Theory of chemical bonds in metalloenzymes XXIII fundamental principles for the photo-induced water oxidation in oxygen evolving complex of photosystem II

Abstract

Molecular quantum mechanics (MQM) investigations have been performed for elucidation of fundamental principles of the photo-induced water oxidation in oxygen evolving complex (OEC) of photosystem II (PSII). To this end, as a first theoretical step, broken symmetry (BS) quantum mechanics (QM) and QM(BS)/molecular mechanics (MM) calculations have been conducted for elucidation of geometrical, electronic and spin structures of the CaMn₄O_x (X = 5, 6) cluster in the five steps S_i (i = 0∼4) of the Kok cycle for water oxidation. The QM and QM/MM calculations have provided full optimised geometries of short-lived key intermediates and transition state structure for the O-O bond formation in the native solar-energy conversion. The interplay between theory and experiment have clearly indicated that the CaMn₄O₅ cluster in OEC of PSII exhibits typical physicochemical properties of strong correlation electron system (SCES) confined with effective protein field. Our QM and QM/MM computational results for key intermediates and transition structure for the O-O bond formation in the Kok cycle are now plentiful for derivation of fundamental principles (FP) for understanding of photo-induced water oxidation in OEC of PSII.

We summarize twenty nine fundamental principles (FPs) in systematic manner by QM and QM/MM calculations for understanding of water oxidation in Oxygen Evolving Complex(OEC) of Photosystem II(PSII). One of our final aims is theoretical design of the next-generation artificial photosystem materials composed of abundant metal ions.

GRAPHICAL ABSTRACT

KEYWORDS:

• Water oxidation
• reaction mechanism
• CaMn₄O₅ cluster
• OECof PSII

Acknowledgements

One of authors (K. Y) thank Professor J.-R. Shen, Professor N. Kamiya, Prof. J. Messinger and Professor S. Masaoka for helpful discussions on the possible mechanisms of water oxidation in OEC of PSII. Numerical calculations have been carried out under the supports of (1) the computational resource of the center for computational sciences (CCS), University of Tsukuba, (2) the research center for computational Sciences, Okazaki, Japan, and (3) HPCI system research projects using the computational resources of the K computer provided by the RIKEN Advanced Institute for Computational Science (AICS). SY and KY thank Prof. M. Kitagawa in the division of quantum information and quantum biology (QIQB), Osaka University.

Disclosure statement

No potential conflict of interest was reported by the author(s).

Additional information

Funding

This research was supported by Japan Society for the Promotion of Science (JSPS) [grant numbers JP17H04866 and JP18H05154].