Charge parameters of atom-bond electronegativity equalization method (ABEEMσπ) for the oxygen-evolving complex (OEC) in the S2 state were established, which were applied to molecular dynamic (MD) simulation based on ABEEM/MM polarizable force field in order to study the mechanism of photosynthetic oxygen evolution, in combination with broken-symmetry density functional theory (BS-DFT). Charge fitting results at HF/STO-3G level (the reason why the basis set is adopted is shown in the cited literatures) show good linear correlation, proving the rationality and efficiency of the ABEEMσπ model in calculating charge distributions. It can be seen from MD simulations that bidirectional isomerizations of the Mn4CaO5 cluster accompany by the transfer of Ca-bound water molecule W3 to pentacoordinate Mn1(Ⅲ)/Mn4(Ⅲ). For the g=2 to g=4.1 form, W3 leaves for Mn4(Ⅲ), while W3 moves to Mn1(Ⅲ) for the inverse course. Both processes involve motions to the original positions of W4 to W3, W588 to W4, and local rearrangements of the water environment, which may indicate the importance of hydrogen bond network to biocatalysis. The observation of W3 coordination to the vacant site of Mn(Ⅲ) as the sixth ligand proximal to O5 may imply W3 could be the fast-exchanging substrate water (Wf) in the S2 state, which makes O2 with O5 in the S4 state. Based on the inference, we investigate O-O bond formation in all the possible spin states for the two isomeric structures under the framework of oxo-oxyl radical coupling mechanism. It is demonstrated from BS-DFT calculations that O2 formation activity is significantly advantageous for the open-cubane structure than the closed-cubane form, i.e. the differences of barriers and driving forces are beyond 20 kcal/mol and 25 kcal/mol, respectively. For the open-cubane structure, the antiferromagnetic coupling of Mn1(IV)-O· stabilizes the reactants, and the spin-parallel feature between O· radical and Mn4(IV) lowers the barriers, and ferromagnetic coupling of Mn1-Mn3 ensures the release of triplet O2. For the closed-cubane structure, the antiferromagnetic coupled Mn4(IV)-O· changes to more stabilized Mn4(Ⅲ)-oxo, losing the radical character of the ligand oxygen, which greatly increases the barriers. The ferromagnetic coupled Mn4(IV)-O· does not belong to the relatively stable electronic configuration of reactants, and cannot be formed by spin frustration from the stable spin states, for their large energy differences above 20 kcal/mol. Thus it cannot be accepted as the accesses of effective reaction channels. Our work expounds the exclusive role of the open-cubane OEC in oxo-oxyl coupling mechanism of O2 creation. It also reveals that the oxygen evolution reactivity is extremely dependent on the spin coupling ways of manganeses and oxygen radical, meanwhile, the structural flexibility of the OEC is essential to the S-state cycle and photosynthetic water splitting.
郭宇, 姚远, 李慧, 赫兰兰, 朱尊伟, 杨忠志, 宫利东, 刘翠, 赵东霞. 光合释氧机理的ABEEM/MM/MD和BS-DFT理论研究[J]. 化学学报, 2017, 75(9): 903-913.
Guo Yu, Yao Yuan, Li Hui, He Lanlan, Zhu Zunwei, Yang Zhongzhi, Gong Lidong, Liu Cui, Zhao Dongxia. Theoretical Study on the Mechanism of Photosynthetic Oxygen Evolution by ABEEM/MM/MD and BS-DFT. Acta Chim. Sinica, 2017, 75(9): 903-913.