The Charge-Transfer Character of the S 0 f S 2 Transition in the Carotenoid Peridinin Is Revealed by Stark Spectroscopy Lavanya Premvardhan,* ,²,# Emmanouil Papagiannakis, ² Roger G. Hiller, ‡ and Rienk van Grondelle ² Department of Biophysics and Physics of Complex Systems, DiVision of Physics and Astronomy, Faculty of Sciences, Vrije UniVersiteit, De Boelelaan 1081, 1081 HV Amsterdam, The Netherlands, and Macquarie UniVersity, New South Wales 2109, Australia ReceiVed: April 19, 2005; In Final Form: June 3, 2005 Peridinin, the carotenoid in the peridinin chlorophyll a protein (PCP), was studied by Stark (electroabsorption) spectroscopy to determine the change in electrostatic properties produced on excitation within the absorption band, in methyl tetrahydrofuran (MeTHF) versus ethylene glycol (EG), at 77 K. Strikingly, a large change in the permanent dipole moment (|Δµ b|) was found between the ground state, S 0 (1 1 A g * - ), and the Franck- Condon region of the S 2 (1 1 B u * + ) excited state, in both MeTHF (22 D) and EG (∼27 D), thus revealing the previously unknown charge transfer (CT) character of this π-π* transition in peridinin. Such a large |Δµ b| produced on excitation, we suggest, facilitates the bending of the lactone moiety, toward which charge transfer occurs, and the subsequent formation of the previously identified intramolecular CT (ICT) state at lower energy. This unexpectedly large S 2 dipole moment, which has not been predicted even from high-level electronic structure calculations, is supported by calculating the shift of the peridinin absorption band as a function of solvent polarity, using the experimentally derived result. Overall, the photoinduced charge transfer uncovered here is expected to affect the excited-state reactivity of peridinin and, within the protein, be important for efficient energy transfer from the carotenoid S 2 and S 1 /ICT states to the chlorophylls in PCP. Introduction The functional importance of carotenoids in photosynthesis is underscored by their ubiquitous presence as light harvestors and as photoprotectors that deactivate singlet oxygen and quench harmful triplets and radicals in plants. 1-3 A characterization of these systems is relevant to understand their effectiveness in photosynthesis and, furthermore, to design artificial systems 4,5 that mimic the useful properties that carotenoids exhibit in nature. Of the many carotenoids, peridinin (Scheme 1) is one of the most abundant and is found within the water-soluble peripheral peridinin chlorophyll a protein (PCP) and the membrane-associated intrinsic light-harvesting complex (LHC) of dinoflagellates. 6 Its primary role in energy transfer to chlorophyll a (Chl-a) in PCP 7-9 has led to extensive studies of its photophysics in the context of its biological function at the molecular level. Nevertheless, there remain unanswered ques- tions about its electronic properties, particularly in the excited state. To this end, the Stark-effect study and solvent-shift analysis presented here provide new information about the electronic properties of the initially excited state, which comple- ments the existing understanding of the rather peculiar photo- physics of peridinin. 3,8,10-20 The photophysical properties of carotenoids and retinals, decided by the nature of their potential energy surfaces (PES), are described in similar terms to (all-trans) linear polyenes of the C 2h point group because of the π-conjugated backbone they have in common. 21 The strongly allowed transition of caro- tenoids in the vis-near-UV wavelength region is characterized as a 1 1 A g * - f 1 1 B u * + (S 0 f S n , most often n ) 2) transition. 1 Absorption to S 1 (2 1 A g * - ), the lowest singlet excited state, is symmetry forbidden from the ground state and is thus not directly accessible by one-photon processes. 21 Although the PES of peridinin is described in a similar manner, it exhibits photophysical properties distinct from most other carotenoids. This has been attributed to the presence of a state, possibly S 1 itself, possessing charge-transfer (CT) character. 10,14,16,19,22 However, the identity and energetic location of this CT state, hereafter called the ICT state, continue to be strongly debated. Calculations find either a charge-transfer state distinct from S 1 14 or that S 1 itself possesses CT character. 16 Analysis of experi- mental studies also interpret the ICT state to be either strongly coupled to S 1 15,17 or distinct from S 1 . 10,19 Of note is a recent multipulse transient absorption (pump-dump-probe) experi- * To whom correspondence should be addressed. E-mail: lp2f@nat.vu.nl. ² Vrije Universiteit. # Current Address: DBJC/SBFM, CEA-Saclay, Ba ˆt 528, 91191 Gif/ Yvette, Cedex, France. ‡ Macquarie University. SCHEME 1: Molecular Structure of Peridinin a a The molecular structure of peridinin is shown with the different moieties encircled. The distances between the central points of these moieties are ∼5 Å between a and b and ∼10 Å between b and c. Also marked in the structure, in bold-dashed lines, are the nodes in the S 2 wave function 16 in the lactone ring (see text). 15589 J. Phys. Chem. B 2005, 109, 15589-15597 10.1021/jp052027g CCC: $30.25 © 2005 American Chemical Society Published on Web 07/22/2005