Solar-to-Chemical Conversion. Группа авторов

feature of the OEC is that electrons and protons are removed in an alternate fashion along the S‐state cycle [126–128]. This creates a redox‐leveling effect, which means that the four successive oxidative steps can take place within a narrow range of potential.

Figure 3.8 The cycle of intermediate oxidation states of the oxygen‐evolving complex. Water is assumed to bind at the S₃ state of the cluster and upon reconstitution of the S₀ state. The S₄ state is a postulated but unobserved transient intermediate that decays spontaneously to S₀ with release of dioxygen.

The geometric structure of the OEC has been the subject of speculation for a very long time [129, 130], ever since EPR studies on the S₂ state in 1981 established the presence of four antiferromagnetically interacting Mn ions giving rise to a multiline g = 2 EPR signal arising from a cluster with total spin state S = 1/2 [131]. Extended X‐ray absorption fine structure (EXAFS) studies provided increasingly detailed and accurate information about the metal–metal distances within the cluster over the next decades [130, 132–139], but no unique three‐dimensional reconstruction of this information could be achieved without additional input from crystallography [140, 141]. The appearance of the first XRD structure of PS‐II in 2001 [47] and the development of crystallographic models over the following years culminated in an atomic‐resolution model of the OEC core in 2011 [55]. A particular challenge for crystallography was the control of X‐ray radiation damage that led to reduction of the Mn ions [136, 142, 143] and compromised the quality and reliability of structural information contained in the fitted structural models [144–146]. This problem was addressed to large extent [147, 148] by the use of XFEL approaches [57], although certain structural details remain debatable [56, 149–151].

Our present view of the OEC cluster in the dark‐stable S₁ state is depicted in Figure 3.9. It is an asymmetric Mn₄CaO₅ cluster, where three Mn ions and a Ca ion form a Mn₃CaO₄ cubane unit, while a fourth Mn ion is attached externally to this cubane both by coordination to an oxo bridge of the cubane and by a fifth oxo bridge (note that the protonation state of the bridges cannot be inferred from crystallographic models). The inorganic core is mostly ligated by carboxylates provided by the D1 and CP43 proteins: D1‐Asp170, D1‐Glu189, D1‐Glu333, D1‐Asp342, CP43‐Glu354, and the C‐terminal D1‐Ala344. There is a single nitrogen‐donor ligand, D1‐His332, coordinated to Mn1. Four water‐derived ligands, i.e. H₂O or OH, are identified in the crystallographic models; two of them are attached to Mn4 (W1 and W2), and two are attached to calcium (W3 and W4).

Figure 3.9 The Mn₄CaO₅ cluster and its protein pocket in the dark‐stable S₁ state as revealed by protein crystallography (PDB ID: 3WU2, a), and a scheme showing the commonly used labeling of the ions comprising the inorganic core.

The second coordination sphere of the OEC contains the redox‐active tyrosine and its hydrogen‐bonded histidine partner D1‐His190. The tyrosine hydrogen‐bonds directly with one of the Ca‐bound waters and hence is in close interaction with the cluster. Additional residues such as D1‐His337, CP43‐Arg357, D1‐Asp61, and D2‐Lys317, as well as a functionally required chloride ion, interact with the inorganic core and its ligands mostly via hydrogen bonds. These residues play important roles in regulating properties of the cluster and its ligands [152–157], such as the magnetic interaction between specific pairs of Mn ions and local pK_a values of various groups, and may influence or directly participate in proton translocation. An important additional aspect of the local environment of the OEC is the system of water channels and hydrogen‐bonding networks that surround it. These channels and networks are crucial for connecting the active site of water oxidation to the solvent‐exposed surface of the protein and play critical roles in substrate delivery, proton transfer, and product release [158–173].

      There is a strong but complex connection between the geometric and electronic structure of the OEC. This connection is key for deciphering the structure of the other S‐states and, eventually, for understanding the mechanism of biological water oxidation [7]. In the following, some of the currently most well‐supported ideas about the geometric and electronic structure of the other S‐states will be presented, with the caveat that there exist significant open questions and ambiguities about many of the specifics [7, 8].

A central question concerns the oxidation states of the Mn ions, their distribution within the cluster, and how they change along the S_i–S_i+1 transitions. Important information on the electronic structure of the cluster can be obtained from magnetic resonance methods, as well as from XAS and XES [128, 174–183]. Structural interpretations of such data can in turn be achieved by spectroscopy‐oriented quantum chemical methods [146, 150, 179, 184–193] that have been extensively benchmarked for high‐valent manganese systems [150, 179, 186, 194–198] and additionally incorporate geometric information from EXAFS and crystallographic models. The dominant view is that the Mn oxidation states evolve from Mn(III)₃Mn(IV) in the S₀ state to Mn(III)₂Mn(IV)₂ in S₁, Mn(III)Mn(IV)₃ in S₂, and Mn(IV)₄ in S₃. This assignment is called the “high oxidation state scheme” [199] as opposed to the low oxidation state hypothesis [200–205] that assigns two more electrons to the Mn ions, with oxidation states ranging from Mn(III)₃Mn(II) in S₀ to Mn(III)₂Mn(IV)₂ in S₃. EPR spectroscopy has helped to identify spin states of all observable intermediates (S = 1/2 for S₀ [206–213], S = 0 for S₁ with a low‐lying S = 1 state [212–217], two forms of S₂ with S = 1/2 and S ≥ 5/2 [218–225], and S = 3 for S₃ [226–228]) but cannot uniquely assign absolute oxidation states. ⁵⁵Mn electron nuclear double resonance (ENDOR) studies of the S₂ state first demonstrated the “3+1” Y‐shaped configuration of the cluster [176, 229], while ⁵⁵Mn hyperfine coupling parameters supported the Mn(III)Mn(IV)₃ oxidation state assignment for S₂ [176, 230, 231] and confirmed the absence of Mn(II) in the S₀ state [230, 232]. Electron–electron double resonance (ELDOR) detected nuclear magnetic resonance experiments (EDNMR) of the S₃ state [228] demonstrated that all Mn ions are similar and isotropic, consistent with the Mn(IV)₄ oxidation state assignment. X‐ray absorption and emission spectroscopies broadly agree with the results of magnetic resonance spectroscopies regarding oxidation states and localization of oxidation events. X‐ray absorption near‐edge spectroscopy (XANES) shows a shift of the Mn K‐edge to higher energies with each S‐state transition, consistent with successive Mn‐based oxidation [181, 233, 234] and a change in coordination in the S₂ → S₃ transition [235]. XES studies observe changes in the Kβ′, Kβ_1,3, and Kα lines. Recent time‐resolved studies of Kβ_1,3 emission spectra of the OEC at room temperature that included comparisons with reference compounds support the high oxidation state assignment described above as well as Mn(III)–Mn(IV) oxidation in the S₂ → S₃ transition [182], while room‐temperature Kα XES studies that similarly compared data on the OEC with those on synthetic compounds in different oxidation states confirmed that the OEC reaches the Mn(IV)₄ oxidation level in the S₃ state [183]. The same assignment of oxidation states is supported by independent studies of photoactivation