The Center of Artificial Photosynthesis (CAP) for Solar Fuels has made progress in natural water oxidation, proposing a new mechanism for O₂ formation in nature by using quantum chemical calculations in a study titled “Alternative mechanism for O₂ formation in natural photosynthesis via nucleophilic oxo–oxo coupling,” published in the Journal of the American Chemical Society (J. Am. Chem. Soc. 2023, 145, 4129-4141).

The emergence of oxygen (O₂) has played an essential role in the evolution of life. In nature, O₂ is produced by photosynthetic water splitting in plants, algae, and cyanobacteria, and the light-driven reaction at the water oxidation center is catalyzed by the “oxygen-evolving complex (OEC)” embedded in photosystem II (PSII). However, the mechanism behind the O-O bond formation has remained a mystery for billions of years. Eight Nobel Prizes have been awarded to outstanding contributors to natural photosynthesis in history, but humans have not yet fully understood the most important chemical reaction on Earth.

The prevailing theoretical model for O-O bond formation is "radical coupling” involving a Mn(IV)-oxyl unit in an “open-cubane” Mn₄CaO₆ cluster, supported experimentally by the S₃ state of cyanobacterial PSII featuring an additional Mn-bound oxygenic ligand. However, it was recently proposed that the major structural form of the S₃ state of higher plants lacks this extra ligand, and that the resulting S₄ state would feature instead a penta-coordinate dangler Mn(V)=oxo, covalently linked to a “closed-cubane” Mn₃CaO₄ cluster. To test this proposal, the researchers explored in the new study many possible pathways of O-O bond formation, and demonstrated that the nucleophilic oxo-oxo coupling (NOOC) between Mn(V)=oxo and μ₃-oxo is the only eligible mechanism in such a system. The reaction is facilitated by a specific conformation of the cluster and concomitant water binding, which is delayed compared to the radical coupling mechanism. An energetically feasible process is described starting from the valid S₄ state through sequential formation of peroxide and superoxide, followed by O₂ release and a second water insertion. The new mechanism is consistent with available experimental thermodynamic and kinetic data, offering a viable alternative pathway for O₂ formation in natural photosynthesis, especially higher plants. Furthermore, the theoretical results provide support for the Mn(V)=oxo entity as a key species involved in O-O bond formation in PSII and reflected in synthetic model compounds. The alternative NOOC pathway represents an important complement to the long-standing RC mechanism characterized by Mn(IV)-oxyl in natural water oxidation.

Westlake University Prof. Licheng Sun is the corresponding author and Dr. Yu Guo the first author of the study. The work, done in collaboration with Swedish scholars, was financially supported by the National Key R&D Program of China as well as Westlake University. Westlake’s High-Performance Computing Center provided computational assistance.