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 Mn 4 CaO 5 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 Mn 4 CaO 5 cluster showed a single phase with a time constant of ∼45 μs. A relatively small H/D kinetic isotope effect of ∼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 Mn 4 CaO 5 cluster gives rise to barrierless deprotonation upon S 1 formation through a strongly hydrogen-bonded water molecule.