Photosystem II (PSII) catalyzes water oxidation by capturing sunlight energy at the unique pair of Chlorophylls P680 within a picosecond time scale that initiates a serial reduction/oxidation reaction between two plastoquinone, QA, and QB, a radical active tyrosine YZ, a catalytic manganese cluster, and substrate water molecules. This reaction is the Kok cycle catalyzed by the Mn4CaO5 cluster, which incorporates an extra oxygen O6 in the S3-state to form a possible di-oxygen. The structural changes of the metal cluster and its environment during the Kok cycle have been examined at the millisecond time range. Here I will present the structural dynamics of PSII from nanoseconds to milliseconds after one or two flashes, which correspond to S1-S2 and S2-S3 transitions, respectively, using pump-probe serial femtosecond crystallography.
YZ, a tyrosine residue connecting the P680 and the Mn4CaO5 cluster, together with its surrounding amino acid residues and water molecules, showed structural changes at nanosecond and microsecond time ranges, reflecting the fast electron and proton transfer following flash illumination. Notably, one water molecule emerged and was bound to the Ca2+ ion in the sub-microsecond time after two flash illuminations, which disappeared later with the concomitant increase of O6, suggesting this water (O6*) is the origin of O6. There are concerted movements of water molecules in the O1- and O4-channels, protein residues, and even ligands to complete the electron transfer, proton release, and substrate water delivery. These results provide crucial insights into the molecular mechanisms of water oxidation in PSII.
References: Li H, Nature 626, 670-677 (2024).
Acknowledgment: I acknowledge many co-workers who cannot be listed due to the limited space. The work is a collaboration with several groups, including Shen Laboratory at Okayama University.