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Functional Properties of the Oxygen Evolving Complexof Photosystem 11" Doorpieter Van Vliet, 15April 1996

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Functional Properties of the Oxygen Evolving Complexof Photosystem 11 Functional propertieso fth eoxyge nevolvin gcomple x ofphotosyste mI I Promoter: dr.T.J . Schaafsma,hoogleraa r in demoleculair e fysica. Co-promotor: dr. A.W.Rutherford , directeur derecherch e CNRS,Gif-sur-Yvette . ( r > *!-,.„•?o ! Q0 o: -/<X r P.H. van Vliet Functionalpropertie s ofth e oxygenevolvin gcomple x ofphotosyste m II Proefschrift ter verkrijging van degraa d van doctor in de landbouw- en milieuwetenschappen, op gezagva n de rector magnificus, dr. CM. Karssen, in het openbaar te verdedigen op maandag 15apri l 1996 des namiddags te vier uur in de Aula van de Landbouwuniversiteit te Wageningen. Y-MQ^\'b^ VoorLeontin e BIBIiOTHEEX LANDBOUWUNlVERSTTiaT WAGENINGEN CIP-DATAKONINKL0K E BIBLIOTHEEK, DEN HAAG Vliet,P.H .va n Functionalpropertie so fth eoxyge n evolvingcomple xo f photosystemn /P.H . vanVliet .- [S.l.: s.nj . -m . ThesisLandbouwuniversitei tWageningen .- Wit href .- Withsummar yi nDutch . ISBN 90-5485-532-0 Subject headings:photosynthesi s / oxygen evolution. Stellingen 1 Itca n notb eexclude d thatsom eo f thechange si nth e S2minu s SjFTI R spectrum observed byNoguch i etal. i nPhotosyste mI Iafte r Ca2+depletio n bylo wp Htreatmen ti n thepresenc e ofcitrate ,originat efro m binding ofcitrat et oPS-I I(Noguchi ,T. ,Ono ,T .& Inoue,Y . (1995)Biochim. Biophys. Acta1228, 189-200) . 2 Theconclusio n byKusunok i thatth eEP R signalfro m theS 3 statei nCa 2+-depleted PS-II originates from aperoxid eradica li sno t sufficiently supported byexperimenta l data (Kusunoki,M .(1995 ) Chem. Phys. Letters239, 148-157) . 3 Invie w of therepor tb yDeligiannakL set al., i ti smos tstraightforwar d toconside rth e acceptor component "D4go" inPhotosyste mI Idescribe d by Stemleran dJursini c asth e non-heme iront owhic h formate isboun d (Deligiannakis,Y. , Petrouleas,V . &Diner ,B .A . (1994)Biochim. Biophys. Acta1188, 260-270;Stemler ,A .& Jursinic ,P .A .(1993 ) Biochim. Biophys. Acta1183, 269-280). 4 Incontras tt owha ti sgenerall y thought,th eF ~anio nca nfunctionall y occupy theCl~-sit e inPhotosyste mI Iessentia l for oxygen evolvingactivit y(this Thesis, Chapter4) . 5 Theelectro nmicroscop y studyo ftwo-dimensiona lcrystal s ofPhotosyste mI Ib yFor det al. does not sufficiently ruleou tth epossibilit y thatth eregio ni nTris-washe d Photosystem IIwhic hi sassigne d toa micro-cavity ,i sunstaine dprotei n (Ford,R .C , Rosenberg,M . F, Shepherd,F .H. ,McPhie ,P .& Holzenburg ,A .(1995 )Micron 26, 133-140) . 6 Theobservatio n byLindber g etal. of aresidua l oxygenevolvin g activity inPhotosyste m IIafte r releaseo f allexchangeabl e Cl~followin g longincubatio n in aCl~-fre e buffer- solution atp H6.3 ,i sconsisten twit hthei rearlie rrepor t whichindicate d thepresenc eo fa fraction ofcenter scontainin g Cl~whic h isno texchangeabl e underthes e conditions (Lindberg,K. ,Wydrzynski ,T. ,Vanngard ,T. ,& Andreasson ,L-E .(1990 )FEBSLett. 264, 153-155;Lindberg ,K. ,Vanngard ,T. ,& Andreasson ,L-E .(1993 )Photosynth. Res.38, 401-408). 7 Theassumptio n byRobert s andLindah l thata significan t fraction ofth epurifie d nickel- ironhydrogenas e contains anicke lio nwhic hi sEP Rsilen tunde ral lcondition s anddoe s notchang eit soxidatio n stateupo n lowering of theredoxpotential ,implie stha tthi s fraction exhibits nohydrogenas eactivit y (Roberts,L .M. ,& Lindahl ,P .A .(1994 ) Biochemistry 33, 14339-14350). 8 Measurements of thelight-intensit y dependent 820n mabsorbanc echange si nleave sma y yield information onelectro ndono revent st oth ereactio n centero fPhotosyste mI invivo. 9 Extensivepublicit y given topossibl enegativ eclimati ceffect s causedb yeart h atmospheric pollution,wil lcontinu eunti lal lterrestria l oil sources havebee nexhausted . Stellingen behorendbij het proefschrift "Functional properties of the Oxygen Evolving Complexof Photosystem 11" doorPieter van Vliet, 15april 1996. Preface Iwoul d liket othan kal lth epeopl ewh odirectl yo rindirectl y contributed tothi sThesis . Itwa sa grea t pleasuret owor ki nth e groupo f BillRutherford . Bill's support andenthousias m wereenormous .Th ediscussion s thatw eha d of experiments,editoria l aspects andabou tman y othersubjects , Ienjoye d very much. Tjeerd Schaafsma gave a great deal of support by constructive discussions and very useful adviceo neditoria l aspects.Th evisit st oth eDepartmen t ofMolecula rPhysic sI enjoyed very much and I experienced them as a confirmation of the fruitful link between Saclay and Wageningen. Paul Mathis gave me the important support that I required to work in the Section de Bioenergenquei n Saclay and healway s showed hisinteres t in mywork . Significant contributions to this Thesis came also from Alain Boussac, Sun Un and Andreas Seidler.Th eman y discussions with them werequit e useful. Although I spent most of my time in Saclay in complete darkness, working there was big fun atleas t in partdu et oth emusi c partiesa tBill' s place andth eplayin g biljart after work now and then with (among others) Klaus Brettel,Andrea s Seidler andWinfrie d Leibl.I never figured out, though, howAndrea s was able on certain evenings to,beside s playing very well, systematically leavem e themos tunfavourabl e ball positions imaginable. Significant support I received from Jacintha who decided tojoi n me and to work in France. Family and friends showed continuous interest in us and visited us frequently in France.Fro m Marry and Dick van Vliet,an d Miep andTo nVerd uw ereceive d significant and specialsuppor t in many different ways.Thi sinclude d designing theimag e onth ecove r ofthi s Thesis byTo nVerdu . Contents page Abbreviations 1 1 Introduction 2 2 Overview andrational e ofmethod s and techniques used. 11 3 Chloride-depletion effects in the Calcium-deficient Oxygen Evolving 16 Complex of Photosystem II (Van Vliet, P., Boussac, A., & Rutherford A.W. (1994)Biochemistry 33, 12998-13004). 4 Properties of the Chloride-Depleted Oxygen Evolving Complex of 32 Photosystem II studied by EPR (Van Vliet, P. & Rutherford A.W. (1996) Biochemistry, inpress) . 5 Properties of the Iodide-Reconstituted Oxygen Evolving Complex of 58 Photosystem II studied by EPR (Van Vliet, P., Homann, P.H. & Rutherford A.W. , inpreparation) . 6 On the magnetic properties Oxygen Evolving Complex of Photosystem II 71 studied by EPR (Van Vliet,P .& Rutherfor d A.W. (1996),i npreparation) . 7 On the magnetic properties of the Chloride-Depleted Oxygen Evolving 85 Complex of Photosystem II studied by EPR (Van Vliet, P., Un, S. & Rutherford A.W. (1996),i npreparation) . Summary 95 Samenvatting 98 Abbreviations ATP adenosine triphosphate CW continuous wave EPR electron paramagnetic resonance Mn manganese NADP nicotinamide adenine dinucleotide phosphate P primary electron donor Peso primary electron donor of photosystem II P700 primary electron donor of photosystem I PPBQ phenyl-p-benzoquinone PS photosystem QA, QB primary and secondary quinone electron acceptors of photosystem II S0..S4 redox states of the donor side of photosystem II TyrD side-path electron donor of photosystem II Tyrz secondary electron donor of photosystem II Chapter1 Introduction The membrane spanning protein complexes Photosystem I (PS-I) and Photosystem II (PS-II) in the photosynthetic membrane of green plants and cyanobacteria, use light as an energy source to drive a chain of redox reactions mediating electron transfer from water to NADP+. PS-I and PS-II function as follows; their light-harvesting components (the antenna) contain chlorophyll molecules that absorb incident light. After light absorption, the excitation energy is rapidly transferred between the antenna chlorophylls. After excitation of special chlorophylls in the reaction center, closely connected to the antenna, a primary radical pair is formed denoted P+I-, where P is the primary electron donor and I is the primary electron acceptor. The primary charge separation is followed by electron transfer steps that further separate the charges across the membrane. The components in PS-I and PS-II, essential for this electron transfer, are depicted in Figure 1.Electro n transfer events occurring in PS-II are reviewed in Refs. 1-4 and those occurring in PS-I are reviewed in Refs. 5 and 6. Detailed information on photosynthetic electron transport in green plants and cyanobacteria can be found in [7].Photosyntheti c systems also are found in purple bacteria, green sulphur bacteria and heliobacteria.Thes e arereviewe d in Refs. 8an d9 . Figure 1show s a schematic view on photosynthetic electron transport in green plants and cyanobacteria. The oxygen evolving complex (OEC) of PS-II catalyzes the oxidation of water, resulting in the formation of molecular oxygen as a by-product and the release of protons into an enclosed compartment, called the lumen. At the stromal side of the photosynthetic membrane, PS-II reduces bound plastoquinone (QB) to plastoquinol (PQH2) accompanied by proton uptake.PQH 2the n dissociates from its sitean d isreplace d bya n other plastoquinone (PQ) molecule from the PQ-pool. At the lumenal side of the membrane, PQH2 is re-oxidized by the Rieske-cytochrome b/f complex (reviewed in Ref. 10) accompanied by additional release of protons into the lumen. A water soluble copper protein, plastocyanin (PC), shuttles the electrons from cytochrome f to the photo-oxidized primary electron donor (P700) inPS-I . The electron on the photo-reduced primary electron acceptor chlorophyll (AQ) PS-II Rieske- PS-I ATP-ase cyt b/f IT NADP + H+ __-*NADPH A N ADP + Pi ATP + 2H FNR \ / * / X_Fd \ / Stroma / v 1 A/B PQ QA"*QB cyt bS63 A,|FX t M I \! Phe cyt b563 \ PQH p I \ FeS cytf t I ^PC4 Lumen OEC 2ir \ ir / 2H20 02 + 4H + Figure 1. Schematic representation of photosynthetic electron transport in green plants and cyanobacteria. OEC, oxygen evolving complex; P680. primary electron donor; Phe, pheophytin primary electron acceptor; QA) Oj, primary and secondary quinone electron acceptors; PQ, plastoquinone pool; PQH2, plastoquinol; FeS, Rieske-iron; cyt f, cytochrome f; PC, plastocyanin; P7OO, primary electron donor; Arj, chlophyll primary electron acceptor; Ai, phylloquinone; FA«, FX, iron sulphur clusters; Fd, ferredoxin; FNR, ferredoxin-NADP+-reductase.
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