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.