Using small molecule complexes to elucidate features of photosynthetic water oxidation
Abstract
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, ISI, Google ScholarAfrati 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, ISI, Google ScholarAhrling 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, ISI, Google ScholarAlexiou M, 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, ISI, Google ScholarBakou 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. . Crossref, Google ScholarBaldwin 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, ISI, Google ScholarBaldwin 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, ISI, Google ScholarBashkin 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, ISI, Google 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, ISI, Google ScholarBouwman 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, ISI, Google ScholarBritt 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, ISI, Google ScholarBrudvig 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, ISI, Google ScholarCampbell 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, ISI, Google ScholarCasey 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, ISI, Google ScholarCaudle 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, ISI, Google ScholarCaudle 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, ISI, Google ScholarChan 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. . ISI, Google ScholarCheniae 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, ISI, Google ScholarCinco 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, ISI, Google ScholarCollins T.J& Gordon-Wylie S.W . 1989A manganese(V)-oxo complex. J. Am. Chem. Soc. 111, 4511–4513.doi:10.1021/ja00194a063. . Crossref, ISI, Google ScholarCollins 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, ISI, Google ScholarDau 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, ISI, Google ScholarDismukes 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, ISI, Google ScholarFerreira 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, ISI, Google ScholarGardner 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, ISI, Google ScholarGhanotakis 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, ISI, Google ScholarGibney 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, ISI, Google ScholarGupta 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, ISI, Google ScholarHan 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. ISI, Google ScholarHaumann 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, ISI, Google ScholarHillier 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, ISI, Google ScholarHillier 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, ISI, Google ScholarHillier 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, ISI, Google ScholarHoganson 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, ISI, Google ScholarHomann 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, ISI, Google ScholarHsieh 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, ISI, Google 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, ISI, Google ScholarKim 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, ISI, Google ScholarKitajima 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, ISI, Google ScholarKulik 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, ISI, Google ScholarLah 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, ISI, Google 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, ISI, Google ScholarLibby 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, ISI, Google ScholarLibby 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, ISI, Google ScholarLindberg 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, ISI, Google ScholarLoll 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, ISI, Google ScholarLundberg 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, ISI, Google ScholarMcEvoy J.P& Brudvig G.W . 2006Water-splitting chemistry of photosystem II. Chem. Rev. 106, 4455–4483.doi:10.1021/cr0204294. . Crossref, PubMed, ISI, Google ScholarMessinger 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, ISI, Google ScholarMeyer 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, ISI, Google ScholarMiller 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, ISI, Google 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, ISI, Google 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, ISI, Google 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, ISI, Google ScholarPeloquin 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, ISI, Google ScholarPenner-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, ISI, Google ScholarPopelkova 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, ISI, Google ScholarPoulsen 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, ISI, Google ScholarProserpio 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, ISI, Google ScholarRiggs-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, ISI, Google ScholarRobblee 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, ISI, Google ScholarRuettinger 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, ISI, Google ScholarSauer K . 1980A role for manganese in oxygen evolution in photosynthesis. Acc. Chem. Res. 13, 249–256.doi:10.1021/ar50152a001. . Crossref, ISI, Google ScholarSiegbahn 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, ISI, Google ScholarTagore 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, ISI, Google ScholarTagore 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, ISI, Google ScholarTangoulis 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, ISI, Google ScholarTommos 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, ISI, Google Scholarvan Gorkom H.J& Yocum C.F The calcium and chloride cofactors. Photosystem II: the light-driven water: plastoquinone oxidoreductase., Wydrzynski T.J& Satoh K Advances in photosynthesis and respiration vol. 222005pp. 307–328. Eds. Dordrecht, The Netherlands:Springer. Google ScholarVincent 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, ISI, Google ScholarWaggoner 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, ISI, Google ScholarWieghardt K . 1989Die aktiven Zentren in manganhaltigen Metalloproteinen und anorganische Modellkomplexe. Angew. Chem. 101, 1179–1198.doi:10.1002/ange.19891010905. . Crossref, Google ScholarWieghardt K, Bossek U, Nuber B, Weiss J, Gehring S& Haase W . 1988Synthesis of novel trimeric μ-oxo-bridged manganese (IV) complexes: [L3Mn3IV(μ2-O)3(μ3-XO4)]Br3(X=P, As, or Vv; L=1, 4, 7-triazacyclononane). J. Chem. Soc. Chem. Commun. 17, 1145–1146.doi:10.1039/C39880001145. . Crossref, Google ScholarWincencjusz 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, ISI, Google ScholarWu 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, ISI, Google ScholarWydrzynski T Photosystem II: the light-driven water: plastoquinone oxidoreductase. 2005Dordrecht, The Netherlands:Springer. Google ScholarYachandra V.K The catalytic manganese cluster: organization of the metal ions. Photosystem II: the light-driven water: plastoquinone oxidoreductase., Wydrzynski T.J& Satoh K Advances in photosynthesis and respiration vol. 222005pp. 235–260. Eds. Dordrecht, The Netherlands:Springer. Google ScholarYachandra 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, ISI, Google ScholarYachandra 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, ISI, Google ScholarYano 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, ISI, Google ScholarYano J, 2006Where water is oxidized to dioxygen: Structure of the photosynthetic Mn4Ca cluster. Science. 314, 821–825.doi:10.1126/science.1128186. . Crossref, PubMed, ISI, Google ScholarYocum 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, ISI, Google ScholarYocum 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, ISI, Google 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, ISI, Google ScholarZouni 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, ISI, Google Scholar
- 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, ISI, Google ScholarMessinger 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, ISI, Google ScholarWeng 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, ISI, Google Scholar


