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Reversible Structural Isomerization of Nature’s Water Oxidation Catalyst Prior to O–O Bond Formation

16, 2022

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Photosystem II (PSII) is a metalloenzyme that catalyzes water splitting to molecular oxygen in cyanobacteria, algae, and plants. It evolved about 3 billion years ago at the level of ancient cyanobacteria. The embedded “oxygen-evolving complex (OEC)”, composed of a Mn4CaO5 cluster surrounded by water and amino acid ligands, acts as a highly efficient water oxidation catalyst. Due to charge separations in the reaction center of PSII, the OEC is initially stepwise oxidized during the cyclic catalysis, so that it attains four (meta)stable intermediates (S0, S1, S2, and S3) and one transient S4 state, the latter of which initiates O2 formation. Accounting also for proton release and charge of the Mn4CaO5(6) complex, the classical five-step “S-state cycle” can be refined to instead include nine intermediate states that are separated by kinetically distinguishable proton and electron transfer steps.

Structural polymorphism of the OEC has been proposed and experimentally observed, mainly by electron paramagnetic resonance spectroscopy, for some decades. The unique “distorted chair”-like geometry of the Mn4CaO5(6) cluster shows structural flexibility that has been frequently proposed to involve “open” and “closed”-cubane forms from the S1 to S3 states. The isomers are interconvertible in the S1 and S2 states, while in the S3 state, the open-cubane structure is observed to dominate in Thermosynechococcus elongatus (cyanobacteria) samples. It is commonly assumed that the O–O bond formation in the S4 state also occurs in the open-cubane conformation. However, there have been also several proposals based on a closed-cubane structure, which is in sharp contrast in terms of geometric configuration. This motivates us to investigate if structural heterogeneity exists just before the S4 state is formed from the S3 state via electron abstraction by Yz.

In this work, using density functional theory calculations, we go beyond the S3+Yz state to the S3nYz → S4+Yz step, and report for the first time that the reversible isomerism, which is suppressed in the S3+Yz state, is fully recovered in the ensuing S3nYz state due to the proton release from a manganese-bound water ligand. The altered coordination strength of the manganese–ligand facilitates formation of the closed-cubane form, in a dynamic equilibrium with the open-cubane form. The open-closed isomerization in the S3nYz state may correspond to the proposed “structural isomerization” preceding dioxygen formation and to thereby constitute the rate limiting 1–2 ms phase (slow phase) that follows a 200 μs lag phase and precedes the much more rapid O2 formation.

This tautomerism immediately preceding dioxygen formation may constitute the rate limiting step for O2 formation, and exert a significant influence on the water oxidation mechanism in photosystem II. The restored structural heterogeneity prior to the S4 state diversifies the viable options for O–O bond formation in PSII. In this way, the availability of both open and closed-cubane structures in the S4 state may reflect a “two-pronged” arrangement of the OEC, allowing for efficient and robust water oxidation, and may have contributed to its evolutionary development. The elegant structural reversibility triggered by proton release in the natural enzyme may provide a useful reference for designs of artificial catalysts.