Tamura Hiroyuki, Saito Keisuke, Ishikita Hiroshi
Department of Applied Chemistry, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-8654, Japan.
Research Center for Advanced Science and Technology, The University of Tokyo, 4-6-1 Komaba, Meguro-ku, Tokyo 153-8904, Japan.
ACS Omega. 2025 Jun 3;10(23):24461-24471. doi: 10.1021/acsomega.5c00945. eCollection 2025 Jun 17.
The mechanism of water oxidation catalyzed by MnCaO in photosystem II lacks consensus, particularly regarding proton-coupled electron transfer in the second flash-induced S to S transition. Here, we investigate the electron transfer mechanism during the S to S transition using a quantum mechanical/molecular mechanical/polarizable continuum model approach. The electrostatic interaction with the oxidized redox-active tyrosine, TyrZ, triggers proton release not from a ligand water molecule near chloride (W2) at dangling Mn (Mn4) or a ligand water molecule at Ca (W3), but from a ligand water molecule (W1) near D1-Asp61 at Mn4, forming OH at Mn-(IV). OH formation at Ca is significantly less stable than that at Mn4-(IV). Incorporation of the OH species into MnCaO induces a valence-state conversion from (III,IV,IV,IV) to (IV,IV,IV,III). Interestingly, subsequent water incorporation from a water channel and restoration of the H-bond network of TyrZ not only elevate the redox potential of TyrZ but also convert the valence state back to (III,IV,IV,IV), facilitating electron transfer to TyrZ. The electronic coupling between Mn1 and TyrZ is 1 to 3 meV in the S to S transition, significantly smaller than those between Mn4 and TyrZ in the S to S (∼170 meV) and S to S (∼120 meV) transitions. This step serves as the rate-limiting step if [Mn-(IV)] is considered to be the relevant state to S.
光系统II中由MnCaO催化的水氧化机制尚未达成共识，特别是在第二次闪光诱导的S到S跃迁中的质子耦合电子转移方面。在这里，我们使用量子力学/分子力学/可极化连续介质模型方法研究S到S跃迁过程中的电子转移机制。与氧化的氧化还原活性酪氨酸TyrZ的静电相互作用触发质子释放，不是来自悬垂锰（Mn4）处靠近氯离子的配体水分子（W2）或钙（Ca）处的配体水分子（W3），而是来自Mn4处靠近D1-Asp61的配体水分子（W1），在Mn-(IV)处形成OH。在Ca处形成OH的稳定性明显低于在Mn4-(IV)处。将OH物种纳入MnCaO会导致价态从(III,IV,IV,IV)转变为(IV,IV,IV,III)。有趣的是，随后从水通道掺入水并恢复TyrZ的氢键网络不仅提高了TyrZ的氧化还原电位，还将价态转换回(III,IV,IV,IV)，促进电子向TyrZ转移。在S到S跃迁中，Mn1和TyrZ之间的电子耦合为1到3 meV，明显小于S到S（约170 meV）和S到S（约120 meV）跃迁中Mn4和TyrZ之间的电子耦合。如果将[Mn-(IV)]视为与S相关的状态，这一步骤将作为限速步骤。
