Role of D1-Glu65 in Proton Transfer during Photosynthetic Water Oxidation in Photosystem II

• Published in: The journal of physical chemistry. B 2022-10, Vol.126 (41), p.8202-8213
• Main Authors: Shimada, Yuichiro, Sugiyama, Ayane, Nagao, Ryo, Noguchi, Takumi
• Format: Article
• Language: English
• Subjects: B: Biophysical and Biochemical Systems and Processes; Manganese - chemistry; Oxidation-Reduction; Oxygen - metabolism; Photosystem II Protein Complex - chemistry; Protons; Spectroscopy, Fourier Transform Infrared - methods; Water - chemistry
• ISSN: 1520-6106; 1520-5207
• DOI: 10.1021/acs.jpcb.2c05869

Photosynthetic water oxidation takes place at the Mn4CaO5 cluster in photosystem II (PSII) through a light-driven cycle of five intermediates called S states (S0–S4). Although the PSII structures have shown the presence of several channels around the Mn4CaO5 cluster leading to the lumen, the pathways for proton release in the individual S-state transitions remain unidentified. Here, we studied the involvement of the so-called Cl channel in proton transfer during water oxidation by examining the effect of the mutation of D1-Glu65, a key residue in this channel, to Ala using Fourier transform infrared difference and time-resolved infrared spectroscopies together with thermoluminescence and delayed luminescence measurements. It was shown that the structure and the redox property of the catalytic site were little affected by the D1-Glu65Ala mutation. In the S2 → S3 transition, the efficiency was still high and the transition rate was only moderately retarded in the D1-Glu65Ala mutant. In contrast, the S3 → S0 transition was significantly inhibited by this mutation. These results suggest that proton transfer in the S2 → S3 transition occurs through multiple pathways including the Cl channel, whereas this channel likely serves as a single pathway for proton exit in the S3 → S0 transition.