Monitoring the Reaction Process During the S₂ → S₃ Transition in Photosynthetic Water Oxidation Using Time-Resolved Infrared Spectroscopy

Abstract

Photosynthetic water oxidation performed at the MnCaO cluster in photosystem II plays a crucial role in energy production as electron and proton sources necessary for CO fixation. Molecular oxygen, a byproduct, is a source of the oxygenic atmosphere that sustains life on earth. However, the molecular mechanism of water oxidation is not yet well-understood. In the reaction cycle of intermediates called S states, the S → S transition is particularly important; it consists of multiple processes of electron transfer, proton release, and water insertion, and generates an intermediate leading to O-O bond formation. In this study, we monitored the reaction process during the S → S transition using time-resolved infrared spectroscopy to clarify its molecular mechanism. A change in the hydrogen-bond interaction of the oxidized Y radical, an immediate electron acceptor of the MnCaO cluster, was clearly observed as a ∼100 μs phase before the electron-transfer phase with a time constant of ∼350 μs. This observation provides strong experimental evidence that rearrangement of the hydrogen-bond network around Y, possibly due to the movement of a water molecule located near Y to the Mn site, takes place before the electron transfer. The electron transfer was coupled with proton release, as revealed by a relatively high deuterium kinetic isotope effect of 1.9. This proton release, which decreases the redox potential of the MnCaO cluster to facilitate electron transfer to Y, was proposed to determine, as a rate-limiting step, the relatively slow electron-transfer rate of the S → S transition.

Five-coordinate Mn IV intermediate in the activation of nature’s water splitting cofactor

“…The fast 30-μs kinetic phase is attributed to deprotonation of the cluster, with the slow 350-μs phase representing structural rearrangement, e.g., water insertion and cofactor oxidation. A more recent FTIR study suggests that deprotonation may also occur during the slow 350-μs phase (19). In either case, theoretical calculations support the notion that cofactor oxidation only proceeds via redox tuning (deprotonation) of the cofactor.…”

“…In the next state, S 3 , the net oxidation state of the cofactor is all (Mn IV ) 4 . Electron paramagnetic resonance (EPR) (16), X-ray absorption spectroscopy (XAS) and X-ray emission spectroscopy (XES) (17,18), Fourier transform infrared (FTIR) (19,20), and recent XFEL data (8,21) suggest that in this S state, all 4 Mn ions are octahedral, requiring the insertion of a new water molecule into the cofactor. Structural models of the cofactor in the S 3 state more closely resemble the preceding S 2 A form compared with the S 2 B form, with an additional oxygen (most likely hydroxide) ligand at Mn1 (8,14,16,21) (Fig.…”

Structural isomers of the S2 state in photosystem II: do they exist at room temperature and are they important for function?

“…The W20 density is already weak in the dark state in comparison to other waters, indicating its higher mobility or lower occupancy. It is likely that the overall changes observed above are a consequence of the oxidation of Mn4 from +3 to +4 in the S 1 to S 2 transition and the connected increase in charge of the cluster (Klauss et al , Sakamoto et al ). Thus, we speculate that the structural changes observed in the W20 region are a consequence of charge compensation around the OEC.…”

D1-Asn-298 in photosystem II is involved in a hydrogen-bond network near the redox-active tyrosine YZ for proton exit during water oxidation

“…The recent X-ray free electron laser study for the S 3 -state showed the displacement of a water molecule near O4, suggesting the involvement of water molecules near O4 in proton transfer (21). The hydrogen-bond network near Y Z has also been suggested to be a proton pathway (16,17,42,43). Y Z form a hydrogen-bonded triad with D1-His-190 and D1-Asn-298, which is connected with a hydrogen-bond network leading to PsbV through D1-Asn-322 (designated "Y Z -Asn-298 path"; Fig.…”