Photo-CIDNP MAS NMR Studies on Photosynthetic Reaction Centers
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1 Photo-CIDNP MAS NMR Studies on Photosynthetic Reaction Centers Anna Diller
2 ISBN
3 Photo-CIDNP MAS NMR Studies on Photosynthetic Reaction Centers PROEFSCHRIFT ter verkrijging van de graad van Doctor aan de Universiteit Leiden, op gezag van de Rector Magnificus Prof. mr. P. F. van der Heijden, volgens besluit van het College voor Promoties te verdedigen op dinsdag 18 september 2007 klokke uur door Anna Diller geboren te Lichtenfels, Duitsland in 1977
4 Promotiecommissie Promotor: Copromotor: Referent: Overige Leden: Prof. dr. H. J. M. de Groot Dr. J. Matysik Prof. dr. W. Lubitz, Max-Planck-Institut für Bioanorganische Chemie, Mülheim/Ruhr Prof. dr. J. Brouwer Prof. dr. W. J. de Grip Dr. P. Gast Gefördert von der Volkswagen-Stiftung (Förderinitiative Intra- und intermolekulare Elektronenübertragung, I/78010)
5 When you think outside the box, the box goes away. Richard R. Reisman Für meine Eltern
6 List of abbreviations 1D 2D a e ALA ATP ATPase BChl BPhe, φ CIDNP Chl CP CSA DD DFT DNP DR EDTA ENDOR EPR ESEEM FWHH hf hfi His HOMO LDAO LH LUMO MAS MAOSS n.a. One-dimensional Two-dimensional absorptive emissive δ-aminolevulinic acid Adenosine triphosphate Adenosine triphosphate synthase Bacteriochlorophyll Bacteriopheophytin Chemically induced dynamic nuclear polarization Chlorophyll Cross polarization Chemical shift anisotropy Differential decay Density functional theory Dynamic nuclear polarization Differential relaxation Ethylene diamino tetra acetate Electron nuclear double resonance Electron paramagnetic resonance Electron spin echo envelope modulation Full width at half height hyperfine hyperfine interaction Histidine Highest Occupied Molecular Orbital Lauryldimethylamine N -oxide N,N-dimethyldodecylamine-N-oxide Light harvesting Lowest Occupied Molecular Orbital Magic-angle spinning Magic-angle oriented sample spinning natural abundance
7 List of abbreviations NADP + NADPH NMR n.s. OD ODV P Phe Photo-CIDNP ppm PS I PS II PSU Q Rb. RC rf Rps. S/N SLF ppm TPPM TSM w/v WT Nicotinamide adenine dinucleotide phosphate (oxidized form) Nicotinamide adenine dinucleotide phosphate (reduced form) Nuclear magnetic resonance number of scans Optical density Optical density per volume Electron donor Pheophytin Photochemically induced dynamic nuclear polarization parts per million Photosystem I Photosystem II Photosynthetic unit Ubiquinone Rhodobacter Reaction center radio frequency Rhodopseudomonas signal-to-noise Separated Local Field parts per million Two pulse-phase modulation Electron-electron-nuclear three spin mixing weight per volume Wildtype
8
9 Contents 1 Introduction Photosynthesis Photosystems Bacterial reaction centers Photosystem I Photosystem II Electron transfer in photosystem II Redox potential of photosystem II Photo-CIDNP MAS NMR The Photo-CIDNP effect Photo-CIDNP mechanisms in solids Aim and scope of the thesis Signals in solid-state photochemically induced dynamic nuclear polarization recover faster than with the longitudinal relaxation time Introduction Experimental section Theory Source and drain terms in photo-cidnp buildup kinetics NMR signal recovery as a function of repetition time Estimate of loss factors Results Recovery experiments on photosynthetic reaction centers Analysis of the recovery kinetics Discussion T 1 relaxation of aromatic carbons Comparison with earlier studies on photo-cidnp build-up Mechanism of fast recovery... 47
10 2.5.4 Maximum polarization and signal-to-noise enhancement Conclusions Photo-CIDNP solid-state NMR on Photosystems I and II: what makes P680 special? Introduction Materials and methods Results Discussion The photo-cidnp effect The ground-state electronic structure The electronic structure of the radical pair N-photo-CIDNP MAS NMR analysis of the electron donor of photosystem II Introduction Material and Methods Sample preparation MAS NMR measurements Results and Discussion N photo-cidnp MAS NMR on PS I N photo-cidnp MAS NMR on PS II Matrix involvement The hinge model of the donor of PS II C photo-cidnp MAS NMR on chromatophores and cells of Rhodobacter sphaeroides allows for spectral editing Introduction Materials and Methods Culturing of Rhodobacter sphaeroides Incorporation of isotope labels Preparation of cells, chromatophores and RCs MAS NMR measurements Results and Discussion... 96
11 C photo-cidnp MAS NMR experiments on purified RCs C photo-cidnp MAS NMR experiments on chromatophores The possibility of centrifugal orientation of chromatophores The possibility of magnetic field-orientation of chromatophores C photo-cidnp MAS NMR experiments on entire cells Possible origin of sign-change of the donor signals Conclusions Current view and Outlook The donor of photosystem II Photo-CIDNP as a tool for functional screening of RCs and spectral editing Orientational effects in Photo-CIDNP MAS NMR Summary 125 Samenvatting 129 Zusammenfassung 133 Publications 137 Curriculum vitae 139 Nawoord 140
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