Protein Dielectric Environment Modulates the Electron-Transfer Pathway in Photosynthetic Reaction Centers

Abstract

The replacement of tyrosine by aspartic acid at position M210 in the photosynthetic reaction center of Rhodobacter sphaeroides results in the generation of a fast charge recombination pathway that is not observed in the wild-type. Apparently, the initially formed charge-separated state (cation of the special pair, P, and anion of the A-side bacteriopheophytin, H(A)) can decay rapidly via recombination through the neighboring bacteriochlorophyll (B(A)) soon after formation. The charge-separated state then relaxes over tens of picoseconds and recombination slows to the hundreds-of-picoseconds or nanosecond timescale. This dielectric relaxation results in a time-dependent blue shift of B(A)(-) absorption, which can be monitored using transient absorbance measurements. Protein dynamics also appear to modulate the electron transfer between H(A) and the next electron carrier, Q(A) (a ubiquinone). The kinetics of this reaction are complex in the mutant, requiring two kinetic terms, and the spectra associated with the two terms are distinct; a red shift of the H(A) ground-state bleaching is observed between the shorter and longer H(A)-to-Q(A) electron-transfer phases. The kinetics appears to be pH-independent, suggesting a negligible contribution of static heterogeneity originating from protonation/deprotonation in the ground state. A dynamic model based on the energy levels of the two early charge-separated states, P(+)B(A)(-) and P(+)H(A)(-), has been developed in which the energetics of these states is modulated by fast protein dielectric relaxations and this in turn alters both the kinetic complexity of the reaction and the reaction pathway.

Putative Hydrogen Bond to Tyrosine M208 in Photosynthetic Reaction Centers from Rhodobacter capsulatus Significantly Slows Primary Charge Separation

“…Heterogeneous kinetics in wild-type RCs have been ascribed to pigment/protein conformers or populations 66 , 88 and links between protein dynamics and ET have been much discussed. 29 , 64 , 89 The presence, position, and orientation of water molecules may contribute, 1 , 2 such as one (“water-A”) that may bridge the His (M202, equiv of M200 in Rb. capsulatus ) ligand on P M and B A via hydrogen bonds, and that has been the subject of much recent study.…”

Temperature dependence of nanosecond charge recombination in mutant Rhodobacter sphaeroides reaction centers: modelling of the protein dynamics

“…This is because ET can be easily followed by transient absorption measurements due to strong light absorption by the ET cofactors (pigments) that are embedded inside these proteins and which interact with nearby amino acid residues. There is increasing evidence from theoretical predictions [1][2][3][4][5] and experimentation [6][7][8][9] that the local protein dynamics affect the rate constants of intra-protein ET. Such protein dynamics are spread over very broad range of time scales, from picoseconds to seconds [10], matching the time range of ET reactions in photosynthetic proteins [11][12][13][14].…”

Assemblies of Boron Dipyrromethene/Porphyrin, Phthalocyanine, and C60 Moieties as Artificial Models of Photosynthesis: Synthesis, Supramolecular Interactions, and Photophysical Studies

“…The photoinduced EET processes of the covalent conjugates [ZnPc(BODIPY) n ] and [ZnPc(H 2 Por) n ] ( n =2, 4) were studied in the polar benzonitrile by various steady‐state and time‐resolved spectroscopic methods. For the supramolecular tetrads [ZnPc(BODIPY) 2 :C 60 Im] and [ZnPc(H 2 Por) 2 :C 60 Im], the photophysical properties were examined in less polar toluene based on the fact that the protein environment surrounding the photosynthetic reaction center is nonpolar with a low dielectric constant ( ϵ ) of approximately 2.25 …”