Alternative Mechanism for O₂ Formation in Natural Photosynthesis via Nucleophilic Oxo–Oxo Coupling

Abstract

O2 formation in photosystem II (PSII) is a vital event on Earth, but the exact mechanism remains unclear. The presently prevailing theoretical model is “radical coupling” (RC) involving a Mn(IV)-oxyl unit in an “open-cubane” Mn4CaO6 cluster, which is 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. For this proposal, we explore here a large number of possible pathways of O–O bond formation and demonstrate 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 RC mechanism. An energetically feasible process is described starting from the valid S4 state through the sequential formation of peroxide and superoxide, followed by O2 release and a second water insertion. The newly found mechanism is consistent with available experimental thermodynamic and kinetic data and thus a viable alternative pathway for O2 formation in natural photosynthesis, in particular for higher plants.

Is There a Different Mechanism for Water Oxidation in Higher Plants?

“…Starting with the Mn(V)�O structure and approaching a TS structure, here led to a similar TS as found in the WU mechanism with an approximate barrier of +12.6 kcal/mol with respect to Mn(V)�O. 14 The wave function for the TS has undergone a drastic change from the one of Mn(V)�O, and is now much more Mn(IV)-oxyl like. Also, approaching outside water toward the empty site of Mn4 led to a large energy decrease for the TS energy by −11.1 kcal/ mol.…”

“…The spin on the oxo has now changed from +0.11 in the Mn(V)−oxo structure to −0.40, and the one on Mn4 from 1.91 to 2.63, indicating a large change from Mn(V)�O toward Mn(IV)−oxyl. Therefore, the TS is not of oxo−oxo, as claimed for the WU mechanism, 14 but of oxyl− oxo type. An outside water molecule now has a rather short distance to Mn4 with a distance of 3.13 Å.…”

“…To complete the picture, calculations were finally done without Asp61 since that was the model used for the WU mechanism . The charge of the model is then +2 instead of +1.…”

“…In a very recent paper by Messinger and co-workers, a new mechanism for dioxygen formation in higher plants was suggested. The starting point was the earlier assignment of the S 3 state as a closed cubane in the WU mechanism . To reach the new S 4 state, an electron and a proton were removed from S 3 .…”

O–O Bond Formation and Oxygen Release in Photosystem II Are Enhanced by Spin-Exchange and Synergetic Coordination Interactions

“…Inspired by the recent study, 104 two representative spin states (S = 11/2 and S = 7/2) have been considered for the O−O coupling reactions. In S = 11/2, the electrons of all Mn ions are spin-up (denoted as αααα), while in S = 7/2, the electrons at Mn 4 are spin-down and the electrons at left Mn ions are spin-up (denoted as αααβ).…”