Histidine Protonation and the Oxidizing Power of the Oxygen‐Evolving Complex

Redox tuning of the oxygen‐evolving complex (OEC) is essential for photosynthetic water oxidation in photosystem II (PSII). The PSII crystal structure indicates that D1‐His337, which forms an H‐bond with the OEC, can adopt either a doubly protonated cationic form or a singly protonated charge‐neutral form. Here, we investigate the redox potential ( E m ) of OEC components in the PSII protein environment, considering all redox‐active sites involved in the electron‐transfer cascade driving water oxidation. Singly protonated D1‐His337 is unstable, exhibiting an exceptionally low E m , such that one‐electron oxidation generates a cation radical and inhibits oxidation of the Mn 4 CaO 5 core. In contrast, doubly protonated D1‐His337 is oxidation‐stable, upshifting E m (Mn4(III/IV)) by > 200 mV in the S 1 to S 2 transition. p K a (D1‐His337) responds to the net charge difference between S 1 and S 2 , but remains essentially unchanged between the open‐ and closed‐cubane S 2 conformations despite their different Jahn–Teller axes. Doubly protonated D1‐His337 is also required to preserve the canonical Mn oxidation ordering, i.e., Mn3(III) oxidation in the S 0 to S 1 transition followed by Mn4(III) oxidation in the S 1 to S 2 transition, thereby serving as a key external electrostatic modulator for the Mn 4 CaO 5 core.