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Referring back to Figure 3.2 that depicts the main components involved in oxygenic photosynthesis, it is useful to translate that scheme into a corresponding energy/electron flow diagram, the so‐called Z‐scheme of photosynthesis shown in Figure 3.6. The essential features are the utilization of two charge separation events (at P680 of PS‐II and P700 of PS‐I) with distinct potentials and the closely spaced electron transfer cascades that contribute to stabilization of charge separation and unidirectionality of electron transfer. It is noted that purple bacteria utilize only a type II reaction center that lacks the water oxidizing ability of PS‐II, whereas green sulfur bacteria utilize only type I centers, related to PS‐I. A one‐step process is in principle harder to apply to water splitting because of constraints placed on the reduction potential of the excited reaction center chromophore: it should be more positive than the water oxidation potential yet more negative than the hydrogen evolution potential. This creates limitations regarding the minimum excitation energy required to drive a single‐step water splitting process. By contrast, the two‐step process embodied in the Z‐scheme of oxygenic photosynthesis relaxes these constraints by utilizing two photons per electron transferred from water to the final electron acceptor and hence being able to use sunlight of lower energy that what would have been necessary otherwise. In the context of artificial photosynthesis, an implementation of the Z‐scheme (for instance, in multi‐junction photovoltaic devices) would similarly offer higher flexibility in the choice of materials and redox linkers/mediators, requiring only that the excited‐state potential of the reaction center at the oxidative side be lower than that of the reaction center at the reducing side.

Figure 3.6 Simplified Z‐scheme of natural oxygenic photosynthesis, showing how two photons are used per electron flowing from the terminal donor (H₂O) to the terminal acceptor (NADP⁺) of the light‐dependent reactions.

Both photosystems have homodimeric structures and exhibit high similarity in the proteins and cofactors comprising their core regions, suggestive of their common evolutionary origin. In the following we will focus on the enzyme responsible for water oxidation, PS‐II (see Figure 3.7). Crystallographic structures of PS‐II are mostly available from thermophilic cyanobacteria such as Thermosynechococcus elongatus and Thermosynechococcus vulcanus. Conventional X‐ray diffraction (XRD) studies, which first yielded a PS‐II crystallographic model in 2001 [47] and make use of synchrotron X‐ray radiation, have more recently been supplanted by approaches that utilize X‐ray free‐electron laser (XFEL) femtosecond pulses [48, 49]. Through a long series of XRD studies [50–56], the highest‐resolution cyanobacterial PS‐II crystallographic models currently stand at 1.9 Å [55] and 1.87/1.85 Å [56]. Presently available XFEL models have still not achieved comparable resolution, but they have opened the way for probing intermediate states of the water oxidation cycle [57-63]. Higher‐plant PS‐II structures that resolve internal cofactors have so far been reported from cryo‐electron microscopy at comparatively lower resolution [64, 65].

Figure 3.7 Photosystem II from T. vulcanus (PDB ID: 3WU2, a) and major redox‐active components within a PS‐II monomer involved in the main‐pathway electron transfer indicated with red arrows (b).

Each monomer of cyanobacterial PS‐II consists of 20 protein chains, a large number of organic cofactors such as chlorophylls, pheophytins, carotenoids, lipids, and quinones, and a number of inorganic cofactors that include hemes, a nonheme iron, calcium and chloride ions, and the tetramanganese–calcium cofactor (Mn₄CaO_x) of the OEC. Four transmembrane proteins comprise the core of the enzyme and host all major nonprotein cofactors; these are denoted D1, D2, CP43, and CP47. The PS‐II core proteins are surrounded by additional proteins that may be either permanently or transiently attached [64, 66–70]. In contrast to the highly conserved core proteins, extrinsic or auxiliary proteins have larger variation between different species. The redox‐active cofactors that participate in electron transfer from water to plastoquinone Q_B are arranged in quasi‐symmetric branches (Figure 3.7). Importantly, only one branch is considered to be active in electron transfer, while the other is mostly involved in protective and regulatory functions [71]. The core chlorophylls of PS‐II are four Chl a molecules denoted P_D1, P_D2, Chl_D1, and Chl_D2. These are assigned to the charge separation apparatus of PS‐II, called P680 because of the absorption maximum at 680 nm observed for the cationic radical. Transfer of excitation energy to this set of chromophores results in a charge‐separated state. Our knowledge of the possible nature of initial excited states and localization of charge separation among the core chromophores under various conditions is incomplete [72], but it is accepted that within picoseconds charge separation stabilizes in a state that can be described as [P680^•+ Pheo_D1^•−] [73]. The electron hole is principally localized on chlorophyll P_D1 [74], as opposed to being equally distributed in the P_D1P_D2 pair, presumably as a combined result of the pigment conformation and the effect of the protein matrix [75–77]. Electron transfer on the acceptor side subsequently occurs within hundreds of picoseconds from Pheo_D1^•− to the non‐exchangeable plastoquinone Q_A. Electron transfer from Q_A⁻ to the final electron acceptor plastoquinone Q_B is much slower compared with the previous electron transfer steps, up to a millisecond for the second reduction that creates the plastoquinol (Q_BH₂) that will be released to carry the two electrons further down the chain as depicted in Figures 3.2 and 3.6. The nonheme iron and its (bi)carbonate ligand mediate and modulate electron transfer between the Q_A and Q_B sites without Fe participating directly in redox chemistry [78–81].

The charge separation site of PS‐II is interfaced with the water oxidation site via a redox‐active tyrosine (D1‐Tyr161) known as Y_Z. While the enzyme is poised in the [P680^•+ Q_A^•−] charge‐separated state, Y_Z is oxidized by P680^•+ within tens of nanoseconds. The redox‐active Y_Z is tightly hydrogen‐bonded to the imidazole side group of histidine D1‐His190 [82], which in turn is hydrogen‐bonded to the conserved [83] asparagine D1‐Asn298. Formation of the tyrosyl radical is thought to be coupled to proton shift from the phenolic proton of Y_Z to His190 and possibly to further proton translocation from His190 to Asn298 [84–86]. The tyrosyl radical Y_Z^• is reduced directly by the Mn₄CaO_x cluster of the OEC in the micro‐ to millisecond time scale. Successive oxidations of the OEC by the Y_Z^• radical formed after each light‐driven charge separation event lead to accumulation of electron holes (oxidizing equivalents) at the manganese cluster. Four holes are stored at the OEC before it can catalyze the four‐electron oxidation of water into dioxygen. The details of the catalytic cycle of the OEC will be discussed in the next section of this chapter.

Another redox‐active tyrosine (D2‐Tyr160, Y_D) is found in a position homologous to Y_Z (see Figure 3.7), but that branch does not contain a water oxidation site. Y_D presumably participates in regulatory and protective mechanisms of PS‐II, such as influencing the charge distribution among the chlorophylls of P680^•+ or resetting the OEC to its resting state at night [75, 87–92]. Like Y_Z, the Y_D tyrosine is hydrogen‐bonded to a histidine residue (D2‐His189), but otherwise it is located in a hydrophobic region as opposed to the water‐rich environment of Y_Z and displays slower redox kinetics compared with Y_Z [93–96]. A single water molecule present within a phenylalanine‐rich cavity adjacent to Y_D and which can occupy either a proximal or a distal position with respect to the phenolic side chain is suggested to regulate the redox behavior of Y_D. [97, 98]

The central design principle of the electron transfer cascade is that the thermodynamic properties of each redox‐active component and the kinetics of electron transfer contribute to stabilization of charge‐separated states, ensuring high quantum yield [99] and directionality of electron transfer. The fast increase in the distance between electron and hole suppresses recombination reactions, but at the same time the multiple steps involved in the process lead to a decrease in free energy differences, reducing the total efficiency. PS‐II successfully couples processes that occur in time scales spanning several orders of magnitude, but it is important to note that under normal operating conditions the enzyme has a lifetime of less than half an hour. Damage originates principally in formation of triplet‐state chlorophyll, whose reaction with triplet dioxygen creates highly reactive, hence damaging singlet dioxygen [100]. The functionality of PS‐II is restored through highly efficient repair mechanisms [101–107].

Research into artificial molecular charge‐separating systems has a long history [39, 104–108]. The central challenge in artificial constructs is to stabilize the charge‐separated state long enough that it can perform redox reactions. For the charge‐separated state to be kinetically competent, it has been realized early on that species comprising at least three components, i.e. triads instead of simple electron donor–acceptor dyads, are required. A representative example of such a system is the molecular carotenoid–porphyrin–fullerene (C–P–C₆₀) triads [39, 109]. In this case light excitation leads first to formation of an excited singlet state localized on the central light‐absorbing porphyrin dye (C–P*–C₆₀). The initial excited state then relaxes to a charge‐separated C–P^•+–C₆₀^•− state. Charge recombination between the porphyrin and the fullerene is outcompeted by efficient hole transfer to the carotene, leading to the C^•+–P–C₆₀^•− state with a quantum yield of 95% [109]. The spatial separation of charges in this state contributes to lifetimes in the scale of tens to hundreds of nanoseconds in solution or microseconds in a glass matrix [109, 110]. Even more complicated molecular constructs have been reported that incorporate their own antenna systems and photoprotection units [111, 112]. The use of components based on transition metal ions, particularly ruthenium photosensitizers that can be directly linked to manganese‐based oxidation catalysts, also has a long history and is an active field of research [113–116]. A thorough overview of many additional molecular systems for photoinduced electron transfer is provided in the review by El‐Khouly et al. [12] The challenges in this field, at least in terms of molecular systems discussed in the present chapter, remain the achievement of robustness, kinetic competence of charge‐separated states, and coupling of the one‐electron chemistry with accumulation of oxidizing equivalents so that concerted multi‐electron transformations can be achieved.