Photosystem redox activity

The realization of the widespread occurrence of amino acid radicals in enzyme catalysis is recent and has been documented in several reviews (52-61). Among the catalytically essential redox-active amino acids glycyl [e.g., anaerobic class III ribonucleotide reductase (62) and pyruvate formate lyase (63-65)], tryptophanyl [e.g., cytochrome peroxidase (66-68)], cysteinyl [class I and II ribonucleotide reductase (60)], tyrosyl [e.g., class I ribonucleotide reductase (69-71), photosystem II (72, 73), prostaglandin H synthase (74-78)], and modified tyrosyl [e.g., cytochrome c oxidase (79, 80), galactose oxidase (81), glyoxal oxidase (82)] are the most prevalent. The redox potentials of these protein residues are well within the realm of those achievable by biological oxidants. These redox enzymes have emerged as a distinct class of proteins of considerable interest and research activity. 

In photosynthesis, water oxidation is accomplished by photosystem II (PSII), which is a large membrane-bound protein complex (158-161). To the central core proteins D1 and D2 are attached different cofactors, including a redox-active tyro-syl residue, tyrosine Z (Yz) (158-162), which is associated with a tetranuclear manganese complex (163). These components constitute the water oxidizing complex (WOC), the site in which the oxidation of water to molecular oxygen occurs (159, 160, 164). The organization is schematically shown in Fig. 18. 

The question of the molecular basis for the S states has existed since the original proposal by Kok and coworkers. As first formulated, the S state designation referred to the oxidation state of the O2-evolving center which could, in principle, include all of photosystem II and its associated components. Indeed, there are a number of redox-active components on the electron-donor side of photosystem II in addition to the Mn complex, such as the tyrosine radical that gives rise to EPR signal, and cytochrome b jg. 

Hammarstrom L, Styring S. Proton-coupled electron transfer of tyrosines in Photosystem II and model systems for artificial photosynthesis the role of a redox-active link between catalyst and photosensitizer. Energy Environ Sci. 2011 4 2379-88. 

Figure 3 The geometric arrangement of the redox active cofactors in Photosystem I and Photosystem II as given by the X-ray crystal structures PS I pdb entry IJBO (2) and PS II pdb entry 2AXT (3).

Redox-active amino acids are now recognized to play important roles in many biological electron-transfer reactions. In 1988, Bridgette Barry and Gerry Babcock" used EPR spectroscopy to demonstrate the involvement of an isotope-labeled radical in the water-splitting reaction in photosystem II of... 

ML Gilchrist, Jr., JA Ball, DW Randall and RD Britt (1995) Proximity of the manganese cluster of photosystem II to the redox-active tyrosine Yz- Proc Nat Acad Sci, USA 92 9545-9549... 

Photosystem II (PSII) is a large, heteromeric enzyme complex with more than twenty different protein subunits and an array of cofactors, that participate in the photosynthetic electron transport in the thylakoid membranes of chloroplasts and cyanobaaeria. PSII demonstrates the oxido-reductase aaivity and couples the oxidation of H2O with the reduction of plastoquinones through a series of intermediate redox reactions. The central core of the PSII reaction center is composed of D1 and D2 proteins associated >vith redox active components. These compounds include a tetra-manganese cluster, two redox-active residues, four to six chlorophyll a molecules, two pheophytins, and plastoquinones and The secondary plastoquinone Qg is a two-electron carrier which... 

Two water molecules are oxidized by four consecutive charge-separation reactions through photosystem II to form a molecule of diatomic oxygen and four hydrogen ions. The outcoming electron in each step is transferred to a redox-active tyrosine residue followed by the reduction of a photoxidized... 

In this section we look at ways in which Nature carries out redox chemistry with reference to blue copper proteins, iron-sulfur proteins and cytochromes. The redox steps in Photosystem II were outlined in the discussion accompanying equation 22.54. We have already discussed two topics of prime importance to electron transfer in Nature. The first is the way in which the reduction potential of a metal redox couple such as Fe +/Fe + can be tuned by altering the ligands coordinated to the metal centre. Look back at the values of for Fe +/Fe + redox couples listed in Table 8.1. The second is the discussion of Marcus-Hush theory in Section 26.5 this theory applies to electron transfer in bioinorganic systems where communication between redox active metal centres may be over relatively long distances as we shall illustrate in the following examples. 

Due to the probability of excitation energy from an absorbed photon to move from a closed to an open reaction center before being emitted as fluorescence, the relationship between the fluorescence quantum yield and the redox state of Qa is not linear. A correction to take into account this non-linear property (10) was not applied to Figure 1 since its applicability to inactive centers is questionable. Figure 1 thus does not give much information about the relative stoichiometries of photosystem II active and inactive centers. It is, however, an independent, rapid, non-invasive measurement upon an in vivo system which corroborates our earlier report (5) of the existence of a significant fraction of inactive photosystem II in vivo. It also confirms our earlier conclusion that the slow turnover rate of inactive centers is due to a very slow oxidation of Qa in these centers. 

Photosystem II contains two redox active tyrosines, Yp and Y, (1). Y acts as an electron conduit between the manganese cluster, where water oxidation occurs, and the primary donor of photosystem II, PssQ (2). The other redox-active tyrosine, Y, forms a stable radical and is oxidized and reduced by the manganese (3,4). These two radicals give rise to identical EPR spectra. Site-specific mutagenesis has recently demonstrated that Yp" " is tyrosine-160 of the D2 polypeptide (5,6) and that Y is tyrosine-161 of the D1 polypeptide (7,8). 

Photosystem II (PSII) contains a remarkably stable tyrosine radical D", located at tyr-160 in the D2 polypeptide, which exhibits a well-known electron paramagnetic resonance (EPR) spectrum, EPR Signal Ilg (1). The function of D" " in the mechanism of photosynthetic H2O oxidation remains unclear despite evidence that it can oxidize the Mn complex, the H20-oxidation catalyst in PSII, from the Sq state to the normally daik-stable Si state (2). Several studies indicate that die oxidation state of the Mn complex influences the electron spin-lattice relaxation rate of D" (3-5), perhaps via a weak dipolar coupling, as suggested by Evelo et al. (5). Hence, the relaxation properties of D may provide a probe for the topology of redox-active sites in the 02-evolving center (OEC) and of the magnetic properties of the Mn complex. 

Albeit the substantial progress in the bioelectrochemical activation of enzymes, one could identify two important future challenges in the field (i) The active relay units wiring the redox centers of the enzymes with the electrodes could be generated by photoinduced electron transfer. This could pave the way to the photochemical wiring of enzymes and to the development of photobiofuel cells, (ii) DNA scaffolds provide unique templates for the ordered self-assembly of molecular or biomolecular units through dictated hybridization. The ordering of relay units and enzymes, or of relay units photosystems, on DNA templates associated with electrodes may yield attractive new supramolecular nanostructures for bioelectronics and optobioelec tronic s. 

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