Abstract
The catalytic cycle of the oxygen-evolving complex (OEC) of photosystem II (PSII) comprises five intermediate states Si (i = 0–4), from the most reduced S0 state to the most oxidized S4, which spontaneously evolves dioxygen. The precise geometric and electronic structure of the Si states, and hence the mechanism of O–O bond formation in the OEC, remain under investigation, particularly for the final steps of the catalytic cycle. Recent advances in protein crystallography based on X-ray free-electron lasers (XFELs) have produced new structural models for the S3 state, which indicate that two of the oxygen atoms of the inorganic Mn4CaO6 core of the OEC are in very close proximity. This has been interpreted as possible evidence for “early-onset” O–O bond formation in the S3 state, as opposed to the more widely accepted view that the O–O bond is formed in the final state of the cycle, S4. Peroxo or superoxo formation in S3 has received partial support from computational studies. Here, a brief overview is provided of spectroscopic information, recent crystallographic results, and computational models for the S3 state. Emphasis is placed on computational S3 models that involve O–O formation, which are discussed with respect to their agreement with structural information, experimental evidence from various spectroscopic studies, and substrate exchange kinetics. Despite seemingly better agreement with some of the available crystallographic interpretations for the S3 state, models that implicate early-onset O–O bond formation are hard to reconcile with the complete line of experimental evidence, especially with X-ray absorption, X-ray emission, and magnetic resonance spectroscopic observations. Specifically with respect to quantum chemical studies, the inconclusive energetics for the possible isoforms of S3 is an acute problem that is probably beyond the capabilities of standard density functional theory.
Highlights
In oxygenic photosynthetic organisms conversion of solar to chemical energy is initiated by the light-driven four-electron oxidation of water in the membrane protein complex Photosystem II (PSII), a water–plastoquinone oxidoreductase [1,2] (Figure 1a)
We provide a brief overview of selected experimental information on the geometric and electronic structure parameters of the S3 state, compiled from the numerous spectroscopic studies that were performed before the advent of X-ray free-electron lasers (XFELs) crystallographic models
The representative studies discussed in the preceding section have advanced a range of peroxo models for the S3 state that are of different quality in terms of computational refinement, with differences in bonding topology and protonation states, and with highly uncertain relative energies compared to alternative redox forms
Summary
In oxygenic photosynthetic organisms conversion of solar to chemical energy is initiated by the light-driven four-electron oxidation of water in the membrane protein complex Photosystem II (PSII), a water–plastoquinone oxidoreductase [1,2] (Figure 1a). With respect to dioxygen evolution, a long-held and currently popular view is that formation of the O–O bond occurs in the S4 state or, more realistically, as part of a still unknown multistage S3 –S0 transition that has so far been explored only in various computational studies [35,36,37,38]. Evaluation of the computational models with respect to spectroscopic data suggests that O–O coupling in the S3 state remains the least likely among currently proposed hypotheses, but it is acknowledged that the nature of the S3 state and of the S2 –S3 transition are not yet sufficiently understood to allow definitive structural assignments of intermediates
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