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Excitation Energy Transfer by Coherent and Incoherent Mechanisms in the Peridinin–Chlorophyll a Protein Soumen Ghosh, Michael M. Bishop, Jerome D Roscioli, Amy M. LaFountain, Harry A. Frank, and Warren F. Beck J. Phys. Chem. Lett., Just Accepted Manuscript • DOI: 10.1021/acs.jpclett.6b02881 • Publication Date (Web): 02 Jan 2017 Downloaded from http://pubs.acs.org on January 3, 2017
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The Journal of Physical Chemistry Letters
Excitation Energy Transfer by Coherent and Incoherent Mechanisms in the Peridinin–Chlorophyll a Protein Soumen Ghosh,# Michael M. Bishop,#† Jerome D. Roscioli, Amy M. LaFountain,§ Harry A. Frank,§ and Warren F. Beck* Department of Chemistry, Michigan State University, East Lansing, Michigan 48824-1322 USA †Current address: The Dow Chemical Company, Midland, Michigan 48674 USA § Department of Chemistry, University of Connecticut, Storrs, Connecticut 06269-3036 USA
*Corresponding author. Email:
[email protected]. #These authors made equal contributions to the work.
Abstract. Excitation energy transfer from peridinin to chlorophyll (Chl) a is unusually efficient in the peridinin–chlorophyll a protein (PCP) from dinoflagellates. This enhanced performance is derived from the long intrinsic lifetime of 4.4 ps for the S2 (11Bu+) state of peridinin in PCP, which arises from the electron withdrawing properties of its carbonyl substituent. Results from heterodyne transient grating spectroscopy indicate that S2 serves as the donor for two channels of energy transfer: a 30 fs process involving quantum coherence and delocalized peridinin–Chl states, and an incoherent, 2.5 ps process initiated by dynamic exciton localization, which accompanies the formation of a conformationally distorted intermediate in 45 fs. The lifetime of the S2 state is lengthened in PCP by its intramolecular charge transfer (ICT) character, which increases the system–bath coupling and slows the torsional motions that promote nonradiative decay to the S1 (21Ag−) state.
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The Journal of Physical Chemistry Letters
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Of the known photosynthetic light-harvesting complexes that employ carotenoids as mid-visible antenna chromophores,1 the peridinin–chlorophyll a protein (PCP) from marine dinoflagellates is noted for its very high (~90%) quantum efficiency for excitation energy transfer from the carotenoid peridinin to Chl a.2-5 Each subunit of PCP binds a dense cluster of eight peridinins and two Chl a chromophores in a C2-symmetric, two-domain assembly (Figure 1a) inside a basket of α helices. The four peridinins in each domain are nearly in van der Waals contact (3.3 to 3.8 Å separation) with a central Chl a.6 The structure of PCP indicates an elegant interplay between the electronic effects of carbonyl substitution of the conjugated polyene of peridinin7 and of the strained conformations imposed on the peridinins by the binding sites in PCP.8 The states and mechanisms that mediate excitation energy transfer from peridinin to Chl a in PCP have been investigated in several laboratories using femtosecond spectroscopy.2-5,9 The scheme that emerges from this work involves two energy transfer channels. The S2 (11Bu+) state of peridinin is reported to have a very short lifetime, ~50 fs, which limits the yield of an ultrafast energy transfer process involving it as the donor state. The nature of this process remains in question because it has not yet been observed directly. The product of the nonradiative decay of the S2 state is usually identified as a vibrationally excited (or "hot") S1 (21Ag−) state species. During and after vibrational cooling in
