Photoinduced electron transfer in ruthenium-modified cytochrome c

Abstract

Distant heme-Ru electronic couplings have been extracted from intramolecular electron-transfer rates in Ru(histidine-X) (X=33,39,62) derivatives of cytochrome c. The rates (and the couplings) correlate with the lengths of u-tunneling pathways comprised of covalent bonds, hydrogen bonds, and through-space jumps from the histidines to the heme group.The electron-transfer (ET) reactions that occur within and between proteins typically involve prosthetic groups separated by distances that are often greater than 10 A. An understanding of how the intervening medium, driving force, and nuclear reorganization energetics and dynamics modulate protein ET reactions has been a central goal of our research program. In recent years, we have been examining the rates of electron transfer between surface-bound ruthenium complexes and metalloprotein active sites.' This work has provided a considerable capacity for predicting protein ET rates.We have been guided by semiclassical ET theory, which describes the rate constant for nonadiabatic reaction between a donor and acceptor held at fixed distance and orientatiox2The tunneling matrix element HAD is a measure of the electronic coupling between the reactants and the products at the transition state. The magnitude of HAD depends upon donor-acceptor separation, orientation, and the nature of the intervening medium. The exponential term in Eq. 1 reflects the interplay between reaction driving force (-AGO) and nuclear reorganization energy (A). Various approaches have been used to test the validity of Eq. 1, and to extract the ET parameters HAD and A. Driving-force studies have proven to be a reliable approach, and such studies have been emphasized in our own work.In the nonadiabatic limit, the probability is quite low that reactants will cross over to products at the transition-state configuration.' This probability depends upon the electronic hopping frequency (determined by HAD) and upon the frequency of motion along the reaction ~oordinate.~ When solvent reorientation dominates A, the nuclear reorientation timescale is believed to be given by the solvent longitudinal dielectric relaxation time, T~. The nonadiabatic limit for ET results when HA; a {A,fi/4?r7L}'*.3 Water reorients very rapidly ( T~ = 0.5 ps4) and the solvent-controlled adiabatic limit results when HAD B 80 cm-'. Conversely, when HAD 4 80 cm-', Eq. 1 should adequately describe the ET kinetics. Reorientation of the peptide matrix introduces complications in protein ET. Timescales for this nuclear motion are much slower than the 7L for water.s In situations where slow peptide motions dominate A, much smaller values of HA, are necessary to achieve the "solvent-controlled'' adiabatic limit.In simple models, the electronic-coupling strength is predicted to decay exponentially with increasing donor-acceptor separation (Eq. 2):286In Eq. 2, HADo is the electronic coupling at close contact (do), and P is the rate of decay of coupling with distance (a). Studies of the distance dependence of ET rates in donor-acceptor...

Bimolecular Electron Transfer in the Marcus Inverted Region

“…The distance dependence of V is exponential and given by 86 where d is the edge-to-edge distance between the Ru II diimine and the heme of the protein and acceptor and V (0) is the value of V at d = d 0 , which has been defined to be 3 Å to account for the electron clouds about the outermost atoms of each reactant. 47a, For cyt c , β is 1.2 Å -1 and V (0) is 200 cm -1 . 47a,, It is well established that the ET reactions of cationic metal complexes featuring hydrophobic ligation spheres proceed at the exposed heme edge of the protein. , Singly modified peptide and NMR studies show that positively charged reactants access the recessed heme edge near Lys-27, ,, thereby permitting us to relate the edge-to-edge ET distance, d , in eq 10, to the protein and Ru II diimine center-to-center distance, r . The distance from the outermost meso position of the heme to the center of the protein, determined from the crystal structure of cyt c , corresponds to 9.1 Å .…”

“…47a,86 For cyt c, β is 1.2 Å -1 and V(0) is 200 cm -1 . 47a, 51,89 It is well established that the ET reactions of cationic metal complexes featuring hydrophobic ligation spheres proceed at the exposed heme edge of the protein. 90,91 Singly modified peptide and NMR studies show that positively charged reactants access the recessed heme edge near Lys-27, 70,71,92 thereby permitting us to relate the edge-to-edge ET distance, d, in eq 10, to the protein and Ru II diimine center-to-center distance, r. The distance from the outermost meso position of the heme to the center of the protein, determined from the crystal structure of cyt c, corresponds to 9.1 Å.…”

Multi-Heme Self-Assembly in Phospholipid Vesicles

“…In such a case, the lack of a terminal imidazole in the linker would not prevent electron transfer to the surface-docked cytochrome c . On the other hand, if the tether were the main electron transfer pathway, the lack of ligation and the resulting spacial registration would decrease the efficiency of electron transfer significantly.…”

Theoretical analyses of the fluorescence lifetimes of thed-amino acid oxidase–benzoate complex dimer from porcine kidney: molecular dynamics simulation and photoinduced electron transfer

“…The original Marcus theory 42,43 has been modied in various ways. [44][45][46][47][48] In the present analysis, KM theory 47 was used, because it is applicable for both non-adiabatic ET processes and adiabatic ET processes, and has been found to give satisfactory results for both static, 27,33,35,36 and dynamic ET analyses. [28][29][30][31][32] When the donor is Trp or Tyr, the ET rate described by the KM theory is expressed by eqn (1).…”