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      Quantum Coherence in Photosynthesis for Efficient Solar Energy Conversion

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          Abstract

          The crucial step in the conversion of solar to chemical energy in Photosynthesis takes place in the reaction center where the absorbed excitation energy is converted into a stable charge separated state by ultrafast electron transfer events. However, the fundamental mechanism responsible for the near unity quantum efficiency of this process is unknown. Here we elucidate the role of coherence in determining the efficiency of charge separation in the plant photosystem II reaction centre (PSII RC) by comprehensively combining experiment (two-dimensional electronic spectroscopy) and theory (Redfield theory). We reveal the presence of electronic coherence between excitons as well as between exciton and charge transfer states which we argue to be maintained by vibrational modes. Furthermore, we present evidence for the strong correlation between the degree of electronic coherence and efficient and ultrafast charge separation. We propose that this coherent mechanism will inspire the development of new energy technologies.

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          Most cited references38

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          Lessons from nature about solar light harvesting.

          Solar fuel production often starts with the energy from light being absorbed by an assembly of molecules; this electronic excitation is subsequently transferred to a suitable acceptor. For example, in photosynthesis, antenna complexes capture sunlight and direct the energy to reaction centres that then carry out the associated chemistry. In this Review, we describe the principles learned from studies of various natural antenna complexes and suggest how to elucidate strategies for designing light-harvesting systems. We envisage that such systems will be used for solar fuel production, to direct and regulate excitation energy flow using molecular organizations that facilitate feedback and control, or to transfer excitons over long distances. Also described are the notable properties of light-harvesting chromophores, spatial-energetic landscapes, the roles of excitonic states and quantum coherence, as well as how antennas are regulated and photoprotected.
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            Theoretical examination of quantum coherence in a photosynthetic system at physiological temperature.

            The observation of long-lived electronic coherence in a photosynthetic pigment-protein complex, the Fenna-Matthews-Olson (FMO) complex, is suggestive that quantum coherence might play a significant role in achieving the remarkable efficiency of photosynthetic electronic energy transfer (EET), although the data were acquired at cryogenic temperature [Engel GS, et al. (2007) Evidence for wavelike energy transfer through quantum coherence in photosynthetic systems. Nature 446:782-786]. In this paper, the spatial and temporal dynamics of EET through the FMO complex at physiological temperature are investigated theoretically. The numerical results reveal that quantum wave-like motion persists for several hundred femtoseconds even at physiological temperature, and suggest that the FMO complex may work as a rectifier for unidirectional energy flow from the peripheral light-harvesting antenna to the reaction center complex by taking advantage of quantum coherence and the energy landscape of pigments tuned by the protein scaffold. A potential role of quantum coherence is to overcome local energetic traps and aid efficient trapping of electronic energy by the pigments facing the reaction center complex.
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              Dynamics of light harvesting in photosynthesis.

              We review recent theoretical and experimental advances in the elucidation of the dynamics of light harvesting in photosynthesis, focusing on recent theoretical developments in structure-based modeling of electronic excitations in photosynthetic complexes and critically examining theoretical models for excitation energy transfer. We then briefly describe two-dimensional electronic spectroscopy and its application to the study of photosynthetic complexes, in particular the Fenna-Matthews-Olson complex from green sulfur bacteria. This review emphasizes recent experimental observations of long-lasting quantum coherence in photosynthetic systems and the implications of quantum coherence in natural photosynthesis.
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                Author and article information

                Journal
                101235387
                34285
                Nat Phys
                Nat Phys
                Nature physics
                1745-2473
                7 July 2014
                1 September 2014
                09 February 2016
                : 10
                : 9
                : 676-682
                Affiliations
                [1 ]Department of Physics and Astronomy, VU University, Amsterdam, The Netherlands
                [2 ]Department of Chemical Physics, Lund University, Lund, Sweden
                [3 ]A. N. Belozersky Institute of Physico-Chemical Biology, Moscow State University, Moscow, Russia
                Author notes
                [* ]Contact information: Dr. Elisabet Romero, eli@ 123456few.vu.nl , Phone +31 20 5987426, Fax +31 20 5987999
                [†]

                Current address: Center for Physical Sciences and Technology, Vilnius, Lithuania

                [‡]

                Current address: TU Delft, Applied Sciences ChemE/Chemical Engineering, Delft, The Netherlands

                Author Contributions: E.R., R.A., M.F., J.T., and D.Z. collected the experimental 2DES data. R.A., and M.F. developed the data analysis programs. E.R. analyzed the experimental data. V.I.N., E.R., and R.v.G. developed the theoretical modeling. E.R. D.Z., and R.v.G. designed the research. E.R., V.I.N., D.Z., and R.v.G. wrote the paper. All authors discussed the results and commented on the manuscript.

                Article
                EMS59054
                10.1038/nphys3017
                4746732
                26870153
                c5582b3e-58ea-4522-893b-2dea8199e992

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