Max-Planck-Institut für Chemische Energiekonversion , Stiftstrasse 34-36, D-45470 Mülheim an der Ruhr, Germany.
Department of Life Sciences, Imperial College London , London SW7 2AZ, United Kingdom.
J Am Chem Soc. 2017 Oct 18;139(41):14412-14424. doi: 10.1021/jacs.7b05263. Epub 2017 Oct 3.
Nature's water-splitting catalyst, an oxygen-bridged tetramanganese calcium (MnOCa) complex, sequentially activates two substrate water molecules generating molecular O. Its reaction cycle is composed of five intermediate (S) states, where the index i indicates the number of oxidizing equivalents stored by the cofactor. After formation of the S state, the product dioxygen is released and the cofactor returns to its lowest oxidation state, S. Membrane-inlet mass spectrometry measurements suggest that at least one substrate is bound throughout the catalytic cycle, as the rate of O-labeled water incorporation into the product O is slow, on a millisecond to second time scale depending on the S state. Here, we demonstrate that the MnOCa complex poised in the S state contains an exchangeable hydroxo bridge. On the basis of a combination of magnetic multiresonance (EPR) spectroscopies, comparison to biochemical models and theoretical calculations we assign this bridge to O5, the same bridge identified in the S state as an exchangeable fully deprotonated oxo bridge [Pérez Navarro, M.; et al. Proc. Natl. Acad. Sci. U.S.A. 2013, 110, 15561]. This oxygen species is the most probable candidate for the slowly exchanging substrate water in the S state. Additional measurements provide new information on the Mn ions that constitute the catalyst. A structural model for the S state is proposed that is consistent with available experimental data and explains the observed evolution of water exchange kinetics in the first three states of the catalytic cycle.
自然界的水分解催化剂是一个氧桥接的四锰钙（MnOCa）配合物，它依次激活两个底物水分子，生成分子氧。它的反应循环由五个中间（S）态组成，其中指数 i 表示辅助因子存储的氧化当量数。在 S 态形成后，释放出产物氧气，辅助因子回到其最低氧化态 S。膜进质谱测量表明，至少有一个底物在整个催化循环中结合，因为 O 标记水掺入产物 O 的速率很慢，取决于 S 态，在毫秒到秒的时间范围内。在这里，我们证明了处于 S 态的 MnOCa 配合物含有可交换的羟桥。基于磁多共振（EPR）光谱学、与生化模型和理论计算的比较，我们将该桥分配给 O5，这与 S 态中鉴定为可交换的完全去质子化的氧桥相同[Pérez Navarro，M.；等人。美国国家科学院院刊。2013, 110, 15561]。这种氧物种是 S 态中缓慢交换的底物水的最可能候选物。进一步的测量提供了关于构成催化剂的 Mn 离子的新信息。提出了一个 S 态的结构模型，该模型与现有实验数据一致，并解释了催化循环的前三个状态中水交换动力学的观察到的演变。
