Article pubs.acs.org/JPCB
Femtosecond Heterodyne Transient Grating Studies of Nonradiative Deactivation of the S2 (11Bu+) State of Peridinin: Detection and Spectroscopic Assignment of an Intermediate in the Decay Pathway 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 United States Department of Chemistry, University of Connecticut, Storrs, Connecticut 06269-3036 United States
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S Supporting Information *
ABSTRACT: Femtosecond heterodyne transient grating spectroscopy was employed to investigate the nonradiative decay pathway from the S2 (11Bu+) state to the S1 (21Ag−) state of peridinin in methanol solution. Just as previously observed by this laboratory for β-carotene in benzonitrile, the real (absorption) and imaginary (dispersion) components of the transient grating signal obtained with Fourier transform spectral interferometry from peridinin exhibit ultrafast responses indicating that S2 state decays in 12 fs to produce an intermediate state, Sx. The excited state absorption spectrum from the Sx state of peridinin, however, is found to be markedly blue-shifted from that of β-carotene because it makes a substantial contribution to the signal observed with 40 fs, 520 nm pulses. The results of a global target analysis and numerical simulations using nonlinear response functions and the multimode Brownian oscillator model support the assignment of Sx to a displaced conformation of the S2 state rather than to a vibrationally excited (or hot) S1 state. The Sx state in peridinin is assigned to a structure with a distorted conjugated polyene backbone moving past an activationenergy barrier between planar and twisted structures on the S2 potential surface. The lengthened lifetime of the Sx state of peridinin in methanol, 900 ± 100 fs, much longer than that typically observed for carotenoids lacking carbonyl substituents, ∼150 fs, can be attributed to the slowing of torsional motions by solvent friction. In peridinin, the system−bath coupling is significantly enhanced over that in β-carotene solution most likely due to the intrinsic intramolecular charge transfer character it derives from the electron withdrawing nature of the carbonyl substituent. An important additional implication is that the Sx state, and the distorted structures reached subsequently along the torsional gradient on the S2 potential surface, may serve as the principal excitation energy transfer donors to chlorophyll a in the peridinin−chlorophyll a protein from dinoflagellates.
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INTRODUCTION Carotenoids perform several essential functions in photosynthetic organisms,1,2 including photoprotection3 and light harvesting in the blue-green (450−550 nm) part of the solar spectrum where (bacterio)chlorophyll ((B)Chl) absorbs inefficiently.3,4 The mechanisms that allow efficient excitation energy transfer between carotenoids and (B)Chl in lightharvesting proteins have yet to be fully elucidated owing to the complexity of the nonradiative decay pathways and the production of dark intermediate states5 following optical excitation of carotenoids in solution and in proteins. This contribution deals with the earliest dynamics that follow optical preparation of the S2 (11Bu+) state of peridinin, the principal light-harvesting chromophore in the peridinin− chlorophyll a protein (PCP).6−8 This work is motivated by our recent proposal9 that the S2 state in carotenoids naturally obtains an intramolecular charge-transfer (ICT) character by undergoing activated torsional motions of the conjugated polyene backbone. In recent work on β-carotene,10 we suggested that structures near an activation energy barrier on © 2016 American Chemical Society
the S2 potential surface dividing planar and twisted structures account for the formation in
