Understanding Two Different Structures in the Dark Stable State of the Oxygen-Evolving Complex of Photosystem II: Applicability of the Jahn-Teller Deformation Formula.

Tanaka et al. (J. Am. Chem. Soc., 2017, 139, 1718) recently reported the three-dimensional (3D) structure of the oxygen evolving complex (OEC) of photosystem II (PSII) by X-ray diffraction (XRD) using extremely low X-ray doses of 0.03 and 0.12 MGy. They observed two different 3D structures of the CaMn4O5 cluster with different hydrogen-bonding interactions in the S1 state of OEC keeping the surrounding polypeptide frameworks of PSII the same. Our Jahn-Teller (JT) deformation formula based on large-scale quantum mechanics/molecular mechanics (QM/MM) was applied for these low-dose XRD structures, elucidating important roles of JT effects of the MnIII ion for subtle geometric distortions of the CaMn4O5 cluster in OEC of PSII. The JT deformation formula revealed the similarity between the low-dose XRD and damage-free serial femtosecond X-ray diffraction (SFX) structures of the CaMn4O5 cluster in the dark stable state. The extremely low-dose XRD structures were not damaged by X-ray irradiation. Implications of the present results are discussed in relation to recent SFX results and a blue print for the design of artificial photocatalysts for water oxidation.