Electronic Couplings and Energy Transfer Dynamics in the Oxidized Primary Electron Donor of the Bacterial Reaction Center Xanthipe J. Jordanides,* ,²,§ Gregory D. Scholes, ², | Warwick A. Shapley, ‡ Jeffrey R. Reimers,* ,‡ and Graham R. Fleming ² Department of Chemistry, UniVersity of California, Berkeley, and Physical Biosciences DiVision, Lawrence Berkeley National Laboratory, Berkeley, California 94720, and School of Chemistry, The UniVersity of Sydney, NSW 2006, Australia ReceiVed: August 23, 2003; In Final Form: NoVember 6, 2003 It has been known for 30 years that the oxidized special pair radical cation P + is as efficient as the neutral ground-state species P in quenching excitation from the neighboring accessory bacteriochlorophylls B L and B M , but the mechanism for this process has remained elusive. Indeed, simple treatments based on application of standard Fo ¨ rster theory to the most likely acceptor candidate fails by 5 orders of magnitude in the prediction of the energy transfer rates to P + . We present a qualitative description of the electronic energy transfer (EET) dynamics that involves mixing of the strongly allowed transitions in P + with a manifold of exotic lower- energy transitions to facilitate EET on the observed time scale of 150 fs. This description is obtained using a three-step procedure. First, multireference configuration-interaction (MRCI) calculations are performed using the semiempirical INDO/S Hamiltonian to depict the excited states of P + . However, these calculations are qualitatively indicative but of insufficient quantitative accuracy to allow for a fully a priori simulation of the EET and so, second, the INDO results are used to establish a variety of scenarios, empirical parameters that are then fitted to describe a range of observed absorption and circular dichroism data. Third, EET according to these scenarios is predicted using a generalized Fo ¨rster theory that uses donor and acceptor transition densities, which together account for the large size of the chromophores in relation to the interchromophore spacings. The spectroscopic transitions of P + that facilitate the fast EET are thus unambiguously identified. I. Introduction The photosynthetic reaction center (RC) of purple bacteria is a pigment-protein complex present in the thylakoid mem- brane that, under low light intensity, efficiently accepts excitation energy either directly or from antenna complexes to initiate light- induced charge separation from the primary electron donor, a bacteriochlorophyll dimer (P); this is the first step in photo- synthesis. 1 The photoexcited dimer (P*) then transfers an electron to either bacteriopheophytin acceptors H L or H M within three picoseconds 2 and with a quantum yield of nearly one. 3 If, however, the RC is exposed to high light conditions or a chemical oxidant, the primary electron donor 4 P + is directly formed and electron transfer and, in turn, photosynthesis are blocked. The radical pair P + H - is then generated and decays in about 200 ps. Under high light intensity conditions, P* can quench excitation by rapid electronic energy transfer (EET) from higher energy RC pigments, either from the monomeric “ac- cessory” bacteriochlorophyll-a molecules (B L and B M ) or from the bacteriopheophytins (H L and H M ). 5-18 Four of the RC pigments are pictured in Figure 1. The absorption bleach of the accessory bacteriochlorophylls B, created by 800-nm light, recovers in ∼130 fs in the neutral RC due to fast EET. Throughout this manuscript, the term “neutral” is used to refer to the “unoxidized” reaction center. Remarkably, recovery also occurs in ∼150 fs in the oxidized RC. 9 In both cases, the ground- state recovery of the bacteriochlorophylls has been interpreted as arising following energy transfer to the special pair within the RC. It is hence clear that EET to the oxidized primary electron donor (from the accessory bacteriochlorophyll or from the antenna) still occurs, 5,8,9,19 despite the quite different natures of the acceptor states P and P + . Why the neutral RC and oxidized RC primary electron employed donors are equally efficient quenchers of the excita- tion has been an unanswered question for the past 30 years and has led to speculation that a unique EET mechanism is at work in the RC. The main goal of this paper is to understand the experimental observation that P + readily quenches the excitation * Correspondingauthors.E-mail: xjj2@cornell.edu;reimers@chem.usyd.edu.au ² University of California and LBNL. ‡ The University of Sydney. § Present address: School of Applied and Engineering Physics, Cornell University, Ithaca, New York 14853. | Present address: Lash Miller Chemical Laboratories, 80 St. George Street, University of Toronto, Toronto, Canada M5S 3H6. Figure 1. A view from the lumenal side of the membrane of the special pair of BChls; PM and PL and the accessory BChls, BL, and BM are shown. The arrows represent the approximate Qy transition dipole moments for the localized excited states, which are very different than the Qy directions taken from the QM/MM optimized structure. 20 1753 J. Phys. Chem. B 2004, 108, 1753-1765 10.1021/jp036516x CCC: $27.50 © 2004 American Chemical Society Published on Web 01/10/2004