Modeling Electron Transfer in Biochemistry: A Quantum Chemical Study of Charge Separation in <i>Rhodobacter </i><i>s</i><i>phaeroides</i> and Photosystem II

Abstract

High-level quantum chemical methods (hybrid density-functional type) are applied to the light-driven charge-separation process in the photosynthetic reaction centers of both bacteria and photosystem II in green plants. Structural information on the bacterial system provides the basis for choosing the models used in the calculations. The energetics of the electron transfer from the (bacterio)chlorophyll to the quinone are calculated as well as those of the intermediate step involving the (bacterio)pheophytin. The surrounding protein is treated as a dielectric medium, and the cavities around the solute molecules are determined by isodensity surfaces. The dielectric effects on the charge-separation processes are calculated to be as large as 50 kcal/mol. It is shown that hydrogen bonding between the chromophores and certain peptide residues as well as the axial histidine ligand on the (bacterio)chlorophylls contributes substantially to the energetics. Good agreement with experimentally estimated driving forces of the different steps is obtained within 2 kcal/mol for the bacteriosystem and within 8 kcal/mol for photosystem II. The results for photosystem II have a lower accuracy, as expected, due to the lack of detailed structural information on this system. Recent low-resolution data indicating a weaker coupling between the chlorophylls in P680 as compared to that of the special pair in the bacterial systems are taken into account in the calculations. In the bacterial system, charge separation to the accessory bacteriochlorophyll is essentially thermoneutral and the P865+BPheo- state is stable by 7.5 kcal/mol. In photosystem II, charge separation to the P680+Pheo- state is much less strongly driven, and the absence of an axial histidine ligand to the accessory chlorophyll appears necessary to allow its formation. The creation of the tyrosine radical (YZ) by proton-coupled electron transfer to the photoionized reaction center chlorophyll in photosystem II is also studied. In this case as well, hydrogen bonding to other peptide residues plays an important role in the overall energetic balance of the reaction.