Department of Chemistry, Yale University, New Haven, Connecticut 06520-8107, United States.
Department of Chemistry and Chemical Biology and The Baruch '60 Center for Biochemical Solar Energy, Rensselaer Polytechnic Institute, Troy, New York 12180, United States.
J Am Chem Soc. 2021 Jun 9;143(22):8324-8332. doi: 10.1021/jacs.1c00633. Epub 2021 May 24.
We address the protonation state of the water-derived ligands in the oxygen-evolving complex (OEC) of photosystem II (PSII), prepared in the S state of the Kok cycle. We perform quantum mechanics/molecular mechanics calculations of isotropic proton hyperfine coupling constants, with direct comparisons to experimental data from two-dimensional hyperfine sublevel correlation (HYSCORE) spectroscopy and extended X-ray absorption fine structure (EXAFS). We find a low-barrier hydrogen bond with significant delocalization of the proton shared by the water-derived ligand, W1, and the aspartic acid residue D1-D61 of the D1 polypeptide. The lowering of the zero-point energy of a shared proton due to quantum delocalization precludes its release to the lumen during the S→ S transition. Retention of the proton facilitates the shuttling of a proton during the isomerization of the tetranuclear manganese-calcium-oxo (MnCa-oxo) cluster, from the "open" to "closed" conformation, a step suggested to be necessary for oxygen evolution from previous studies. Our findings suggest that quantum-delocalized protons, stabilized by low-barrier hydrogen bonds in model catalytic systems, can facilitate the accumulation of multiple oxidizing equivalents at low overpotentials.
我们研究了光合作用系统 II（PSII）中氧释放复合物（OEC）中源自水的配体的质子化状态，该复合物是在 Kok 循环的 S 态下制备的。我们进行了各向同性质子超精细耦合常数的量子力学/分子力学计算，并与二维超精细亚层相关（HYSCORE）光谱和扩展 X 射线吸收精细结构（EXAFS）的实验数据进行了直接比较。我们发现源自水的配体 W1 和 D1 多肽的天冬氨酸残基 D1-D61 之间存在一个低势垒氢键，质子具有明显的离域化。由于量子离域化，共享质子的零点能降低，从而阻止其在 S→S 转变过程中释放到腔室中。质子的保留有助于在四核锰-钙-氧（MnCa-oxo）簇的异构化过程中质子的转移，从“开”构象到“闭”构象，这一步骤在之前的研究中被认为是氧气释放所必需的。我们的研究结果表明，在模型催化体系中，由低势垒氢键稳定的离域化质子可以在低过电势下促进多个氧化当量的积累。
