X-ray spectroscopy-based structure of the Mn cluster and mechanism of photosynthetic oxygen evolution

Abstract

The mechanism by which the Mn-containing oxygen evolving complex (OEC) produces oxygen from water has been of great interest for over 40 years. This review focuses on how X-ray spectroscopy has provided important information about the structure of this Mn complex and its intermediates, or S-states, in the water oxidation cycle. X-ray absorption near-edge structure spectroscopy and high-resolution Mn Kbeta X-ray emission spectroscopy experiments have identified the oxidation states of the Mn in the OEC in each of the intermediate S-states, while extended X-ray absorption fine structure experiments have shown that 2.7 A Mn-Mn di-mu-oxo and 3.3 A Mn-Mn mono-mu-oxo motifs are present in the OEC. X-ray spectroscopy has also been used to probe the two essential cofactors in the OEC, Ca2+ and Cl-, and has shown that Ca2+ is an integral component of the OEC and is proximal to Mn. In addition, dichroism studies on oriented PS II membranes have provided angular information about the Mn-Mn and Mn-Ca vectors. Based on these X-ray spectroscopy data, refined models for the structure of the OEC and a mechanism for oxygen evolution by the OEC are presented.

Fig. 1

The S-state scheme for oxygen evolution. Proposed Mn oxidation states and corresponding EPR signals are shown for each S-state in the Kok cycle.

Fig. 2

Kβ X-ray emission spectra of Mn oxides (adapted from Bergmann et al. [28]). The Kβ spectra consist of two main features: the Kβ′ peak at ~6475 eV and the Kβ_1,3 peak at ~6490 eV. The separation of these two features is due to the exchange interaction of the unpaired 3d electrons with the 3p hole, which is formed as a final state after the core hole is filled by a 3p→1s fluorescence transition. The spin of the unpaired 3d valence electrons can be either parallel (Kβ′) or antiparallel (Kβ_1,3) to the hole in the 3p level. The splitting between the Kβ′ and Kβ_1,3 peaks becomes smaller for higher oxidation states because fewer 3d electrons interact with the 3p hole. Thus, in contrast to the inflection points of the XANES edges, the Kβ_1,3 peaks shift to lower energy with higher oxidation states, as is seen above with the Mn oxides. The magnitude of the Kβ_1,3 peak first-moment shift for ${\text{Mn}}_2^{\text{III}}{\mathrm{O}}_3\to {\text{Mn}}^{\text{IV}}{\mathrm{O}}_2$ is roughly a factor of four larger than the first-moment shift for the S₁→S₂ transition, where only one Mn out of four is being oxidized.

Fig. 3

Oscillation patterns from XANES and Kβ XES flash (nF) experiments. (A) Oscillation of XANES inflection point energies (I.P.E.) of 0F to 6F samples. (B) Oscillation of first moments () of Kβ spectra from 0F to 3F samples (4F to 6F were not collected). XANES and Kβ X-ray emission spectra shift in opposite directions in response to Mn oxidation (see text for details).

Fig. 4

Possible core structures for the active site of the OEC in PS II. Adapted from DeRose et al. [40]. Only Mn and bridging O are shown.

Fig. 5

Proposed model for the active site of the OEC in PS II from the work of Cinco et al. [72]. The model incorporates the finding from the isotropic Sr-substituted PS II studies: Sr²⁺ (and therefore Ca²⁺) is intimately linked to the Mn cluster at a distance of ~3.4–3.5 Å. This linkage requires single-atom (oxygen) bridging that can derive from acidic protein residues (aspartate or glutamate), hydroxide, or water. Depicted is one of several possible configurations consistent with the findings of the isotropic Sr EXAFS studies.

Fig. 6

Refined models for the active site of the OEC in PS II. These models incorporate the recent finding from oriented Sr-substituted PS II studies that the Sr–Mn vectors lie at an average angle of ~23° with respect to the membrane normal; thus, the refined angle for the 3.3 Å Mn–Mn vector is ~62°. The distance between the two Mn atoms on either end of the complex in model A can be somewhat shortened by using a different oxygen ligand atom from the inner Mn to form the di-μ-oxo binuclear unit on the right side. This is shown in model B. Model C is a variation on a model originally proposed by Siegbahn [46]. The position of the Mn on the end of the mono-μ-oxo bridge can be varied by rotation about the inner Mn–O mono-μ-oxo bond.

Fig. 7

Summary of the changes in Mn–Mn distances in the native S₁, native S₂, modified S₂, ${{\mathrm{S}}_3}^{\prime }({\mathrm{S}}_2{\mathrm{Y}}_{\mathrm{Z}}^{•})$, and native S₃ states of PS II as determined by XAS. Reprinted from Liang et al. [90]. Copyright 2000 American Chemical Society

Fig. 8

Scheme showing two different paths by which an oxyl radical formed in the S₃ state may form an O–O bond in the transient S₄ state before release of dioxygen. One path involves the formation of an O–O bond between the two oxo groups of one binuclear unit. The other path for the formation of the O–O bond is the reaction of the oxyl radical formed with OH⁻ or H₂O that is a ligand of Mn or in the outer sphere of the Mn cluster. The Mn–Mn distances in the transient S₄ state are unknown at present. Reprinted from Liang et al. [90]. Copyright 2000 American Chemical Society