Electron-transfer kinetics and electrostatic properties of the Rhodobacter sphaeroides reaction center and soluble c-cytochromes.

The kinetics of electron transfer between the Rhodobacter sphaeroides R-26 reaction center and nine soluble c-cytochromes have been analyzed and compared to the patterns of the surface electrostatic potentials for each of the proteins. Characteristic first-order electron-transfer rates for 1:1 complexes formed at low ionic strength between the reaction center and the different c-cytochromes were identified and found to vary by a factor of almost 100, while second-order rates were found to differ by greater than 10(6). A correlation was found between the location of likely electrostatic interaction domains on each cytochrome and its characteristic rate of electron transfer. The interaction domains were identified by mapping electrostatic potentials, calculated from the Poisson-Boltzmann equation, onto simulated "encounter surfaces" for each of the cytochromes and the reaction center. For the reaction center, the c-cytochrome binding domain was found to have almost exclusively net negative potential (< -3 kT) and to be shifted slightly toward the M-subunit side of the reaction center. The location of interaction domains of complementary, positive potential (> 3 kT) differed for each cytochrome. The correspondence between electrostatic, structural, and kinetic properties of 1:1 reaction center-cytochrome complexes leads to a proposed mechanism for formation of reaction center-cytochrome electron-transfer complexes that is primarily driven by the juxtaposition of regions of delocalized complementary potential. In this mechanism the clustering of charged residues is of primary importance and not the location of specific residues. A consequence of this mechanism is that many different sets of charge distributions are predicted to be capable of stabilizing a specific configuration for a reaction center-cytochrome complex. This mechanism for reaction center association with water-soluble c-cytochromes fits molecular recognition mechanisms proposed for c-cytochromes in nonphotosynthetic systems. In general, the kinetic scheme for reaction center driven cytochrome oxidation was found to vary between a simple two-state model, involving cytochrome in free and reaction center bound states, and a three-state model, that includes cytochrome binding in kinetically competent ("proximal") and incompetent ("distal") modes. The kinetically incompetent mode of cytochrome binding is suggested not to be an intrinsic feature of the reaction center-cytochrome association but is likely to be due to variation in the physical state of the reaction center.

[1]  P. Dutton,et al.  Cytochrome c2 and reaction center of Rhodospeudomonas spheroides Ga. membranes. Extinction coefficients, content, half-reduction potentials, kinetics and electric field alterations. , 1975, Biochimica et biophysica acta.

[2]  J. D. Morgan,et al.  Molecular dynamics of ferrocytochrome c. Magnitude and anisotropy of atomic displacements. , 1981, Journal of molecular biology.

[3]  J. Lavergne,et al.  Restricted diffusion in photosynthetic membranes. , 1991, Trends in biochemical sciences.

[4]  R. Chollet,et al.  Photosynthetic carbon metabolism in Panicum milioides, a C3-C4 intermediate species: evidence for a limited C4 dicarboxylic acid pathway of photosynthesis. , 1979, Biochimica et biophysica acta.

[5]  J J Wendoloski,et al.  Molecular dynamics of a cytochrome c-cytochrome b5 electron transfer complex. , 1987, Science.

[6]  E. Margoliash,et al.  Species specificity of long-range electron transfer within the complex between zinc-substituted cytochrome c peroxidase and cytochrome c , 1985 .

[7]  J. P. Allen.  Crystallization and preliminary X-ray diffraction analysis of cytochrome c2 from Rhodobacter sphaeroides. , 1988, Journal of molecular biology.

[8]  P. Weber,et al.  Electrostatic analysis of the interaction of cytochrome c with native and dimethyl ester heme substituted cytochrome b5. , 1986, Biochemistry.

[9]  O. El-Kabbani,et al.  Comparison of reaction centers from Rhodobacter sphaeroides and Rhodopseudomonas viridis: overall architecture and protein-pigment interactions. , 1991, Biochemistry.

[10]  J. Hall,et al.  The reaction of cytochromes c and c2 with the Rhodospirillum rubrum reaction center involves the heme crevice domain. , 1987, The Journal of biological chemistry.

[11]  R. Dickerson,et al.  The structure of Paracoccus denitrificans cytochrome c550. , 1976, The Journal of biological chemistry.

[12]  J. Hall,et al.  Reaction of cytochromes c and c2 with the Rhodobacter sphaeroides reaction center involves the heme crevice domain. , 1987, Biochemistry.

[13]  G. Feher,et al.  Interaction of cytochrome c with reaction centers of Rhodopseudomonas sphaeroides R-26: localization of the binding site by chemical cross-linking and immunochemical studies. , 1983, Biochemistry.

[14]  G. Brayer,et al.  Yeast iso-1-cytochrome c. A 2.8 A resolution three-dimensional structure determination. , 1988, Journal of molecular biology.

[15]  B. Honig,et al.  On the calculation of electrostatic interactions in proteins. , 1985, Journal of molecular biology.

[16]  I. Rayment,et al.  Crystallization and preliminary analysis of crystals of cytochrome c2 from Rhodopseudomonas capsulata. , 1987, Journal of molecular biology.

[17]  M. Natan,et al.  Long-range electron transfer within metal-substituted protein complexes , 1991 .

[18]  G. Brayer,et al.  High-resolution refinement of yeast iso-1-cytochrome c and comparisons with other eukaryotic cytochromes c. , 1990, Journal of molecular biology.

[19]  J. C. Reynolds,et al.  Diffusion-controlled association rate of cytochrome c and cytochrome c peroxidase in a simple electrostatic model , 1986 .

[20]  D. Devault,et al.  Microsecond photooxidation kinetics of cytochrome c 2 from Rhodopseudomonas sphaeroides: in vivo and solution studies , 1979, FEBS letters.

[21]  G. Brayer,et al.  High-resolution three-dimensional structure of horse heart cytochrome c. , 1990, Journal of molecular biology.

[22]  R. Dickerson,et al.  Conformation change of cytochrome c. I. Ferrocytochrome c structure refined at 1.5 A resolution. , 1981, Journal of molecular biology.

[23]  N. Kasai,et al.  Crystallization and preliminary X-ray diffraction study of ferrocytochrome c2 from Rhodopseudomonas viridis. , 1986, Journal of molecular biology.

[24]  S. Woehler,et al.  Electrostatic and steric control of electron self-exchange in cytochromes c, c551, and b5. , 1989, Biophysical journal.

[25]  J. B. Matthew.  Electrostatic effects in proteins. , 1985, Annual review of biophysics and biophysical chemistry.

[26]  B. Durham,et al.  Photoinduced electron transfer between cytochrome c peroxidase and horse cytochrome c labeled at specific lysines with (dicarboxybipyridine)(bisbipyridine)ruthenium(II) , 1992, Biochemistry.

[27]  J. Deisenhofer,et al.  The photosynthetic reaction center from the purple bacterium Rhodopseudomonas viridis and its relevance to photosystem II , 1989 .

[28]  B. Lou,et al.  Proton NMR comparison of noncovalent and covalently cross-linked complexes of cytochrome c peroxidase with horse, tuna, and yeast ferricytochromes c. , 1992, Biochemistry.

[29]  S. Harvey.  Treatment of electrostatic effects in macromolecular modeling , 1989, Proteins.

[30]  A. Verméglio,et al.  Electron transfer between primary and secondary donors in Rhodospirillum rubrum: evidence for a dimeric association of reaction centers. , 1990, Biochemistry.

[31]  R. Huber,et al.  Structural homology of reaction centers from Rhodopseudomonas sphaeroides and Rhodopseudomonas viridis as determined by x-ray diffraction. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[32]  Kurt Wüthrich,et al.  Secondary structure of the α-amylase polypeptide inhibitor Tendamistat from Streptomyces tendae determined in solution by 1H nuclear magnetic resonance , 1985 .

[33]  M K Gilson,et al.  Energetics of charge–charge interactions in proteins , 1988, Proteins.

[34]  D. Tiede,et al.  Assessment of the Role of Electrostatics in the Assembly of Reaction Center-Cytochrome C Electron Transfer Complexes , 1991 .

[35]  M. Okamura,et al.  Role of specific lysine residues in binding cytochrome c2 to the Rhodobacter sphaeroides reaction center in optimal orientation for rapid electron transfer. , 1989, Biochemistry.

[36]  G. Mclendon,et al.  Interprotein Electron Transfer , 1992 .

[37]  G. Mclendon.  Control of biological electron transport via molecular recognition and binding: The “velcro” model , 1991 .

[38]  O. El-Kabbani,et al.  Structure of the membrane-bound protein photosynthetic reaction center from Rhodobacter sphaeroides. , 1991, Biochemistry.

[39]  T. Meyer,et al.  New perspectives on c-type cytochromes. , 1982, Advances in protein chemistry.

[40]  D. Tiede.  Cytochrome c orientation in electron-transfer complexes with photosynthetic reaction centers of Rhodobacter sphaeroides and when bound to the surface of negatively charged membranes: characterization by optical linear dichroism , 1987 .

[41]  S. Sligar,et al.  Probing the mechanisms of macromolecular recognition: the cytochrome b5-cytochrome c complex. , 1988, Science.

[42]  B. Honig,et al.  A rapid finite difference algorithm, utilizing successive over‐relaxation to solve the Poisson–Boltzmann equation , 1991 .

[43]  G. Bhatia.  Refinement of the Crystal Structure of Oxidized Rhodospirillum Rubrum Cytochrome C2 , 1984 .

[44]  M. Gunner.  The Reaction Center Protein from Purple Bacteria: Structure and Function , 1991 .

[45]  R. Dickerson,et al.  Structure of cytochrome c551 from Pseudomonas aeruginosa refined at 1.6 A resolution and comparison of the two redox forms. , 1982, Journal of molecular biology.

[46]  P. Joliot,et al.  Evidence for supercomplexes between reaction centers, cytochrome c2 and cytochrome bc1 complex in Rhodobacter sphaeroides whole cells , 1989 .

[47]  Chong-Hwan Chang,et al.  The Cytochrome-c Binding Surface of Reaction Centers from Rhodobacter sphaeroides , 1988 .

[48]  R. van Grondelle,et al.  Oxidation of cytochrome c2 and of cytochrome c by reaction centers of Rhodospirillum rubrum and Rhodobacter sphaeroides. The effect of ionic strength and of lysine modification on oxidation rates. , 1987, Biochimica et biophysica acta.

[49]  M. Cusanovich,et al.  The kinetics of photooxidation of c-type cytochromes by Rhodospirillum rubrum reaction centers. , 1979, Archives of biochemistry and biophysics.

[50]  G. Tollin,et al.  Electrostatic interactions during electron transfer reactions between c-type cytochromes and flavodoxin. , 1985, The Journal of biological chemistry.

[51]  G. Moore,et al.  NMR characterization of surface interactions in the cytochrome b5-cytochrome c complex. , 1990, Science.

[52]  B Honig,et al.  Electrostatic control of midpoint potentials in the cytochrome subunit of the Rhodopseudomonas viridis reaction center. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[53]  S. Schichman,et al.  A reassessment of the structure of Paracoccus cytochrome c-550. , 1981, Journal of molecular biology.

[54]  T O Yeates,et al.  Structure of the reaction center from Rhodobacter sphaeroides R-26: membrane-protein interactions. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[55]  S. Sligar,et al.  Genetic engineering of redox donor sites: measurement of intracomplex electron transfer between ruthenium-65-cytochrome b5 and cytochrome c. , 1992, Biochemistry.

[56]  S H Northrup,et al.  Brownian dynamics of cytochrome c and cytochrome c peroxidase association. , 1988, Science.

[57]  T. Poulos,et al.  Kinetics of reduction by free flavin semiquinones of the components of the cytochrome c-cytochrome c peroxidase complex and intracomplex electron transfer. , 1987, Biochemistry.

[58]  G J Williams,et al.  The Protein Data Bank: a computer-based archival file for macromolecular structures. , 1977, Journal of molecular biology.

[59]  L. K. Hanson,et al.  Redox pathways in electron-transfer proteins: correlations between reactivities, solvent exposure, and unpaired-spin-density distributions. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[60]  J. Wendoloski,et al.  Electrostatic field around cytochrome c: theory and energy transfer experiment. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[61]  P. Dutton,et al.  Cytochrome c and c2 binding dynamics and electron transfer with photosynthetic reaction center protein and other integral membrane redox proteins. , 1988, Biochemistry.

[62]  A. Kriauciunas,et al.  Reaction of cytochrome c2 with photosynthetic reaction centers from Rhodopseudomonas viridis. , 1991, Biochemistry.

[63]  N. Xuong,et al.  The structure of oxidized cytochrome c 2 of Rhodospirillum rubrum. , 1976, The Journal of biological chemistry.

[64]  A. Ducruix,et al.  Structure of the detergent phase and protein-detergent interactions in crystals of the wild-type (strain Y) Rhodobacter sphaeroides photochemical reaction center. , 1991, Biochemistry.

[65]  E. Margoliash,et al.  The asymmetric distribution of charges on the surface of horse cytochrome c. Functional implications. , 1982, The Journal of biological chemistry.

[66]  T O Yeates,et al.  Structure of the reaction center from Rhodobacter sphaeroides R-26: the protein subunits. , 1987, Proceedings of the National Academy of Sciences of the United States of America.