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D139N mutation of PsbP enhances the oxygen-evolving activity of photosystem II through stabilized binding of a chloride ion.

Ko ImaizumiTaishi NishimuraRyo NagaoKeisuke SaitoTakeshi NakanoHiroshi IshikitaTakumi NoguchiKentaro Ifuku
Published in: PNAS nexus (2022)
Photosystem II (PSII) is a multisubunit membrane protein complex that catalyzes light-driven oxidation of water to molecular oxygen. The chloride ion (Cl - ) has long been known as an essential cofactor for oxygen evolution by PSII, and two Cl - ions (Cl-1 and Cl-2) have been found to specifically bind near the Mn 4 CaO 5 cluster within the oxygen-evolving center (OEC). However, despite intensive studies on these Cl - ions, little is known about the function of Cl-2, the Cl - ion that is associated with the backbone nitrogens of D1-Asn338, D1-Phe339, and CP43-Glu354. In green plant PSII, the membrane extrinsic subunits-PsbP and PsbQ-are responsible for Cl - retention within the OEC. The Loop 4 region of PsbP, consisting of highly conserved residues Thr135-Gly142, is inserted close to Cl-2, but its importance has not been examined to date. Here, we investigated the importance of PsbP-Loop 4 using spinach PSII membranes reconstituted with spinach PsbP proteins harboring mutations in this region. Mutations in PsbP-Loop 4 had remarkable effects on the rate of oxygen evolution by PSII. Moreover, we found that a specific mutation, PsbP-D139N, significantly enhances the oxygen-evolving activity in the absence of PsbQ, but not significantly in its presence. The D139N mutation increased the Cl - retention ability of PsbP and induced a unique structural change in the OEC, as indicated by light-induced Fourier transform infrared (FTIR) difference spectroscopy and theoretical calculations. Our findings provide insight into the functional significance of Cl-2 in the water-oxidizing reaction of PSII.
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