Protein dielectric environment modulates the electron-transfer pathway in photosynthetic reaction centers.
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.