Philosophical Transactions of the Royal Society B: Biological Sciences
Restricted access

Using small molecule complexes to elucidate features of photosynthetic water oxidation

    The molecular oxygen produced in photosynthesis is generated via water oxidation at a manganese–calcium cluster called the oxygen-evolving complex (OEC). While studies in biophysics, biochemistry, and structural and molecular biology are well known to provide deeper insight into the structure and workings of this system, it is often less appreciated that biomimetic modelling provides the foundation for interpreting photosynthetic reactions. The synthesis and characterization of small model complexes, which either mimic structural features of the OEC or are capable of providing insight into the mechanism of O2 evolution, have become a vital contributor to this scientific field. Our group has contributed to these findings in recent years through synthesis of model complexes, spectroscopic characterization of these systems and probing the reactivity in the context of water oxidation. In this article we describe how models have made significant contributions ranging from understanding the structure of the water-oxidation centre (e.g. contributions to defining a tetrameric Mn3Ca-cluster with a dangler Mn) to the ability to discriminate between different mechanistic proposals (e.g. showing that the Babcock scheme for water oxidation is unlikely).

    References

    • Adelroth P, Lindberg K& Andréasson L.-E. 1995Studies of Ca2+ binding in spinach photosystem II using 45Ca2+. Biochemistry. 34, 9021–9027.doi:10.1021/bi00028a010. . Crossref, PubMed, ISIGoogle Scholar
    • Afrati T, Dendrinou-Samara C, Raptopoulou C.P, Terzis A, Tangoulis V& Kessissoglou D.P. 2002A tetranuclear mixed-valence Mn3IIMnIV compound with (μ4-O)Mn4 core. Angew. Chem. 41, 2148–2150.doi:10.1002/1521-3773(20020617)41:12<2148::AID-ANIE2148>3.0.CO;2-R. . Crossref, PubMed, ISIGoogle Scholar
    • Ahrling K.A, Peterson S& Styring S. 1997An oscillating manganese electron paramagnetic resonance signal from the S0 state of the oxygen evolving complex in photosystem II. Biochemistry. 36, 13 148–13 152.doi:10.1021/bi971815w. . Crossref, ISIGoogle Scholar
    • Alexiou M, et al.2003Models for the lower S states of photosystem II: a trinuclear mixed-valent MnII/MnIV/MnII complex. Inorg. Chem. 42, 2185–2187.doi:10.1021/ic026050h. . Crossref, PubMed, ISIGoogle Scholar
    • Bakou A, Buser C, Dandulakis G, Brudvig G& Ghanotakis D.F. 1992Calcium binding site(s) of photosystem II as probed by lanthanides. Biochim. Biophys. Acta. 1099, 131–136.doi:10.1016/0005-2728(92)90209-K. . CrossrefGoogle Scholar
    • Baldwin M.J, Gelasco A& Pecoraro V.L. 1993The effect of protonation on [Mn(IV)(μ2-O)]2 complexes. Photosynth. Res. 38, 303–308.doi:10.1007/BF00046754. . Crossref, PubMed, ISIGoogle Scholar
    • Baldwin M.J, Stemmler T.L, Riggs-Gelasco P.J, Kirk M.L, Penner-Hahn J.E& Pecoraro V.L. 1994Structural and magnetic effects of successive protonations of oxo bridges in high-valent manganese dimers. J. Am. Chem. Soc. 116, 11 349–11 356.doi:10.1021/ja00104a014. . Crossref, ISIGoogle Scholar
    • Bashkin J.S, Chang H.R, Streib W.E, Huffman J.C, Hendrickson D.N& Christou G. 1987Modelling the photosynthetic water oxidation center: preparation and physical properties of a tetranuclear oxide bridged manganese complex corresponding to the native S2 state. J. Am. Chem. Soc. 109, 6502–6504.doi:10.1021/ja00255a041. . Crossref, ISIGoogle Scholar
    • Bhaduri, S., Pink, M. & Christou, G. 2002 Towards a synthetic model of the photosynthetic water oxidizing complex: [Mn3O4(O2CMe)(4)(bpy)(2)] containing the [Mn-3(IV)(mu-O)(4)](4) core. Chem. Commun. 2352–2353. Google Scholar
    • Bhula R, Gainsford G.J& Weatherburn D.C. 1988A new model for the oxygen-evolving complex in photosynthesis. A trinuclear μ3-oxomanganese(III) complex which contains a μ-peroxo group. J. Am. Chem. Soc. 110, 7550–7552.doi:10.1021/ja00230a053. . Crossref, ISIGoogle Scholar
    • Bouwman E, Bolcar M.A, Libby E, Huffman J.C, Folting K& Christou G. 1992Tetranuclear manganese(III)-oxo-carboxylate complexes possessing terminal phenoxide or alkoxide ligands. Inorg. Chem. 31, 5185–5192.doi:10.1021/ic00051a008. . Crossref, ISIGoogle Scholar
    • Britt R.D, Campbell K.A, Peloquin J.M, Gilchrist M.L, Aznar C.P, Dicus M.M, Robblee J& Messinger J. 2004Recent pulsed EPR studies of the photosystem II oxygen- evolving complex: implications as to water oxidation mechanisms. Biochim. Biophys. Acta. 1655, 158–171.doi:10.1016/j.bbabio.2003.11.009. . Crossref, PubMed, ISIGoogle Scholar
    • Brudvig G.W& Crabtree R.H. 1986Mechanism for photosynthetic O2 evolution. Proc. Natl Acad. Sci. USA. 83, 4586–4588.doi:10.1073/pnas.83.13.4586. . Crossref, PubMed, ISIGoogle Scholar
    • Campbell K.A, Peloquin J.M, Pham D.P, Debus R.J& Britt R.D. 1998Parallel polarization EPR detection of an S1-state ‘Multiline’ EPR signal in photosystem II particles from Synechocystis sp. PCC 6803. J. Am. Chem. Soc. 120, 447–448.doi:10.1021/ja972693y. . Crossref, ISIGoogle Scholar
    • Casey J.L& Sauer K. 1984EPR detection of a cryogenically photogenerated intermediate in photosynthetic oxygen evolution. Biochim. Biophys. Acta. 767, 21–28.doi:10.1016/0005-2728(84)90075-6. . Crossref, ISIGoogle Scholar
    • Caudle M.T& Pecoraro V.L. 1997Thermodynamic viability of hydrogen atom transfer from water coordinated to the oxygen-evolving complex of photosystem II. J. Am. Chem. Soc. 119, 3415–3416.doi:10.1021/ja9641158. . Crossref, ISIGoogle Scholar
    • Caudle M.T, Riggs-Gelasco P, Gelasco A.K, Penner-Hahn J.E& Pecoraro V.L. 1996Mechanism for the homolytic cleavage of alkyl hydroperoxides by the manganese(III) dimer MnIII2(2-OHsalpn)2. Inorg. Chem. 35, 3577–3584.doi:10.1021/ic951462u. . Crossref, ISIGoogle Scholar
    • Chan M.K& Armstrong W.H. 1990Tetranuclear manganese-oxo complex with a 2.7 Å Mn–Mn separation and intramolecular H2O–μ2–O hydrogen-bonded contacts: [Mn4O2(TPHPN)2(H2O)2(CF3SO3)2](CF3SO3)3. Possible mode for binding of water at the active site of the oxygen-evolving complex in photosystem II. J. Am. Chem. Soc. 112, 4985–4986.doi:10.1021/ja00168a067. . ISIGoogle Scholar
    • Cheniae G.M& Martin I.F. 1970Sites of function of manganese within photosystem II. Biochim. Biophys. Acta. 197, 219–239.doi:10.1016/0005-2728(70)90033-2. . Crossref, PubMed, ISIGoogle Scholar
    • Cinco R.M, Robblee J.H, Rompel A, Fernandez C, Yachandra V.K, Sauer K& Klein M.P. 1998Strontium EXAFS reveals the proximity of calcium to the manganese cluster of oxygen-evolving photosystem II. J. Phys. Chem. B. 102, 8248–8256.doi:10.1021/jp981658q. . Crossref, PubMed, ISIGoogle Scholar
    • Collins T.J& Gordon-Wylie S.W. 1989A manganese(V)-oxo complex. J. Am. Chem. Soc. 111, 4511–4513.doi:10.1021/ja00194a063. . Crossref, ISIGoogle Scholar
    • Collins T.J, Powell R.D, Slebodnick C& Uffelman E.S. 1990A water-stable manganese(V)-oxo complex: definitive assignment of a ν(Mn–O) triple bond infrared vibration. J. Am. Chem. Soc. 112, 899–901.doi:10.1021/ja00158a077. . Crossref, ISIGoogle Scholar
    • Dau H, Iuzzolino L& Dittmer J. 2001The tetra-manganese complex during its redox cycle—X-ray absorption results and mechanistic implications. Biochim. Biophys. Acta. 1503, 24–39.doi:10.1016/S0005-2728(00)00230-9. . Crossref, PubMed, ISIGoogle Scholar
    • Dismukes G.C& Siderer Y. 1981Intermediates of a polynuclear manganese center involved in photosynthetic oxidation of water. Proc. Natl Acad. Sci. USA. 78, 274–278.doi:10.1073/pnas.78.1.274. . Crossref, PubMed, ISIGoogle Scholar
    • Ferreira K.N, Iverson T.M, Maghlaoui K, Barber J& Iwata S. 2004Architecture of the photosynthetic oxygen-evolving center. Science. 303, 1831–1838.doi:10.1126/science.1093087. . Crossref, PubMed, ISIGoogle Scholar
    • Gardner K.A& Mayer J.M. 1995Understanding C–H bond oxidations: H and H transfer in the oxidation of toluene by permanganate. Science. 269, 1849–1851.doi:10.1126/science.7569922. . Crossref, PubMed, ISIGoogle Scholar
    • Ghanotakis D.F, Topper J.N, Babcock G.T& Yocum C.F. 1984Water-soluble 17 and 23 kDa polypeptides restore oxygen evolution activity by creating a high-affinity binding site for Ca2+ on the oxidizing side of photosystem-II. FEBS Lett. 170, 169–173.doi:10.1016/0014-5793(84)81393-9. . Crossref, ISIGoogle Scholar
    • Gibney B.R, Wang H, Kampf J.W& Pecoraro V.L. 1996Structural evaluation and solution integrity of alkali metal salt complexes of the manganese 12-metallacrown-4 (12-MC-4) structural type. Inorg. Chem. 35, 6184–6193.doi:10.1021/ic960371+. . Crossref, ISIGoogle Scholar
    • Gupta R, MacBeth C.E, Young V.G& Borovik A.S. 2002Isolation of monomeric MnIII/II–OH and MnIII–O complexes from water: evaluation of O–H bond dissociation energies. J. Am. Chem. Soc. 124, 1136–1137.doi:10.1021/ja016741x. . Crossref, PubMed, ISIGoogle Scholar
    • Han K& Katoh S. 1993Different localization of 2 Ca2+ in spinach oxygen-evolving photosystem II membranes—evidence for involvement of only one Ca2+ in oxygen evolution. Plant Cell Physiol. 34, 585. ISIGoogle Scholar
    • Haumann M, Liebisch P, Muller C, Barra M, Grabolle M& Dau H. 2005Photosynthetic O2 formation tracked by time-resolved X-ray experiments. Science. 310, 1019–1021.doi:10.1126/science.1117551. . Crossref, PubMed, ISIGoogle Scholar
    • Hillier W, Messinger J& Wydrzynski T. 1998Kinetic determination of the fast exchanging substrate water molecule in the S3 state of photosystem II. Biochemistry. 37, 16 908–16 914.doi:10.1021/bi980756z. . Crossref, ISIGoogle Scholar
    • Hillier W, Hendry G, Burnap R.L& Wydrzynski T. 2001Substrate water exchange in photosystem II depends on the peripheral proteins. J. Biol. Chem. 276, 46 917–46 924.doi:10.1074/jbc.M102954200. . Crossref, ISIGoogle Scholar
    • Hillier W& Wydrzynski T. 2000The affinities for the two substrate water binding sites in the O(2) evolving complex of photosystem II vary independently during S-state turnover. Biochemistry. 39, 4399–4405. Crossref, PubMed, ISIGoogle Scholar
    • Hoganson C.W& Babcock G.T. 1997A metalloradical mechanism for the generation of oxygen in photosynthesis. Science. 277, 1953–1956.doi:10.1126/science.277.5334.1953. . Crossref, PubMed, ISIGoogle Scholar
    • Homann P.H. 2002Chloride and calcium in photosystem II: from effects to enigma. Invited contribution. Photosynth. Res. 73, 169–175.doi:10.1023/A:1020486729283. . Crossref, PubMed, ISIGoogle Scholar
    • Hsieh W.Y, Campbell K.A, Gregor W, Britt R.D, Yoder D.W, Penner-Hahn J.E& Pecoraro V.L. 2004The first spectroscopic model for the S-1 state multiline signal of the OEC. Biochim. Biophys. Acta. 1655, 149–157.doi:10.1016/j.bbabio.2003.12.001. . Crossref, PubMed, ISIGoogle Scholar
    • Kessissoglou, D. P., Kirk, M. L., Bender, C. A., Lah, M. S. & Pecoraro, V. L. 1989 A bent mixed valence Mn(III/II/III) complex: a new class of trinuclear, acetate bridged Schiff base compounds exhibiting a g=2 multiline ESR sig. J. Chem. Soc. Chem. Commun. 84–86. Google Scholar
    • Kessissoglou D.P, Kirk M.L, Lah M.S, Li X, Raptopoulou C, Hatfield W.E& Pecoraro V.L. 1992Structural and magnetic characterization of trinuclear, mixed-valence manganese acetates. Inorg. Chem. 31, 5424–5432.doi:10.1021/ic00052a018. . Crossref, ISIGoogle Scholar
    • Kim D.H, Britt R.D, Klein M.P& Sauer K. 1990The g=4.1 EPR signal of the S2 state of the photosynthetic oxygen-evolving complex arises from a multinuclear manganese cluster. J. Am. Chem. Soc. 112, 9389–9391.doi:10.1021/ja00181a049. . Crossref, ISIGoogle Scholar
    • Kitajima N, Osawa M, Imai S, Fujisawa K, Morooka Y, Heerwegh K, Reed C.A& Boyd P.D.W. 1994Synthesis, structure and magnetic properties of a linear trimanganese(III,II,III) complex bridged with a (μ-hydroxo)bis(μ-acetato) unit. Inorg. Chem. 33, 4613–4614.doi:10.1021/ic00099a004. . Crossref, ISIGoogle Scholar
    • Kulik Leonid V, Epel B, Lubitz W& Messinger J. 200555Mn pulse ENDOR at 34 GHz of the S0 and S2 states of the oxygen-evolving complex in photosystem II. J. Am. Chem. Soc. 127, 2392–2393.doi:10.1021/ja043012j. . Crossref, PubMed, ISIGoogle Scholar
    • Lah M.S& Pecoraro V.L. 1989Isolation and characterization of {MnII[MnIII(salicylhydroximate)]4(acetate)2(DMF)6}.cntdot.2DMF: an inorganic analog of Mn2+ (12-crown-4). J. Am. Chem. Soc. 111, 7258–7259.doi:10.1021/ja00200a054. . Crossref, ISIGoogle Scholar
    • Larson, E. J., Riggs, P. J., Penner-Hahn, J. E.& Pecoraro, V. L. 1992 Protonation of (Mniv(Saltn)(Mu-2-O))2 results in significant modification of structure and catalase-like reactivity. J. Chem. Soc. Chem. Commun. 102–103. Google Scholar
    • Law N.A, Caudle M.T& Pecoraro V.L. 1998Manganese redox enzymes and model systems: properties, structures, and reactivity. Adv. Inorg. Chem. 46, 305–440. Crossref, ISIGoogle Scholar
    • Libby E, Folting K, Huffman J.C& Christou G. 1990Feasibility of a ‘building-block’ approach to higher nuclearity manganese/oxygen/RCO2- aggregates: directed conversion of an [Mn4O2] to an [Mn8O4] complex. J. Am. Chem. Soc. 112, 5354–5356.doi:10.1021/ja00169a055. . Crossref, ISIGoogle Scholar
    • Libby E, McCusker J.K, Schmitt E.A, Folting K, Hendrickson D.N& Christou G. 1991Preparation and properties of models for the photosynthetic water oxidation center: spin frustration in the manganese [Mn4O2(O2CR)7(pic)2]- anion. Inorg. Chem. 30, 3486–3495.doi:10.1021/ic00018a019. . Crossref, ISIGoogle Scholar
    • Lindberg K& Andreasson L.E. 1996A one-site, two-state model for the binding of anions in photosystem II. Biochemistry. 35, 14 259–14 267.doi:10.1021/bi961244s. . Crossref, ISIGoogle Scholar
    • Loll B, Kern J, Saenger W, Zouni A& Biesiadka J. 2005Towards complete cofactor arrangement in the 3.0 Å resolution structure of photosystem II. Nature. 438, 1040–1044.doi:10.1038/nature04224. . Crossref, PubMed, ISIGoogle Scholar
    • Lundberg M& Siegbahn P.E.M. 2004Investigations of structure and mechanism of the oxygen evolving complex in PSII. Phys. Chem. Chem. Phys. 6, 4772–4780.doi:10.1039/b406552b. . Crossref, ISIGoogle Scholar
    • McEvoy J.P& Brudvig G.W. 2006Water-splitting chemistry of photosystem II. Chem. Rev. 106, 4455–4483.doi:10.1021/cr0204294. . Crossref, PubMed, ISIGoogle Scholar
    • Messinger J, Robblee J, Yu W.O, Sauer K, Yachandra V.K& Klein M.P. 1997The S0 state of the oxygen-evolving complex in photosystem II is paramagnetic: detection of an EPR multiline signal. J. Am. Chem. Soc. 119, 11 349–11 350.doi:10.1021/ja972696a. . Crossref, ISIGoogle Scholar
    • Meyer T.J, Huynh M.H.V& Thorp H.H. 2007The possible role of proton-coupled electron transfer (PCET) in water oxidation by photosystem II. Angew. Chem. Int. Ed. Engl. 46, 5284–5304.doi:10.1002/anie.200600917. . Crossref, PubMed, ISIGoogle Scholar
    • Miller C.G, Gordon-Wylie S.W, Horwitz C.P, Strazisar S.A, Peraino D.K, Clark G.R, Weintraub S.T& Collins T.J. 1998A method for driving O-atom transfer: secondary ion binding to a tetraamide macrocyclic ligand. J. Am. Chem. Soc. 120, 11 540–11 541.doi:10.1021/ja972922g. . Crossref, ISIGoogle Scholar
    • Mukherjee, C., Weyhermueller, T., Wieghardt, K. & Chaudhuri, P. 2006 A trinuclear complex containing MnIIMnIIIMnIV, radicals, quinone and chloride ligands potentially relevant to PS II. Dalton Trans. 2169–2171. Google Scholar
    • Mukhopadhyay S, Mandal S.K, Bhaduri S& Armstrong W.H. 2004Manganese clusters with relevance to photosystem II. Chem. Rev. 104, 3981–4026.doi:10.1021/cr0206014. . Crossref, PubMed, ISIGoogle Scholar
    • Pecoraro, V. L. & Hsieh, W. Y. 2000 The use of model complexes to elucidate the structure and function of manganese redox enzymes. In Metal ions in biological systems, vol. 37 (eds H. Sigel & A. Sigel), pp. 429–504. New York, NY: Marcel-Dekker. Google Scholar
    • Pecoraro V.L, Baldwin M.J& Gelasco A. 1994Interaction of manganese with dioxygen and its reduced derivatives. Chem. Rev. 94, 807–826.doi:10.1021/cr00027a012. . Crossref, ISIGoogle Scholar
    • Pecoraro, V. L., Stemmler, A. J., Gibney, B. R., Bodwin, J. J., Wang, H., Kampf, J. W. & Almut, B. 1997 Progress in inorganic chemistry, vol. 45 (ed. K. D. Karlin), pp. 83–177. New York, NY: Wiley & Sons. Google Scholar
    • Pecoraro V.L, Baldwin M.J, Caudle M.T, Hsieh W.-Y& Law N.A. 1998A proposal for water oxidation in photosystem II. Pure Appl. Chem. 70, 925–929. Crossref, ISIGoogle Scholar
    • Peloquin J.M, Campbell K.A, Randall D.W, Evanchik M.A, Pecoraro V.L, Armstrong W.H& Britt R.D. 200055Mn ENDOR of the S2-state multiline EPR signal of photosystem II: implications on the structure of the tetranuclear Mn cluster. J. Am. Chem. Soc. 122, 10 926–10 942.doi:10.1021/ja002104f. . Crossref, ISIGoogle Scholar
    • Penner-Hahn J.E, Fronko R.M, Pecoraro V.L, Yocum C.F, Betts S.D& Bowlby N.R. 1990Structural characterization of the manganese sites in the photosynthetic oxygen-evolving complex using X-ray absorption spectroscopy. J. Am. Chem. Soc. 112, 2549–2557.doi:10.1021/ja00163a011. . Crossref, ISIGoogle Scholar
    • Popelkova H, Betts S.D, Lydakis-Symantiris N, Im M.M, Swenson E& Yocum C.F. 2006Mutagenesis of basic residues R151 and R161 in manganese-stabilizing protein of photosystem II causes inefficient binding of chloride to the oxygen-evolving complex. Biochemistry. 45, 3107–3115.doi:10.1021/bi0523759. . Crossref, PubMed, ISIGoogle Scholar
    • Poulsen A.K, Rompel A& McKenzie C.J. 2005Water oxidation catalysed by a dinuclear Mn complex: a new model for the oxygen evolving center of photosystem II. Angew. Chem. 44, 6916–6920.doi:10.1002/anie.200502114. . Crossref, PubMed, ISIGoogle Scholar
    • Proserpio D.M, Hoffmann R& Dismukes G.C. 1992Molecular mechanism of photosynthetic oxygen evolution. A theoretical approach. J. Am. Chem. Soc. 114, 4374–4382.doi:10.1021/ja00037a052. . Crossref, ISIGoogle Scholar
    • Riggs-Gelasco P.J, Mei R, Ghanotakis D.F, Yocum C.F& Penner-Hahn J.E. 1996X-ray absorption spectroscopy of calcium-substituted derivatives of the oxygen-evolving complex of phostosytem II. J. Am. Chem. Soc. 118, 2400–2410.doi:10.1021/ja9504505. . Crossref, ISIGoogle Scholar
    • Robblee J.H, Cinco R.M& Yachandra V.K. 2001X-ray spectroscopy-based structure of the Mn cluster and mechanism of photosynthetic oxygen evolution. Biochim. Biophys. Acta. 1503, 7–23.doi:10.1016/S0005-2728(00)00217-6. . Crossref, PubMed, ISIGoogle Scholar
    • Ruettinger W, Yagi M, Wolf K, Bernasek S& Dismukes G.C. 2000O2 evolution from the manganese-oxo cubane core Mn4O46+: a molecular mimic of the photosynthetic water oxidation enzyme?. J. Am. Chem. Soc. 122, 10 353–10 357.doi:10.1021/ja0005587. . Crossref, ISIGoogle Scholar
    • Sauer K. 1980A role for manganese in oxygen evolution in photosynthesis. Acc. Chem. Res. 13, 249–256.doi:10.1021/ar50152a001. . Crossref, ISIGoogle Scholar
    • Siegbahn P.E.M& Blomberg M.R.A. 2005Methods and models for studying mechanisms of redox-active enzymes. Phil. Trans. R. Soc. A. 363, 847–860.doi:10.1098/rsta.2004.1542. . Link, ISIGoogle Scholar
    • Tagore R, Chen H, Crabtree R.H& Brudvig G.W. 2006Determination of μ-oxo exchange rates in di-μ-oxo dimanganese complexes by electrospray ionization mass spectrometry. J. Am. Chem. Soc. 128, 9457–9465.doi:10.1021/ja061348i. . Crossref, PubMed, ISIGoogle Scholar
    • Tagore R, Crabtree R.H& Brudvig G.W. 2007Distinct mechanisms of bridging-oxo exchange in di-μ-O dimanganese complexes with and without water-binding sites: implications for water binding in the O2-evolving complex of photosystem II. Inorg. Chem. 46, 2193–2203.doi:10.1021/ic061968k. . Crossref, PubMed, ISIGoogle Scholar
    • Tangoulis V, Malamatari D.A, Soulti K, Stergiou V, Raptopoulou C.P, Terzis A, Kabanos T.A& Kessissoglou D.P. 1996Manganese(II/II/II) and manganese(III/II/III) trinuclear compounds, structure and solid and solution behavior. Inorg. Chem. 35, 4974–4983.doi:10.1021/ic960183j. . Crossref, PubMed, ISIGoogle Scholar
    • Tommos C, Tang X.-S, Warncke K, Hoganson C.W, Styring S, McCracken J, Diner B.A& Babcock G.T. 1995Spin-density distribution, conformation, and hydrogen bonding of the redox-active tyrosine YZ in photosystem II from multiple-electron magnetic-resonance spectroscopies: implications for photosynthetic oxygen evolution. J. Am. Chem. Soc. 117, 10 325–10 335.doi:10.1021/ja00146a017. . Crossref, ISIGoogle Scholar
    • van Gorkom H.J& Yocum C.FThe calcium and chloride cofactors. Photosystem II: the light-driven water: plastoquinone oxidoreductase. , Wydrzynski T.J& Satoh KAdvances in photosynthesis and respiration vol. 222005pp. 307–328. Eds. Dordrecht, The Netherlands:Springer. Google Scholar
    • Vincent J.B, Christmas C, Chang H.R, Li Q, Boyd P.D.W, Huffman J.C, Hendrickson D.N& Christou G. 1989Modeling the photosynthetic water oxidation center preparation and properties of tetranuclear manganese complexes containing [Mn4O2]6+,7+,8+ cores, and the crystal structures of Mn4O2(O2CMe)6(bipy)2 and [Mn4O2(O2CMe)7(bipy)2](ClO4). J. Am. Chem. Soc. 111, 2086–2097.doi:10.1021/ja00188a023. . Crossref, ISIGoogle Scholar
    • Waggoner C.M, Pecoraro V& Yocum C.F. 1989Mono-valent cations (Na+, K+, Cs+) inhibit calcium activation of photosynthetic oxygen evolution. FEBS Lett. 244, 237–240.doi:10.1016/0014-5793(89)81200-1. . Crossref, ISIGoogle Scholar
    • Wieghardt K. 1989Die aktiven Zentren in manganhaltigen Metalloproteinen und anorganische Modellkomplexe. Angew. Chem. 101, 1179–1198.doi:10.1002/ange.19891010905. . CrossrefGoogle Scholar
    • Wieghardt K, Bossek U, Nuber B, Weiss J, Gehring S& Haase W. 1988Synthesis of novel trimeric μ-oxo-bridged manganese (IV) complexes: [L3Mn3IV2-O)33-XO4)]Br3(X=P, As, or Vv; L=1, 4, 7-triazacyclononane). J. Chem. Soc. Chem. Commun. 17, 1145–1146.doi:10.1039/C39880001145. . CrossrefGoogle Scholar
    • Wincencjusz H, Yocum C.F& van Gorkom H.J. 1999Activating anions that replace Cl in the O2-evolving complex of photosystem II slow the kinetics of the terminal step in water oxidation and destabilize the S2 and S3 states. Biochemistry. 38, 3719–3725.doi:10.1021/bi982295n. . Crossref, PubMed, ISIGoogle Scholar
    • Wu A.J, Penner-Hahn J.E& Pecoraro V.L. 2004Structural, spectroscopic, and reactivity models for the manganese catalases. Chem. Rev. 104, 903–938.doi:10.1021/cr020627v. . Crossref, PubMed, ISIGoogle Scholar
    • Wydrzynski TPhotosystem II: the light-driven water: plastoquinone oxidoreductase. 2005Dordrecht, The Netherlands:Springer. Google Scholar
    • Yachandra V.KThe catalytic manganese cluster: organization of the metal ions. Photosystem II: the light-driven water: plastoquinone oxidoreductase. , Wydrzynski T.J& Satoh KAdvances in photosynthesis and respiration vol. 222005pp. 235–260. Eds. Dordrecht, The Netherlands:Springer. Google Scholar
    • Yachandra V.K, DeRose V.J, Latimer M.J, Mukerji I, Sauer K& Klein M.P. 1993Where plants make oxygen: a structural model for the photosynthetic oxygen-evolving manganese cluster. Science. 260, 675–679.doi:10.1126/science.8480177. . Crossref, PubMed, ISIGoogle Scholar
    • Yachandra V.K, Sauer K& Klein M.P. 1996Manganese cluster in photosynthesis: where plants oxidize water to dioxygen. Chem. Rev. 96, 2927–2950.doi:10.1021/cr950052k. . Crossref, PubMed, ISIGoogle Scholar
    • Yano S, Doi M, Tamakoshi S, Mori W, Mikuriya M, Ichimura A, Kinoshita I, Yamamoto Y& Tanase T. 1997Trimanganese complexes with a linear MnIIMnIII MnII assemblage bridged by carbohydrates. Chem. Commun997–998.doi:10.1039/a701198i. . Crossref, ISIGoogle Scholar
    • Yano J, et al.2006Where water is oxidized to dioxygen: Structure of the photosynthetic Mn4Ca cluster. Science. 314, 821–825.doi:10.1126/science.1128186. . Crossref, PubMed, ISIGoogle Scholar
    • Yocum C.Fp. 71 Eds. & Pecoraro V.L. 1992New York, NY:VCH. Google Scholar
    • Yocum C.F& Pecoraro V.L. 1999Recent advances in the understanding of the biological chemistry of manganese. Curr. Opin. Chem. Biol. 3, 182–187.doi:10.1016/S1367-5931(99)80031-3. . Crossref, PubMed, ISIGoogle Scholar
    • Yocum C.F, Yerkes C.T, Blankenship R.E, Sharp R.R& Babcock G.T. 1981Stoichiometry, inhibitor sensitivity, and organization of manganese associated with photosynthetic oxygen evolution. Proc. Natl Acad. Sci. USA. 78, 7507–7511.doi:10.1073/pnas.78.12.7507. . Crossref, PubMed, ISIGoogle Scholar
    • Zaleski, C. M., Dendrinou-Samara, C., Alexiou, M., Kanakaraki, P., Kampf, J., Penner Hahn, J. E., Pecoraro, V. L. & Kessissoglou, D. P. Submitted. Structural and XANES features of tetranuclear [MnSII MnIV] and [Mn2II Mn2III] valence-isomers of manganese clusters. Google Scholar
    • Zouni A, Jordan R, Schlodder E, Fromme P& Witt H.T. 2000First photosystem II crystals capable of water-oxidation. Biochim. Biophys. Acta. 1457, 103–105.doi:10.1016/S0005-2728(00)00100-6. . Crossref, PubMed, ISIGoogle Scholar
    • Zouni A, Witt H.-T, Kern J, Fromme P, Krauss N, Saenger W& Orth P. 2001Crystal structure of oxygen evolving photosystem II from Synechococcus elongatus: a 3.8 Å resolution. Nature. 409, 739–743.doi:10.1038/35055589. . Crossref, PubMed, ISIGoogle Scholar

    Additional reference

    • Hillier, W. & Messinger, J. 2005 Mechanism of photosynthetic oxygen production. In: Photosystem II. The light-driven water: plastoquinone oxidoreductase, advances in Photosynthesis and Respiration, vol. 22 (eds T. Wydrzynski, and K. Satoh), pp. 567–608. Springer: Netherlands. Google Scholar
    • Messinger J, Badger M& Wydrzynski T. 1995Detection of one slowly exchanging substrate water molecule in the S3 state of photosystem II. Proc Natl Acad Sci USA. 92, 3209–3213.doi:10.1073/pnas.92.8.3209. . Crossref, PubMed, ISIGoogle Scholar
    • Messinger J. 2004Evaluation of different mechanistic proposals for water oxidation in photosynthesis on the basis of Mn4OxCa structures for the catalytic site and spectroscopic data. Phys. Chem. Chem. Phys. 6, 4764–4771.doi:10.1039/b406437b. . Crossref, ISIGoogle Scholar
    • Weng T.C, Hsieh W.Y, Uffelman E.S, Gordon-Wylie S.W, Collins T.J, Pecoraro V.L& Penner-Hahn J.E. 2004XANES evidence against a manganyl species in the S3 state of the oxygen-evolving complex. J. Am. Chem. Soc. 126, 8070–8071.doi:10.1021/ja0494104. . Crossref, PubMed, ISIGoogle Scholar