Proton Displacements Coupled to Primary Electron Transfer in the <i>Rhodobacter sphaeroides</i> Reaction Center

Using first-principles molecular dynamics (AIMD) and constrained density functional theory (CDFT) we identify the pathway of primary electron transfer in the <i>R</i>. <i>Sphaeroides</i> reaction center from the special pair excited state (P*) to the accessory bacteriochlorophyll (B_A). Previous AIMD simulations on the special pair (P_LP_M) predicted a charge-transfer intermediate formation through the excited-state relaxation along a reaction coordinate characterized by the rotation of an axial histidine (HisM202). To account for the full electron transfer we extend the model to include the primary acceptor B_A. In this extended model, the LUMO is primarily localized on the acceptor B_A and extends over an interstitial water (water A) that is known to influence the rate of electron transfer (Potter et al. <i>Biochemistry</i> <b>2005</b> <i>280</i>, 27155–27164). A vibrational analysis of the dynamical trajectories gives a frequency of 30–35 cm^–1 for a molecular motion involving the hydrogen-bond network around water A, in good agreement with experimental findings (Yakovlev et al. <i>Biochemistry</i>, <b>2003</b>, <i>68</i>, 603–610). In its binding pocket water A can act as a switch by breaking and forming hydrogen bonds. With CDFT we calculate the energy required to the formation of the charge-separated state and find it to decrease along the predicted anisotropic reaction coordinate. Furthermore, we observe an increased coupling between the ground and charge-separated state. Water A adapts its hydrogen-bonding network along this reaction coordinate and weakens the hydrogen bond with HisM202. We also present AIMD simulations on the radical cation (P^•+) showing a weakening of the hydrogen bond between HisL168 and the 3¹-acetyl of P_L. This work demonstrates how proton displacements are crucially coupled to the primary electron transfer and characterizes the reaction coordinate of the initial photoproduct formation