Abstract
This review compares the three-dimensional structures of the solublec-type cytochromes that functionally link membrane-bound energy transducingcomplexes in algal, cyanobacterial and eubacterial photosynthesis. Inanoxygenic photosynthesis, cytochrome c2transfers electronsbetween the cytochrome bc1complex and the eubacterialreaction center. Cytochrome c6performs the analogous functionin oxygenic photosynthesis, carrying electrons between the cytochromeb6f complex and Photosystem I. One of the most strikingobservations from recent progress in elucidating the structures of themembrane-bound electron transfer partners of cytochrome c2andcytochrome c6is the structural similarity between PhotosystemI and the bacterial reaction center. Are there similarities in thestructures of cytochrome c2and cytochrome c6that are functionally relevant in the context of their interaction withtheir membrane-bound redox partners? In addition to providing a generaldescription of the structures of cytochrome c2and cytochromec6, the following comparison addresses this question.
References
Adam Z and Malkin R (1989) On the interaction between cytochrome fand plastocyanin. Biochim Biophys Acta 975: 158-163
Adir N, Axelrod HL, Beroza P, Isaacson RA, Rongey SH, Okamura MY and Feher G (1996) Co-crystallization and characterization of the photosynthetic reaction center-cytochrome c 2complex from Rhodobacter sphaeroides. Biochemistry 35: 2535-2547
Adzhubei AA and Sternberg MJE (1993) Left-handed polyproline II helices commonly occur in globular proteins. J Mol Biol 229: 472-493
Axelrod HL, Feher G, Allen JP, Chirino AJ, Day MW, Hsu BT and Rees DC (1994) Crystallization and X-ray structure determination of cytochrome c 2from Rhodobacter sphaeroidesin three crystal forms. Acta Crystallogr D50: 596-602
Batie CJ and Kamin H (1981) The relation of pH and oxidation-reduction potential to the association state of the ferredoxin-ferredoxin:NADP reductase complex. J Biol Chem 256: 7756-7763
Benning MW, Wesenberg G Caffrey MS, Bartsch RG, Meyer TE, Cusanovich MA, Rayment I and Holden HM (1991) Molecular structure of cytochrome c 2isolated from Rhodobacter capsulatusdetermined at 2.5 Å resolution. J Mol Biol 220: 673-685
Benning MW, Meyer TE and Holden HM (1996) Molecular structure of a high potential cytochrome c 2isolated from Rhodophila globiformis. Arch Biochem Biophys 333: 338-348
Berghuis AM and Brayer GD (1992) Oxidation state-dependent conformational changes in cytochrome c. J Mol Biol 223: 959-976
Boekema EJ, Dekker JP, van Heel MG, Rogner M, Saenger W, Witt I and Witt HT (1987) Evidence for a trimeric organization of the Photosystem I complex from the thermophilic cyanobacterium Synechococcussp. FEBS Lett 217: 283-286
Bosshard DR, Wynn RMand Knaff DB (1987) Binding site on Rhodospirillum rubrumcytochrome c 2for the Rhodospirillum rubrumcytochrome bc 1complex. Biochemistry 26: 7688-7693.
Campos AP, Auiar AP, Hervas M, Regalla M, Navarro JA, Ortega JM, Xavier AV, De La Rosa MA and Teixeira M (1993) Cytochrome c 6from Monophoridium braunii: A cytochrome with an unusual heme axial coordination. Eur J Biochem 216: 329-341
Chain RK and Malkin R (1991) The chloroplast cytochrome b 6 fcomplex can exist in monomeric and dimeric states. Photosynth Res 28: 59-68
Chen L, Durley R, Poliks BJ, Hamada K, Chen Z, Mathews FS, Davidson VL, Satow Y, Huizinga E, Vellieux FMD and Hol WGJ (1992) Crystal structure of an electron transfer complex between methylamine dehydrogenase and amicyanin. Biochemistry 31: 4959-4964
Davis DJ, Krogmann DW and San Pietro A (1980) Electron donation to Photosystem I. Plant Physiol 65: 697-702
Diaz A, Hervas M, Navarro JA, De La Rosa MA and Tollin G (1994) A thermodynamic study by laser flash photolysis of plastocyanin and cytochrome c 6oxidation by Photosystem I from the green alga Monoraphidium braunii. Eur J Biochem 222: 1001-1007
Feng S, Kasahara C, Rickles RJ and Schreiber SL (1995) Specific interactions outside the proline-rich core of two classes of Src homology 3 ligands. Proc Natl Acad Sci USA 92: 12408-12415
Ferguson-Miller S, Brautigan DL and Margoliash E (1978) Definition of cytochrome c binding domains by chemical modification. III. Kinetics of reaction of carboxydinotrophenyl cytochrome cwith cytochrome coxidase. J Biol Chem 253: 149-159
Frazao C, Soares CM, Carrondo MA, Pohl E, Dauter Z, Wilson KS, Hervas M, Navarro JA, De la Rosa MA and Sheldrick GM (1995) Ab initiodetermination of the crystal structure of cytochrome c 6and comparison with plastocyanin. Structure 3: 1159-1169
Fromme P (1996) Structure and function of Photosystem I. Curr Opin Struct Biol 6: 473-484
Fromme P, Witt HT, Schubert W-D, Klukas O, Saenger W and Krauss N (1996) Structure of Photosystem I at 4.5 Å resolution: A short review including evolutionary aspects. Biochim Biophys Acta 1275: 76-83
Golbeck JH (1994) Photosystem I in cyanobacteria. In: Bryant DA (ed) The Molecular Biology of Cyanobacteria, pp 319-360. Kluwer Academic Publishers, Dordrecht, the Netherlands
Gray, KA, Davidson VL and Knaff DB (1988) Complex formation between methylamine dehydrogenase and amicyanin from Paracoccus denitrificans. J Biol Chem 263: 13987-13990
Hall J, Zha X, Yu L, Yu C-A and Millett F (1989) Role of specific lysine residues in the reaction of Rhodobacter sphaeroidescytochrome c 2with the cytochrome bc 1complex. Biochemistry 28: 2568-2571
Handschumacher MD and Richards FM (1994) SURFACE In: The CCP4 Suite: Programs for Protein Crystallography. Acta Cryst D50: 760-763
Hatanaka H, Sonoike K, Hirano M and Katoh S (1993) Small subunits of Photosystem I reaction center complexes from Synechococcus elongatus. I. Is the psaFgene product required for oxidation of cytochrome c-553? Biochim Biophys Acta 1141: 45-51
Hervas M, DeLaRosa MA and Tollin G (1992) A comparative laser-flash absorption spectroscopy study of algal plastocyanin and cytochrome c-552photooxidation by Photosystem I particles from spinach. Eur J Biochem 203: 115-120
Hippler M, Ratajczak R and Haehnel W (1989) Identification of the plastocyanin binding subunit of Photosystem I. FEBS Lett 250: 280-284
Ho KK and Krogmann DW (1984) Electron donors to P700 in cyanobacteria and algae, an instance of unusual genetic variability. Biochim Biophys Acta 766: 310-316
Huang D, Everly RM, Cheng RH, Heymann JB, Schagger H, Sled V, Ohnishi T, Baker TS and Cramer WA (1994) Characterization of the chloroplast cytochrome b 6 fcomplex as a structural and functional dimer. Biochemistry 33: 4401-4409
Imhoff JF, Truper HG and Pfennig N (1984) Rearrangement of the species and genera of the phototrophic purple nonsulfur bacteria. Int J Sys Bact 34: 340-343
Iwata S, Osermeier C, Ludwig B and Michel H (1995) Structure at 2.8 Å resolution of cytochrome oxidase from Paracoccus denitrificans. Nature 376: 660-669
Jeng M-F and Englander WS (1991) Stable submolecular folding units in a non-compact form of cytochrome c. J Mol Biol 221: 1045-1061
Jeng M-F, Englander WS, Elove GA, Wand J and Roder H (1990) Structural description of acid-denaturated cytochrome cby hydrogen exchange and 2D NMR. Biochemistry 29: 10433-10437
Kabsch W and Sander C (1983) Dictionary of protein secondary structure: Pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 22: 2577-2637
Keller RM, Wuthrich K and Schejter A (1978) H-NMR studies of the heme iron coordination in cytochrome c-552from Euglena gracilis. Biochim Biophys Acta 491: 409-415
Kerfeld CA, Anwar HP, Interrante R, Merchant S and Yeates TO (1995) The structure of chloroplast cytochrome c 6at 1.9 Å resolution: Evidence for functional oligomerization. J Mol Biol 250: 627-647
Kraulis PJ (1991) MOLSCRIPT: A program to produce both detailed and schematic plots of protein structure. J Appl Crystallog 24: 946-950
Krauss N, Hinrichs W, Witt I, Fromme P, Pritzkow W, Dauter Z, Betzel C, Wilson KS, Witt HT and Saenger W (1993) Three-dimensional structure of system I of photosynthesis at 6.0 Å resolution. Nature 361: 326-331
Krauss N, Scubert W-D, Klukas O, Fromme P, Witt HT and Saenger W (1996) Photosystem I at 4 Å resolution represents the first structural model of a joint photosynthetic reaction centre and core antenna system. Nature Struct Biol 3: 965-973
Kruip J, Boekema EJ, Bald D, Boonstra AF and Rogner M (1993) Isolation and structural characterization of monomeric and trimeric Photosystem I complexes (P700-FA/FBand P700-FXfrom the cyanobacterium SynechocystisPCC 6803 J Biol Chem 268: 23353-23360
Kuhn M, Fromme P and Krabben L (1994) A ‘membrane-attached’ α-helix: A conserved structural motif in bacterial reaction centres, Photosystem I and chloroplast NADH-plastoquinone oxidoreductase. Trends Biochem Sci 19: 401-402
Laskowski RA, MacArthur MW, Moss DS and Thornton JM (1993) PROCHECK: A program to check the sterochemical quality of protein structures. J Appl Crystallog 26: 283-291
Liang N, Mauk AG, Pielak GJ, Johnson JA, Smith M and Hoffman BM (1988) Regulation of interprotein electron transfer by residue 82 of yeast cytochrome c. Science 240: 311-313
Long JE, Durham B, Okamura M and Millett F (1989) Role of specific lysine residues in binding cytochrome c 2to the Rhodobacter sphaeroidesreaction center in optimal orientation for rapid electron transfer. Biochemistry 28: 6970-6974
Ludwig ML, Pattridge KA, Powers TB, Dickerson RE and Takano T (1982) Structure analysis of a ferricytochrome cfrom the cyanobacteriumAnacystis nidulans. In: Ho CH (ed) Electron Transport and Oxygen Utilization, pp 27-32. Elsevier Science Publishers, Amsterdam
Martinez SE, Huang D, Szczepaniak A, Cramer WA and Smith JL (1994) Crystal structure of chloroplast cytochrome freveals a novel fold and unexpected heme ligation. Structure 2: 95-105
Mathews FS (1985) The structure function and evolution of cytochromes. Prog Biophys Mol Biol 45: 1-56
Mathews FS, Chen Z-W and Bellamy HD (1991) Three-dimensional structure of p-cresol methylhydroxylase (Flavocytochrome c) from Pseudomonas putidaat 3.0 Å resolution. Biochemistry 30: 238-247
Matsuura K, Fukushima A, Shimada K and Satoh T (1988) Direct and indirect electron transfer from cytochromes cand c 2to the photosynthetic reaction center in pigment—protein complexes isolated from Rhodocyclus gelatinsosus. FEBS Lett 237: 21-25
Meyer TE and Donohue TJ (1995) Cytochromes, iron-sulfur and copper proteins mediating electron transfer from the cyt bc 1complex to photosynthetic reaction center complexes. In: Blankenship RE, Madigan MT and Bauer CE (eds) Anoxygenic Photosynthetic Bacteria, pp 725-745. Kluwer Academic Publishers, Dordrecht, the Netherlands
Miki K, Sogabe S, Uno A, Ezoe T, Kasai N, Saeda M, Matsuura Y and Miki M (1994) Application of automatic molecular replacement procedure to crystal structure analysis of cytochrome c 2from Rhodpseudomonas viridis. Acta Crystallogr D 50: 271-275
Moore GR and Pettigrew GW (1990) Cytochromes c: Evolutionary, Structural and Physiochemical Aspects. Springer-Verlag, Berlin
Morand LZ, Frame MK, Colvert KK, Johnson DA, Krogmann DW and Davis DJ (1989) Plastocyanin cytochrome finteraction. Biochemistry 28: 8039-8047
Morand LZ, Cheng RH and Krogmann DW (1994) Soluble electron transfer catalysts of cyanobacteria. In Bryant DA (ed) The Molecular Biology of Cyanobacteria, pp 243-268. Kluwer Academic Publishers, Dordrecht, the Netherlands
Morschel E and Staehelin LA (1983) Reconstitution of cytochromef/b 6and CF0-CF1ATP-Synthetase complexes into phospholipid and galactolipid liposomes. J Cell Biol 97: 301-310
Musacchio A, Saraste M and Wilmanns M (1994) High-resolution crystal structures of tyrosine kinase SH3 domains complexed with proline-rich polypeptides. Nature Struct Biol 1: 546-551
Paik WK and Kim S (1992) Effect of methyl substitution on protein tertiary structure. J Theor Biol 155: 335-342
Pelletier H and Kraut J (1992) Crystal structure of a complex between electron transfer partners cytochrome cperoxidase and cytochrome c. Science 258: 1748-1755
Qi PX, Urbauer JL, Fuentes EJ, Leopold MF and Ward AJ (1994) Structural water in oxidized and reduced horse heart cytochrome c. Nature Struct Biol 1: 378-381
Ramirez BE, Malmstrom BG, Winkler JR and Gray HB. (1995) The currents of life: The terminal electron transfer complex of respiration. Proc Natl Acad Sci USA 92: 11949-11951
Salemme FR, Freer ST, Xuong NH, Alden RA and Kraut J (1973) The structure of oxidized cytochrome c 2of Rhodospirillum rubrum. J Biol Chem 248: 3910-3921
Schubert WD, Klukas O, Krauss N, Saenger W, Fromme P and Witt HT (1995) Present state of the crystal structure analysis of Photosystem I. Xth International Photosynthesis Congress, Montpellier France, Progr Abstr PL12
Smith JM, Smith WH and Knaff DB (1981) Electrochemical titrations of a ferredoxin-ferredoxin:NADP oxidoreductase complex. Biochim Biophys Acta 635: 405-441
Sogabe S and Miki K (1995) Refined crystal structure of ferrocytochrome c2from Rhodopseudomonas viridisat 1.6 Å resolution. J Mol Biol 252: 235-247
Takano T and Dickerson RE (1982) Conformational differences between ferri-and ferrocytochrome c. In: Ho CH (ed) Electron Transport and Oxygen Utilization, pp 17-26. Elsevier Science Publishers, Amsterdam
Tiede DM, Vashishta A-C and Gunner MR (1993) Electron transfer kinetics and electrostatic properties of the Rb. sphaeroidesreaction center and soluble cytochromes. Biochemistry 32: 4515-4531
Tollin G, Hanson LK, Caffrey M, Meyer TE and Cusanovich MA (1986) Redox pathways in electron-transfer proteins: Correlations between reactivities, solvent exposure, and unpaired-spin-density distributions. Proc Natl Acad Sci USA 83: 3693-3697
Vervoot J (1991) Electron transferring proteins. Curr Opin Struct Biol 1: 889-894
Wood PM (1978) Interchangeable copper and iron proteins in algal photosynthesis. Studies on plastocyanin and cytochrome c-552in Chlamydomonas. Eur J Biochem 87: 9-19
Wynn RM and Malkin R (1988) Interaction of plastocyanin with Photosystem I: A chemical cross-linking study of the polypeptide that binds plastocyanin. Biochemistry 27: 5863-5869
Yu H, Chen JK, Feng S, Dalgarno DC, Brauer AW and Schreiber SL. (1994) Structural basis for the binding of proline-rich peptides to SH3 domains. Cell 76: 933-945
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Kerfeld, C.A. Structural comparison of cytochrome c2and cytochrome c6 . Photosynthesis Research 54, 81–98 (1997). https://doi.org/10.1023/A:1005969216388
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DOI: https://doi.org/10.1023/A:1005969216388