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Femtobiophotonics for the Investigation of Molecular Picobiophotonics for the investigation of pigment-pigment and pigment-protein interactions in photosynthetic complexes vorgelegt von Diplom-Physiker Franz-Josef Schmitt geboren in Marburg/ Lahn von der Fakultät II - Mathematik und Naturwissenschaften der Technischen Universität Berlin zur Erlangung des akademischen Grades Doktor der Naturwissenschaften Promotionsausschuss: Vorsitzender: Prof. Dr. Mario Dähne Berichter/Gutachter: Prof. Dr. Hans Joachim Eichler Berichter/Gutachter: Prof. Dr. Gernot Renger Berichter/Gutachter: Prof. Dr. Thomas Renger Tag der wissenschaftlichen Aussprache: 15.08.2011 Berlin 2011 D 83 page | 1 page | 2 ABSTRACT Franz-Josef Schmitt Picobiophotonics for the investigation of pigment-pigment and pigment-protein interactions in photosynthetic complexes Excitation energy transfer (EET) processes in different photosynthetic pigment-protein-complexes were analysed by time- and wavelength correlated single photon counting (TWCSPC). A new mobile 16-channel photomultiplier with flexible fiber optics, exchangeable light sources and temperature regulator (10 K – 350 K) was built up for the spectroscopy of samples in cuvettes, on surfaces or of whole leaves in vivo. The system represents a mobile setup of the powerful TCSPC technique with high optical throughput up to 106 counts/sec. The theoretical description of the excited state dynamics in systems with pigment-pigment and pigment-protein interaction was performed by using rate equations that were applied on structures with increasing hierarchical complexity. The study started with a system consisting of two excitonically coupled Chl molecules in a tetrameric protein environment represented by the recombinant water soluble Chl binding protein (WSCP) of type IIa and it was completed with a study of the photosystem II (PSII) dynamics in whole leaves of the higher plant Arabidopsis thaliana. In this way a quantification of dissipative excited state relaxation processes as a function of increasing excitation light intensity was achieved. For parameter adaption in the corresponding systems of linear differential equations a highly efficient algorithm was developed that allows the variation of parameters used to fit the time resolved optical data under any constraints on the coefficient matrix (e.g. invariance of the symmetry). The approach permits the determination of selected parameter values, their probability and stability in any dynamical system. A way to calculate thermodynamic quantities (e.g. entropy) under nonequilibrium conditions from rate equations is proposed. The excited state dynamics observed in WSCP were explained by assuming an excitonically coupled Chl dimer that is modulated by the protein environment on different time scales. The dominating fluorescence decay component increases from 4.8 ns or 5.2 ns for Chl b or Chl a homodimers, respectively, at room temperature, to 7.0 or 6.2 ns, respectively, at 10 K. This temperature dependency is most probably caused by the pigment-pigment- interaction and the energies of the triplet states of the Chl molecules. A modulation of the electronic states of the coupled Chl dimer by the protein environment with a typical time constant of 100 ps at 10 K is inferred to be responsible for a fast and strongly temperature dependent fluorescence component. This idea is qualitatively in line with refined theoretical models and results of complementary studies of hole burning and fluorescence line narrowing spectroscopy. In the phycobiliprotein (PBP) antenna of the cyanobacterium Acaryochloris marina EET occurs with characteristic time constants of 400 fs, 3-5 ps and 14 ps inside trimeric phycocyanin (PC), from PC to allophycocyanin (APC) and from APC to the terminal emitter (TE) of the PBP antenna, respectively. The TWCSPC spectra of whole cells and preparations of isolated PBP complexes exhibit a 20 ps component each that indicates the intact EET from PC to the TE in agreement with the results of transient fs absorption spectroscopy. The EET from the PBP antenna to the Chl d containing core antenna complexes of PS II represents an additional limiting transfer step of about 30-40 ps which leads to a time constant of the EET from PBP to Chl d in the range of 70 ps. Coupled and temperature switch-able hybrid systems of surface treated CdSe/ZnS quantum dots (QDs) with 530 nm emission wavelength and the isolated PBP antenna complexes from A.marina were formed in aqueous solution by electrostatic self assembly. Based on the theory of Förster Resonance Energy Transfer (FRET) an average value of 3.2-3.5 nm was obtained for the distance between the neighbouring transition dipole moments in the QDs and the PBP antenna. It was shown that the functional coupling between QDs and PBP complexes is interrupted at temperatures below 0°C. This effect enables the construction of switch-able molecular sensors, photosensibilisators or light harvesting devices with various applications in biochemistry, biomedicine and photovoltaics. page | 3 KURZZUSAMMENFASSUNG Franz-Josef Schmitt Pikobiophotonik zur Untersuchung der Pigment-Pigment und Pigment-Protein Wechselwirkungen in photosynthetischen Komplexen Anregungsenergietransfer-(EET)-prozesse wurden in verschiedenen photosynthetischen Pigment- Protein-Komplexen mit zeit- und wellenlängenkorrelierter Einzelphotonenspektroskopie (TWCSPC) analysiert. Ein neuer mobiler 16-Kanal Photomultiplier mit flexibler Faseroptik, austauschbaren Lichtquellen und einem Kryostaten (10 K – 350 K) wurde für die Spektroskopie von Proben in Küvetten, auf Oberflächen oder von ganzen Blättern in vivo aufgebaut. Das System stellt einen mobilen Messplatz auf Grundlage der leistungsfähigen TCSPC Technik mit hohem Lichtdurchsatz bis zu 106 Photonen/ Sekunde dar. Die theoretische Beschreibung der Anregungszustandsdynamik unter Berücksichtigung von Pigment- Pigment und Pigment-Protein Wechselwirkung erfolgte über Ratengleichungen, die auf Systeme mit hierarchisch steigender Komplexität angewendet wurden. Die Untersuchung startete an einer Anordnung von zwei exzitonisch gekoppelten Chl Molekülen in einer tetrameren Proteinumgebung wie sie in rekombinantem wasserlöslichen Chlorophyll bindenden Protein (WSCP) des Typs IIa vorliegt und wurde mit einer Untersuchung der Photosystem II (PSII) Dynamik in ganzen Blättern der höheren Pflanze Arabidopsis thaliana abgeschlossen. Auf diese Weise wurde z.B. die Quantifizierung dissipativer Relaxationsprozesse der Anregungszustände bei ansteigender Intensität des Anregungslichtes ermöglicht. Für die Parameteranpassung in den entsprechenden Systemen linearer Differentialgleichungen wurde ein effizienter Algorithmus entwickelt, der die Variation von Parametern zur Anpassung der zeitaufgelösten optischen Daten unter beliebigen Randbedingungen an die Koeffizientenmatrix (z.B. Invarianz der Symmetrie) ermöglicht. Der Zugang erlaubt die Bestimmung ausgewählter Parameterwerte, ihre Wahrscheinlichkeit und Stabilität in einem beliebigen dynamischen System. Ein Weg zur Berechnung thermodynamischer Größen (z.B. Entropie) aus Ratengleichungen unter Nichtgleichgewichtsbedingungen wird vorgeschlagen. Die Anregungszustandsdynamik in WSCP wurde durch die Annahme eines gekoppelten Chl Dimers, das durch die Proteinumgebung auf verschiedenen Zeitskalen moduliert wird, erklärt. Die dominierende Komponente der Fluoreszenzkinetik steigt von 4,8 bzw. 5,2 ns für Chl b bzw. Chl a Homodimere bei Raumtemperatur auf 7,0 bzw. 6,2 ns bei 10 K an. Diese Temperaturabhängigkeit wird höchstwahrscheinlich durch die Pigment-Pigment Wechselwirkung und die energetische Lage der Triplettzustände der Chl Moleküle bestimmt. Eine Modulation der elektronischen Zustände durch die Proteinumgebung mit einer typischen Zeitkonstante von 100 ps bei 10 K ist sehr wahrscheinlich für eine schnelle und stark temperaturabhängige Fluoreszenzkomponente verantwortlich, die qualitativ mit weiterentwickelten theoretischen Modellen und Ergebnissen komplementärer Studien mittels Lochbrenn- und Fluoreszenz line narrowing Spektroskopie übereinstimmt. In der Phycobiliprotein (PBP) Antenne des Cyanobakteriums Acaryochloris marina findet der EET mit charakteristischen Zeitkonstanten von 400 fs, 3-5 ps bzw. 14 ps innerhalb des trimeren Phycocyanins (PC), vom PC zum Allophycocyanin (APC) bzw. vom APC zum terminalen Emitter (TE) der PBP Antenne statt. Die TWCSPC Spektren ganzer Zellen und Präparationen von isolierten PBP Komplexen zeigen jeweils eine 20 ps Komponente, die dem Anregungsenergietransfer vom PC zum TE entspricht, in Übereinstimmung mit Ergebnissen aus transienten fs absorptionsspektros- kopischen Untersuchungen. Der EET von der PBP Antenne zu den Chl d haltigen Komplexen der Core Antenne von PS II weist einen zusätzlichen limitierenden Transferschritt von 30-40 ps auf, der zu einer Zeitkonstante für den gesamten EET vom PBP zum Chl d in der Größenordnung von 70 ps führt. Gekoppelte und temperaturschaltbare Hybridsysteme aus oberflächenbehandelten CdSe/ZnS Quantenpunkte (QDs) mit 530 nm Emissionswellenlänge und isolierten PBP Komplexen aus A.marina wurden in wässriger Lösung durch elektrostatische Selbstorganisation gebildet. Nach der Theorie des Förster Resonanz Energietransfers (FRET) wurde der Abstand der benachbarten Übergangsdipolmomente in den QDs und der PBP Antenne zu 3,2-3,5 nm berechnet. Es wurde gezeigt, dass die funktionelle Kopplung von QDs und PBP Komplexen bei Temperaturen unterhalb von 0°C unterbrochen wird. Dies ermöglicht die Konstruktion von schaltbaren molekularer Sonden, Photosensibilisatoren oder Lichtsammelsystemen
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