Coherent Nuclear and Electronic Dynamics in Primary Charge Separation in Photosynthetic Reaction Centers:  A Redfield Theory Approach

Abstract

Primary charge separation dynamics is modeled in the pheophytin-modified Rhodobacter sphaeroides R-26 reaction center (RC). To explain the observed spectral evolution, it is assumed that the process is coupled to coherent nuclear motion. A density matrix equation with the Redfield relaxation superoperator is used for simulation of the electron-vibrational dynamics and its spectral signatures. The model includes two diabatic states, i.e., an excited state P* of the primary donor (i.e., special pair, P), and a charge-transfer state (P+B-, which is the primary photoproduct in the pheophytin-modified RC). The strong coupling of these states with two collective nuclear modes is supposed. The mixing of diabatic states (with different displacements along each of the two nuclear coordinates) results in a complicated potential surface that determines the dynamics of the excited-state wave packet. The coupled nuclear and charge-transfer dynamics is calculated in the basis of vibronic eigenstates obtained by numerical diagonalization of the electron-vibrational Hamiltonian. The third-order nonlinear response associated with excited-state dynamics is calculated, including the P* → P stimulated emission (SE) and the P+B- → P+(B-)* excited-state absorption (ESA). The model allowed us to obtain a quantitative fit of the experimental kinetics of the SE near 900−950 nm and the ESA in the 1020-nm region of the pheophytin-modified Rhodobacter sphaeroides R-26 RC (Yakovlev, A. G.; Shkuropatov, A. Ya.; Shuvalov, V. A. FEBS Lett. 2000, 466, 209). By use of the parameters adjusted from the fit, we have obtained a direct visualization of the electron-vibrational wave packet evolution, including the surface-crossing dynamics superimposed with oscillatory motion along two reaction coordinates in the P* and P+B- states. It is concluded that nonequilibrated vibrational modes involved in electron-transfer play an important role in photoproduct formation in bacterial RC. We found that the specific configuration of two vibrational coordinates (obtained from the modeling) determines high efficiency of charge separation both for coherent and noncoherent excitation.