The direct interpretation of crystallographic models, supported by quantum chemical calculations, indicates that in the S1 state the terminal Mn1 and Mn4 ions are present as Mn(III), with their Jahn–Teller axes aligned almost collinearly along O5. The precise protonation of the model has not been definitively assigned, with the protonation state of O5 (O2− or OH−) and W2 (H2O or OH−) remaining uncertain [145, 146, 150, 151, 237, 238]. The possibility of crystallographically unresolved structural heterogeneity in the S1 state is also discussed [149, 239–241], which would not be unlikely given the spectroscopic heterogeneity reported both in the S1 state and in the S1YZ• intermediate [118, 119, 242–246]. The preceding S0 state has one more Mn(III) ion compared with S1, and this has been assigned to Mn3, making Mn2 the only Mn(IV) ion of the cluster in S0. The most likely protonation state assignment involves a hydroxy for O5, provided this bridge is unprotonated in S1 [150, 247, 248], while a protonated O4 bridge in S0 [249] is less likely according to spectroscopy [248].
A widely accepted structural/electronic model for the S2 state posits the presence of two valence (redox) isomers, i.e. two geometrically similar forms with different distribution of oxidation states among the Mn ions [188, 250, 251] (Figure 3.10). This is based on quantum chemical calculations of exchange coupling constants, spin states, and 55Mn hyperfine coupling parameters that first proposed explicit connections between modified crystallographic models and electronic structure data from magnetic resonance spectroscopies [188]. The two valence isomers differ in the position of the unique Mn(III) ion of the S2 state, either at Mn1 (“open cubane” isomer S2A) or at Mn4 (“closed cubane” isomer, S2B). The different valence distribution has two important consequences: (i) the connectivity within the cluster is slightly different, as the central O5 bridge is more tightly bound to the Mn(IV) ion in each case rather than to the Mn(III) that exhibits a clear Jahn–Teller elongation axis in the O5 direction, and (ii) the exchange coupling topology is different in each isomer, resulting in different total spin states and related spectroscopic properties. Thus, the S2A isomer has a spin S = 1/2 ground state, whereas the S2B isomer has a spin S = 5/2 ground state. These correspond exactly to the two observed EPR signals of the S2 state at g = 2 and g = 4.1, respectively. Additionally, the computed 55Mn hyperfine coupling constants for the S2A model agree very well with the experimental constants measured for the S = 1/2 signal [146, 188]. Finally, the two quantum chemically derived valence isomers are almost isoenergetic and interconvertible over a low barrier, in direct analogy with the two EPR signals being interconvertible and having a small energy separation [252]. Although other possibilities are discussed in the literature [253, 254], no other interpretation satisfies all of the above experimental constraints.
Figure 3.10 Proposed models for the inorganic core in the S2 state of the OEC, with the first coordination sphere mostly omitted for clarity. The different magnetic topologies of the two valence isomers, as expressed through the pairwise exchange coupling constants Jij (values shown in cm−1; J < 0 is antiferromagnetic coupling), lead to different total spin states and g values for the corresponding EPR signals.
The S2 → S3 transition is the most complex among the observable transitions of the catalytic cycle and the subject of active research. The nature of the S3 state itself remains contentious [255], particularly after recent XFEL models of PS‐II were interpreted in terms of mutually incompatible valence states and structural forms [58, 61, 63]. A plausible scenario that is well supported by quantum chemical calculations on realistic models of the OEC and is maximally consistent with spectroscopic data on the electronic structure of the cluster is presented in Figure 3.11. It suggests that the presence of two valence isomers in the S2 state plays a functional role as part of a gating mechanism [7, 191, 256]. The essential features of this mechanism are as follows: (i) formation of the tyrosyl radical, i.e. the S2YZ• intermediate, causes a reorientation of the dipole moment of the OEC toward Asp61 [257], which can act as proton acceptor [51, 152, 181, 258–260]; (ii) deprotonation of the cluster is required for the OEC to progress past the S2YZ• form [191]; and (iii) the deprotonated S2A isomer cannot progress to the S3 state, but the deprotonated S2B is predicted to be so unstable in the presence of YZ• that the cluster spontaneously reduces the tyrosyl radical before completion of a Mn1 → Mn4 O5 bridge shift to yield an all‐Mn(IV) S3 state species, S3B [191]. This has an unusual five‐coordinate Mn(IV) ion at Mn4 that correlates with the high total spin of S = 6, the unusually high local zero‐field splitting of the five‐coordinate Mn(IV) ion [261], and the ability to absorb in the NIR [191]. These properties can explain a whole list of observations regarding the S3 state that would otherwise be incomprehensible. These include the presence of different populations that give or do not give signals in the EPR [228, 242] and that absorb or do not absorb in the NIR [262–265]. This species can subsequently bind water either internally via the calcium ion [250] or externally [191, 266] through a channel associated with methanol and ammonia interaction with the OEC [157, 169, 170, 267–270] to give rise to additional isomers, all assignable to the S3 state and all featuring four Mn(IV) ions [191, 255, 271, 272].
Figure 3.11 The S2 → S3 transition according to Retegan et al. [191] and possible isovalent Mn(IV)4 components of the S3 state; the superscript “W” indicates binding of an additional water ligand.
Alternative ideas for the S3 state include formation of an oxyl radical as opposed to Mn‐centered oxidation [273, 274] and onset of O—O bond formation as a peroxo or superoxo unit [58, 275–277]. These ideas are consistent to some extent with at least one of the available XFEL crystallographic models of the S3 state, but not with the bulk of spectroscopic information that requires Mn‐based oxidation in the S2 → S3 transition [255] or with the most widely accepted interpretations of substrate exchange kinetics [278–280].
The uncertainty about the composition and nature of the S3 state translates into uncertainty about the nature of the subsequent steps that remain experimentally unresolved and include formation of the active species after the final light‐driven oxidation, formation of the O—O bond, release of dioxygen, and reconstitution of the S0 state. A well‐known radical‐based mechanism for O—O bond formation has been proposed by Siegbahn and is based on structure S3A,W of Figure 3.11 [281–288]. It involves ligand‐based oxidation in the S4 state to yield a terminal oxyl radical at Mn1 that couples with the oxo bridge that connects Mn3, Mn4, and Ca