Similarity between oxygen evolution in photosystem II and oxygen reduction in cytochrome c oxidase via proton coupled electron transfers. A unified view of the oxygenic life from four electron oxidation–reduction reactions

Basic concepts and theoretical foundations of broken symmetry (BS) and post BS methods for strongly correlated electron systems (SCES) such as electron-transfer (ET) diradical, multi-center polyradicals with spin frustration are described systematically to elucidate structures, bonding and reactivity of the high-valent transition metal oxo bonds in metalloenzymes: photosystem II (PSII) and cytochrome c oxidase (CcO). BS hybrid DFT (HDFT) and DLPNO coupled-cluster (CC) SD(T₀) computations are performed to elucidate electronic and spin states of CaMn₄O_x cluster in the key step for oxygen evolution, namely S₄ [S₃ with Mn(IV) = O + Tyr161-O radical] state of PSII and P_M [Fe(IV) = O + HO-Cu(II) + Tyr161-O radical] step for oxygen reduction in CcO. The cycle of water oxidation catalyzed by the CaMn₄O_x cluster in PSII and the cycle of oxygen reduction catalyzed by the Cu_A-Fe_a-Fe_a3-Cu_B cluster in CcO are examined on the theoretical grounds, elucidating similar concerted and/or stepwise proton transfer coupled electron transfer (PT-ET) processes for the four-electron oxidation in PSII and four-electron reduction in CcO. Interplay between theory and experiments have revealed that three electrons in the metal sites and one electron in tyrosine radical site are characteristic for PT-ET in these biological redox reaction systems, indicating no necessity of harmful Mn(V) = O and Fe(V) = O bonds with strong oxyl-radical character. Implications of the computational results are discussed in relation to design of artificial systems consisted of earth abundant transition metals for water oxidation.