RC (1990) Bacterial Photosynthesis: From Photons to Ap in the Bacteria. Vol XII, pp 111-149. Academic Press, New York
113. Rich P (1984) Electron and proton transfers through quinones and cytochrome be complexes. Biochim Biophys Acta 768: 53-79
114. 6f complex. Biochemistry 40: 13407-13412
115. 6f complex 'Rieske' iron-sulfur protein domain movements. Biochemistry 41: 4070-4079
116. 2 oxidoreductase from Rhodobacter capsulatus: definiton of a minimal, functional isolated preparation. Biochemistry 32: 1310-1317
117. 1 complex. Biochemistry 39: 4231-4236
118. Salerno J (1984) Cytochrome electron spin resonance line shapes, ligand fields, and components stoichiometry, in ubiquinolcytochrome c oxidoreductase. J Biol Chem 259: 2331-2336
119. 1 complex, probed by electron spin echo envelope modulation. J Biol Chem 277: 4605-4608
120. Saraste M (1999) Oxidative phosphorylation at the fin de siècle. Science 283: 1488-1493
121. 1 complex with a split b is able to support photosynthetic growth of Rhodobacter capsulatus. J Bacteriol 181: 5365-5372
122. Schagger H and Pfeiffer K (2000) Supercomplexes in the respiratory chains of yeast and mammalian mitochondria. EMBO J 19: 1777-1783
123. Schatz G (1996) The protein import system of mitochondria. J Biol Chem 271: 31763-31766
124. 6f complex. J Biol Chem 276: 16780-16785
125. 1 complex in Saccharomyces cerevisiae. J Biol Chem 265: 17005-17011
126. 6f complex of Synechocystis PCC6803. J Biol Chem 277: 10949-10954
127. o-site inhibitor DBMIB favors the proximal position of the chloroplast Rieske protein and induces a pK-shift of the redox-linked proton. FEBS Lett 450: 245-250
128. 1 complex in Paracoccus denitrificans. Eur J Biochem 255: 100-106
129. Schutz M, Brugna M, Lebrun E, Baymann F, Huber R, Stetter KO, Hauska G, Toci R, Lemesle-Meunier D, Tron P, Schmidt C and Nitschke W (2000) Early evolution of cytochrome be complexes. J Mol Biol 300: 663-675
130. 1 complex). FEBS Lett 431: 423-426
131. 1 complex. Biochemistry 38: 3440-3446
132. 1 complex. Biochemistry 41: 14372-14382
133. 1 complex. J Biol Chem 275: 13535-13541
134. 6 and subunit IV. J Biol Chem 270: 10612-10617
135. 6f complex: de plus ça change de plus c'est la même chose. J Bioenerg Biomembr 31: 201-213
136. Srivastava IK, Morrisey JM, Darrouzet E, Daldal F and Vaidya AB (1999) Resistance mutations reveal the atovaquone-binding domain of cytochrome b in malaria parasites. Mol Microbiol 33: 704-11
137. Tanaka K, Takahashi MA and Asada K (1978) Isolation of monomeric cytochrome f from Japanese radish and a mechanism of autoreduction. J Biol Chem 253: 7397-403
138. 1 complex. J Biol Chem 273: 27953-27959
139. 1 complex. J Biol Chem 274: 7146-7152
140. 1 complex from Rhodobacter capsulatus. Mol Microbiol 9: 965-978
141. 1 complex. Biochim Biophys Acta 1555: 166-173
142. 1 complex: effects of inhibitors and mutations. Biochemistry 39: 15484-15492
143. 1 complex of Rhodobacter sphaeroides blocking or impairing quinol oxidation. Biochemistry 32: 8083-8091
144. von Jagow G and Ohnishi T (1985) The chromone inhibitor stigmatellin-binding to the ubiquinol oxidation center at the C-side of the mitochondrial membrane. FEBS Lett 185: 311-315
145. 1 complex. Meth Enzymol 126: 253-271
146. 6 in a cytochrome bf complex isolated from spinach thylakoids. Biochemistry 31: 8455-8459
147. Wang Y, Obungu V and Beattie D (1998) Dicyclohexylcarbodiimide inhibits proton pumping in ubiquinol:cytochrome c oxidoreductase of Rhodobacter sphaeroides and binds to aspartate-187 of cytochrome b. Arch Biochem Biophys 352: 193-198
148. 6f complex from spinach and the cyanobacterium Mastigocladus laminosus. Mol Cell Proteomics 1: 816-827
149. Widger WR, Cramer WA, Herrmann RG and Trebst A (1984) Sequence homology and structural similarity between cytochrome b of mitochondrial complex III and
150. Wollman FA (2001) State transitions reveal the dynamics and flexibility of the photosynthetic apparatus. EMBO J 20: 3623-30
151. 1 complex from bovine heart mitochondria. Science 277: 60-66
152. 1 complex by the formation of an inter subunit disulfide bond between cytochrome b and the iron-sulfur protein. J Biol Chem 275: 38597-38604
153. 1 complex in solution. J Biol Chem 276: 46125-46131
154. Xiong J and Bauer CE (2002) A cytochrome b origin of photosynthetic reaction centers: an evolutionary link between respiration and photosynthesis. J Mol Biol 322: 1025-1037
155. Xiong J, Inoue K and Bauer CE (1998) Tracking molecular evolution of photosynthesis by characterization of a major photosynthesis gene cluster from Heliobacillus mobilis. Proc Natl Acad Sci USA 95: 14851-14856
156. 6f complex to structure changes in the hinge region of the Rieske iron-sulfur protein. J Biol Chem 278: 20925-20933
157. Yu CA (1999) Special issue. J Bioenerg Biomembr 31: 167-288
158. Yu J and Le Brun NE (1998) Studies of the cytochrome subunits of menaquinone:cytochrome c reductase (bc complex) of Bacillus subtilis. Evidence for the covalent attachment of heme to the cytochrome b subunit. J Biol Chem 273: 8860-8866
159. Yu J, Hederstedt L and Piggot PJ (1995) The cytochrome be complex (menaquinone:cytochrome c oxidoreductase) in Bacillus subtilis has a nontraditional subunit organization. J Bacteriol 177: 6751-6760
160. 1 complex. J Bioenerg Biomembr 31: 251-257
161. 1. Nature 392: 677-684
162. 6f complex of oxygenic photosynthesis protects against oxygen damage. J Biol Chem 274: 1581-1587
163. 6f complex. J Biol Chem 276: 38159-38165
164. 6f complex of oxygenic photosynthesis. Proc Natl Acad Sci USA 100: 5160-5163
165. 6f turnover. Biochemistry 37: 10395-10403
166. 6f complexes controls the activation of the LHC II kinase. EMBO J 18: 2961-2969
167. 6f complex of Chlamydomonas reinhardtii. Structural implications and consequences on states transitions. J Biol Chem 277: 12446-12455