O-O bond formation in the S4 state of the oxygen-evolving complex in photosystem II

Based on recent X-ray structures of the oxygen-evolving complex in photosystem II, quantum chemical geometry optimizations of several thousand structures have been performed in order to elucidate the mechanism for dioxygen formation. Many of the results of these calculations have been presented previously. The energetically most stable structure of the S-4 state has been used in the present study to investigate essentially all the possible ways the O-O bond can be formed in this structure. A key feature, emphasized previously, of the S-4 state is that an oxygen radical ligand is present rather than an Mn-V state. Previous studies have indicated that this oxygen radical can form an O-O bond by an attack from a water molecule in the second coordination shell. The present systematic investigation has led to a new type of mechanism that is significantly favored over the previous one. A calculated transition-state barrier of 12.5 kcal mol(-1) was found for this mechanism, whereas the best previous results gave 18-20 kcal mol(-1). A requirement on the spin alignment for a low barrier is formulated.