Effects of distance and driving force on photoinduced electron transfer between photosynthetic reaction centers and gold electrodes

The electron-transfer (ET) parameters for oriented and aligned monolayers of the bacterial photosynthetic reaction center (RC) from Rhodobacter sphaeroides formed on the top of self-assembled monolayers (SAMs) of alkanethiols of various lengths immobilized on gold electrode are estimated using cyclic voltammetry and photoelectrochemistry. Utilization of the unique polyHis tag in the protein and the Ni−NTA chelator complex in SAMs allows for specific protein orientation with the RC primary donor facing the electrode. To improve the efficiency of ET between the RC special pair and the electrode, an RC-Cyt complex was formed (J. Am. Chem. Soc. 2006, 128, 12044−12045). The results are analyzed in terms of integrated Marcus formalism, taking into account the density of electronic states in the metal. The dependence of the ET rate on the distance between RC and electrode demonstrates an adiabatic region up to 10 A, typical for other proteins, followed by a nonadiabatic area of electron tunneling with a β-factor...

[1]  G M Whitesides,et al.  A self-assembled monolayer for the binding and study of histidine-tagged proteins by surface plasmon resonance. , 1996, Analytical chemistry.

[2]  George M. Whitesides,et al.  Structures of self-assembled monolayer films of organosulfur compounds adsorbed on gold single crystals: electron diffraction studies , 1988 .

[3]  R. Marcus,et al.  Electron transfers in chemistry and biology , 1985 .

[4]  David N. Reinhoudt,et al.  Sensor functionalities in self-assembled monolayers , 2000 .

[5]  Sergio Marco,et al.  Nanodissection and high-resolution imaging of the Rhodopseudomonas viridis photosynthetic core complex in native membranes by AFM , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[6]  Christopher C. Moser,et al.  Natural engineering principles of electron tunnelling in biological oxidation–reduction , 1999, Nature.

[7]  J. Kong,et al.  PROBING ELECTRON TRANSFER OF THE REDOX SPECIES IN WILD-TYPE RC PROTEIN AND ITS PIGMENT-REPLACED MUTANTS RE-CONSTITUTED IN SELF-ASSEMBLY MONOLAYERS , 2001 .

[8]  George M. Whitesides,et al.  Redox Properties of Cytochrome c Adsorbed on Self-Assembled Monolayers: A Probe for Protein Conformation and Orientation , 2002 .

[9]  V. Shuvalov,et al.  COUPLING OF PHOTOINDUCED CHARGE SEPARATION IN REACTION CENTERS OF PHOTOSYNTHETIC BACTERIA WITH ELECTRON-TRANSFER TO A CHEMICALLY MODIFIED ELECTRODE , 1989 .

[10]  Electron transfer in gel-immobilized photosynthetic reaction centers , 1997 .

[11]  M. Gunner,et al.  Trapping conformational intermediate states in the reaction center protein from photosynthetic bacteria. , 2001, Biochemistry.

[12]  Nikolai Lebedev,et al.  Integration of Photosynthetic Protein Molecular Complexes in Solid-State Electronic Devices , 2004 .

[13]  David A. Russell,et al.  Self-assembled monolayers: a versatile tool for the formulation of bio-surfaces , 2000 .

[14]  Igor Griva,et al.  Conductive wiring of immobilized photosynthetic reaction center to electrode by cytochrome C. , 2006, Journal of the American Chemical Society.

[15]  S. Boxer,et al.  Rapid isolation of bacterial photosynthetic reaction centers with an engineered poly-histidine tag , 1996 .

[16]  D. Kleinfeld,et al.  Electron-transfer kinetics in photosynthetic reaction centers cooled to cryogenic temperatures in the charge-separated state: evidence for light-induced structural changes. , 1984, Biochemistry.

[17]  L. Arnaut,et al.  Theory of electron transfer reactions in photosynthetic bacteria reaction centers , 1997 .

[18]  R. Murray,et al.  Cyclic Voltammetric Analysis of Ferrocene Alkanethiol Monolayer Electrode Kinetics Based on Marcus Theory , 1994 .

[19]  V. Sundström,et al.  Light in elementary biological reactions , 2000 .

[20]  Daniel J Müller,et al.  Imaging and manipulation of biological structures with the AFM. , 2002, Micron.

[21]  Yukari Sato,et al.  Electrochemical properties of the 2-mercaptohydroquinone monolayer on a gold electrode. Effect of solution pH, adsorption time and concentration of the modifying solution , 1996 .

[22]  F. Armstrong,et al.  Electron-transfer mechanisms through biological redox chains in multicenter enzymes. , 2002, Journal of the American Chemical Society.

[23]  H. Frank,et al.  Electron transfer reactions of redox cofactors in spinach photosystem I reaction center protein in lipid films on electrodes. , 2003, Journal of the American Chemical Society.

[24]  M. Mrksich,et al.  Diels-Alder Reaction for the Selective Immobilization of Protein to Electroactive Self-Assembled Monolayers , 1999 .

[25]  C. Chidsey,et al.  Free Energy and Temperature Dependence of Electron Transfer at the Metal-Electrolyte Interface , 1991, Science.

[26]  Allen J. Bard,et al.  Electrochemical Methods: Fundamentals and Applications , 1980 .

[27]  Daniel A. Lowy,et al.  Miniaturized Reference Electrodes. II. Use in Corrosive, Biological, and Organic Media , 2004 .

[28]  Michael J. Tarlov,et al.  Electron-transfer reaction of cytochrome c adsorbed on carboxylic acid terminated alkanethiol monolayer electrodes , 1991 .

[29]  Igor Griva.  Numerical Experiments with an Interior-Exterior Point Method for Nonlinear Programming , 2004, Comput. Optim. Appl..

[30]  D. Waldeck,et al.  Charge-transfer mechanism for cytochrome c adsorbed on nanometer thick films. Distinguishing frictional control from conformational gating. , 2003, Journal of the American Chemical Society.

[31]  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.

[32]  J. Onuchic,et al.  Tunneling pathway and redox-state-dependent electronic couplings at nearly fixed distance in electron transfer proteins , 1992 .

[33]  Peter Hildebrandt,et al.  Electron-transfer processes of cytochrome C at interfaces. New insights by surface-enhanced resonance Raman spectroscopy. , 2004, Accounts of chemical research.

[34]  Ida Lee,et al.  Biomolecular Electronics: Vectorial Arrays of Photosynthetic Reaction Centers , 1997 .

[35]  V. Budavári,et al.  Noncovalently bonded quinone on self-assembled molecular layers , 2002 .

[36]  Insung S. Choi,et al.  Grafting Nitrilotriacetic Groups onto Carboxylic Acid-Terminated Self-Assembled Monolayers on Gold Surfaces for Immobilization of Histidine-Tagged Proteins , 2004 .

[37]  Nikolai Lebedev,et al.  Effect of protein orientation on electron transfer between photosynthetic reaction centers and carbon electrodes. , 2006, Biosensors & bioelectronics.

[38]  F. Mavelli,et al.  Kinetics of the quinone binding reaction at the QB site of reaction centers from the purple bacteria Rhodobacter sphaeroides reconstituted in liposomes. , 2003, European journal of biochemistry.

[39]  B. Limoges,et al.  Dense monolayers of metal-chelating ligands covalently attached to carbon electrodes electrochemically and their useful application in affinity binding of histidine-tagged proteins. , 2005, Langmuir : the ACS journal of surfaces and colloids.

[40]  J. Kong,et al.  Photoelectric conversion of photosynthetic reaction center in multilayered films fabricated by layer-by-layer assembly , 2002 .

[41]  Michael P. Timko,et al.  POR structural domains important for the enzyme activity in R. capsulatus complementation system , 2004, Photosynthesis Research.

[42]  H. Frank,et al.  Electrochemical reactions of redox cofactors in Rhodobacter sphaeroides reaction center proteins in lipid films. , 2001, Bioelectrochemistry.

[43]  Alan S. Haas,et al.  Cytochrome c and Cytochrome c Oxidase: Monolayer Assemblies and Catalysis , 2001 .

[44]  H. Frank,et al.  Fast reversible electron transfer for photosynthetic reaction center from wild type Rhodobacter sphaeroides re-constituted in polycation sandwiched monolayer film. , 1999, Bioelectrochemistry and bioenergetics.

[45]  I. Willner,et al.  Vectorial photoinduced electron-transfer in tailored redox-active proteins and supramolecular nanoparticle arrays , 2003 .

[46]  J. Kong,et al.  Photoelectrochemistry of photosynthetic reaction centers embedded in Al2O3 gel , 2002 .

[47]  F. Armstrong.  Applications of voltammetric methods for probing the chemistry of redox proteins , 1997 .

[48]  Ranganathan Shashidhar,et al.  Orientated binding of photosynthetic reaction centers on gold using Ni-NTA self-assembled monolayers. , 2004, Biosensors & bioelectronics.

[49]  G. Feher,et al.  Determination of proton transfer rates by chemical rescue: application to bacterial reaction centers. , 2002, Biochemistry.

[50]  G. Whitesides,et al.  Formation of monolayer films by the spontaneous assembly of organic thiols from solution onto gold , 1989 .

[51]  James F. Allen,et al.  Specific alteration of the oxidation potential of the electron donor in reaction centers from Rhodobacter sphaeroides. , 1994, Proceedings of the National Academy of Sciences of the United States of America.