ELECTRON-TRANSFER AND PROTEIN DYNAMICS IN THE PHOTOSYNTHETIC REACTION-CENTER

We have measured the kinetics of electron transfer (ET) from the prima ry quinone (Q(A)) to the special pair (P) of the reaction center (RC) complex from Rhodobacter sphaeroides as a function of temperature (5-3 00 K), illumination protocol (cooled in the dark and under illuminatio n from 110, 160, 180, and 280 K), and warming rate (1.3 and 13 mK/s). The nonexponential kinetics are interpreted with a quantum-mechanical ET model (Fermi's golden rule and the spin-boson model), in which hete rogeneity of the protein ensemble, relaxations, and fluctuations are c ast into a single coordinate that relaxes monotonically and is sensiti ve to all types of relaxations caused by ET. Our analysis shows that t he structural changes that occur in response to ET decrease the free e nergy gap between donor and acceptor states by 120 meV and decrease th e electronic coupling between donor and acceptor states from 2.7 x 10( -4) cm(-1) to 1.8 x 10(-4) cm(-1). At cryogenic temperatures, conforma tional changes can be slowed or completely arrested, allowing us to mo nitor relaxations on the annealing time scale (similar to 10(3)-10(4) s) as well as the time scale of ET (similar to 100 ms). The relaxation s occur within four broad tiers of conformational substates with avera ge apparent Arrhenius activation enthalpies of 17, 50, 78, and 110 kJ/ mol and preexponential factors of 10(13), 10(15), 10(21), and 10(25) s (-1), respectively. The parameterization provides a prediction of the time course of relaxations at all temperatures. At 300 K, relaxations are expected to occur from 1 ps to 1 ms, whereas at lower temperatures , even broader distributions of relaxation times are expected. The wea k dependence of the ET rate on both temperature and protein conformati on, together with the possibility of modeling heterogeneity and dynami cs with a single conformational coordinate, make RC a useful model sys tem for probing the dynamics of conformational changes in proteins.