Department of Physics, School of Science and Technology, Meiji University, Tama-ku, Kawasaki, Kanagawa 214-8571, Japan.
J Photochem Photobiol B. 2011 Jul-Aug;104(1-2):100-10. doi: 10.1016/j.jphotobiol.2011.03.002. Epub 2011 Mar 13.
Photosynthetic water oxidation reaction driven by Sun and catalyzed by a unique Mn(4)Ca cluster in Photosystem II (PSII) is known to take place in an oxygen evolving complex (OEC) that cycles five serial redox states, named "Kok's S(i)-states" (i=0-4). Recently, the atomic crystal structure of PSII from Thermosynechococcus vulcanus was resolved by 1.9 Å-resolution XRD data [55]. Interestingly, it revealed an unusual oxo-bridged Mn(4)CaO(5) cluster in the dark stable S(1)-state, e.g. unusual mono-μ(2)-oxo-mono-μ(4)-oxo-mono-μ(2)-carboxylato bridges connecting Mn(a) (terminal) and Mn(b) (central) ions with unusual atomic distance of 2.9 Å. Using the UDFT/B3LYP/lacvp** geometry optimization method and a truncated cluster model of the chemically-complete OEC put in ε=4 dielectric medium, it is shown that the OEC in S(1) must be in thermal equilibrium between the most-stable isomeric substates ("S(1a) and S(1b)") owing to the quasi-reversible structure change induced by proton migration. Coincidentally, it is found that the Mn(a)-Mn(b) distances in the Mn(4)Ca clusters in S(1a) and S(1b) are given by R(ab)=3.32 Å and 2.77 Å, respectively, so that the apparent distance between Mn(a) and Mn(b) ions in isomeric equilibrium is given by 2.94 Å, in agreement with experimental R(ab)~2.9 Å. Concomitantly, the first full-k-range EXAFS spectrum from powdered PSII [45] is used to provide the second experimental evidence for the S(1)-state OEC being in thermal equilibrium between S(1a) and S(1b)-isomers. These OEC-isomers consist of all the chemically-essential 11 amino acid residues, six cofactor ions and nine essential hydrated water molecules in their chemical ionic states around physiological pH 7, thus reasonably satisfying the biochemical charge neutrality with four Mn ions staying at the oxidation states (Mn(a)(III)/Mn(b)(IV)/Mn(c)(III)/Mn(d)(IV)) with the skeleton structures of MT-5J type and T-shaped DD-4J type. These H-bonding water molecules are found to fill a cavity connecting possible substrate/products channels so as to be arranged as an indispensable part of the catalytic Mn(4)Ca cluster in the order of "current-substrates" (W1/W2 bound to Mn(a)(III)), "next-substrates" (W4/W7) and "next-after-next-substrates" (W5/W6 bound to Ca(2+)). Results show that the Jahn-Teller effect due to Mn(a)(III) ion in these isomers can reasonably explain the very-slow-exchange and very-fast-exchange processes observed in S(1) by time-resolved (18)O-exchange mass spectroscopy.
光合水氧化反应由太阳驱动，并由光合作用 II （PSII）中的独特 Mn(4)Ca 簇催化，已知发生在一个氧释放复合物（OEC）中，该复合物经历五个连续的氧化还原态，称为“Kok 的 S(i)-态”（i=0-4）。最近，通过 1.9 Å 分辨率的 X 射线衍射数据 [55] 解析了来自 Thermosynechococcus vulcanus 的 PSII 的原子晶体结构。有趣的是，它揭示了在黑暗稳定的 S(1)-态中存在一种不寻常的氧桥接 Mn(4)CaO(5)簇，例如连接 Mn(a)（末端）和 Mn(b)（中心）离子的不寻常的单 μ(2)-氧-单 μ(4)-氧-单 μ(2)-羧基桥，具有不寻常的原子距离 2.9 Å。使用 UDFT/B3LYP/lacvp**几何优化方法和化学完整 OEC 的截断簇模型置于 ε=4 介电介质中，表明由于质子迁移引起的准可逆结构变化，OEC 在 S(1)中必须处于最稳定的异构体亚态（“S(1a) 和 S(1b)）之间的热平衡。巧合的是，发现 S(1a) 和 S(1b)中 Mn(4)Ca 簇中的 Mn(a)-Mn(b)距离分别为 R(ab)=3.32 Å 和 2.77 Å，因此异构体平衡中 Mn(a)和 Mn(b)离子之间的表观距离为 2.94 Å，与实验 R(ab)~2.9 Å 一致。同时，[45] 从粉末 PSII 获得的第一个全范围 EXAFS 光谱用于提供 S(1)-态 OEC 在 S(1a)和 S(1b)-异构体之间处于热平衡的第二个实验证据。这些 OEC 异构体由所有化学必需的 11 个氨基酸残基、6 个辅助因子离子和 9 个必需的水合水分子组成，其化学离子状态在生理 pH 7 左右，因此在四个 Mn 离子保持在氧化态（Mn(a)(III)/Mn(b)(IV)/Mn(c)(III)/Mn(d)(IV)）的情况下，合理地满足了生化电荷中性，骨架结构为 MT-5J 型和 T 型 DD-4J 型。发现这些氢键水分子填充了连接可能的底物/产物通道的腔，从而以“当前底物”（与 Mn(a)(III)结合的 W1/W2）、“下一个底物”（W4/W7）和“下一个下一个底物”（与 Ca(2+)结合的 W5/W6）的顺序作为催化 Mn(4)Ca 簇的不可或缺的一部分排列。结果表明，由于这些异构体中的 Mn(a)(III)离子的 Jahn-Teller 效应，可以合理地解释时间分辨（18）O 交换质谱法在 S(1)中观察到的非常慢交换和非常快交换过程。
