Protonation State of a Key Histidine Ligand in the Iron–Quinone Complex of Photosystem II as Revealed by Light-Induced ATR-FTIR Spectroscopy

• Published in: Biochemistry (Easton) Vol. 59; no. 45; pp. 4336 - 4343
• Main Authors: Kimura, Masakazu, Kato, Yuki, Noguchi, Takumi
• Format: Journal Article
• Language: English
• Published: United States American Chemical Society 17.11.2020
• Subjects: Histidine - chemistry; Histidine - metabolism; Iron - chemistry; Ligands; Light; Models, Molecular; Organometallic Compounds - chemistry; Organometallic Compounds - metabolism; Photosystem II Protein Complex - chemistry; Photosystem II Protein Complex - metabolism; Protein Binding; Protein Conformation; Protons; Quinones - chemistry; Spectroscopy, Fourier Transform Infrared
• ISSN: 0006-2960; 1520-4995
• DOI: 10.1021/acs.biochem.0c00810

The iron–quinone complex in photosystem II (PSII) consists of the two plastoquinone electron acceptors, QA and QB, and a non-heme iron connecting them. It has been suggested that nearby histidine residues play important roles in the electron and proton transfer reactions of the iron–quinone complex in PSII. In this study, we investigated the protonation/deprotonation reaction of D1-H215, which bridges the non-heme iron and QB, using attenuated total reflection Fourier transform infrared (ATR-FTIR) spectroscopy. Flash-induced Fe2+/Fe3+ ATR-FTIR difference spectra were measured with PSII membranes in the pH range of 5.0–7.5. In the CN stretching region of histidine, the intensity of a negative peak at 1094 cm–1, which was assigned to the deprotonated anion form of D1-H215, increased as the pH increased. Singular-value decomposition analysis provided a component due to deprotonation of D1-H215 with a pK a of ∼5.5 in the Fe3+ state, whereas no component of histidine deprotonation was resolved in the Fe2+ state. This observation supports the previous proposal that D1-H215 is responsible for the proton release upon Fe2+ oxidation [Berthomieu, C., and Hienerwadel, R. (2001) Biochemistry 40, 4044–4052]. The pH dependence of the 13C isotope-edited bands of the bicarbonate ligand to the non-heme iron further showed that deprotonation of bicarbonate to carbonate does not take place at pH <8 in the Fe2+ or Fe3+ state. These results suggest that the putative mechanism of proton transfer to QBH– through D1-H215 and bicarbonate around Fe2+ functions throughout the physiological pH range.