Mechanism of Proton-Coupled Electron Transfer in the S0-to-S1 Transition of Photosynthetic Water Oxidation As Revealed by Time-Resolved Infrared Spectroscopy

Photosynthetic water oxidation takes place at the Mn4CaO5 cluster in photosystem II through a light-driven cycle of intermediates called S states (S-0-S-4). To unravel the mechanism of water oxidation, it is essential to understand the coupling of electron- and proton-transfer reactions during the S-state transitions. Here, we monitored the reaction process in the S-0 -> S-1 transition using time-resolved infrared (TRIR) spectroscopy. The TRIR signals of the pure contribution of the S-0 -> S-1 transition was obtained by measurement upon a flash after dark adaptation following three flashes. The S-0 -> S(1 )traces at the vibrational frequencies of carboxylate groups and hydrogen bond networks around the Mn4CaO5 cluster showed a single phase with a time constant of similar to 45 mu s. A relatively small H/D kinetic isotope effect of similar to 1.2 together with the absence of a slower phase suggests that proton release is coupled with electron transfer, which is a rate-limiting step. The high rate of proton-coupled electron transfer, which is even higher than pure electron transfer in the S-1 -> S-2 transition, is consistent with the previous theoretical prediction that a hydroxo bridge of the Mn4CaO5 cluster gives rise to barrierless deprotonation upon S-1 formation through a strongly hydrogen-bonded water molecule.