Light Harvesting and Photoprotective Functions of Carotenoids in Compact Artificial Photosynthetic Antenna Designs Gerdenis Kodis,* ,²,‡ Christian Herrero, ² Rodrigo Palacios, ² Ernesto Marin ˜ o-Ochoa, ² Stephanie Gould, ² Linda de la Garza, ² Rienk van Grondelle, § Devens Gust, ² Thomas A. Moore, ² Ana L. Moore, ² and John T. M. Kennis* ,§ Department of Chemistry and Biochemistry and the Center for the Study of Early EVents in Photosynthesis, Arizona State UniVersity, Tempe, Arizona, Department of Biophysics, DiVision of Physics and Astronomy, Faculty of Sciences, Vrije UniVersiteit, 1081 HV Amsterdam, The Netherlands, and Institute of Physics, SaVanoriu 231, LT-2053 Vilnius, Lithuania ReceiVed: July 22, 2003; In Final Form: October 10, 2003 Artificial light-harvesting constructs were synthesized by covalently linking two carotenoids to the central silicon atom of a phthalocyanine (Pc) derivative. Triad 1 binds two carotenoids having nine conjugated double bonds, whereas triad 2 binds two carotenoids having 10 carbon-carbon double bonds in conjugation. Fluorescence excitation experiments indicated that, in triad 1 dissolved in n-hexane, the carotenoid to Pc singlet energy transfer efficiency is ca. 92%, whereas in triad 2, it is 30%. Results from ultrafast laser spectroscopy indicate that upon population of the optically allowed S 2 state of the carotenoid the optically forbidden states S 1 and S* are rapidly generated in both triad 1 and triad 2. In triad 1,S 2 ,S 1 , and S* all contribute singlet electronic energy to Pc. In triad 2, singlet electronic energy transfer to Pc occurs primarily from the optically allowed S 2 state with little energy transfer to Pc via the S 1 state, and there is no evidence for energy transfer via S*. Instead, in triad 2, we find a multiphased quenching of the Pc singlet excited state on the picosecond and nanosecond time scales. Upon intersystem crossing from the singlet excited state of Pc to the triplet state in triad 1, triplet-triplet energy transfer to either of the carotenoids takes place on a time scale significantly shorter than 5 ns. When dissolved in polar solvents, triads 1 and 2 exhibit light- induced electron transfer from either of the carotenoid moieties to the excited singlet Pc species with a time constant of about 2 ps. Charge recombination to the singlet ground state occurs in 10 ps in triad 1 and 17 ps in triad 2. 1. Introduction Carotenoids are indispensable in photosynthetic energy conversion, where they function as light harvesters and photoprotectors. 1-3 They exert their light harvesting (LH) function by absorbing sunlight in the blue and green parts of the solar spectrum and transferring the energy to nearby (bacterio)chlorophyll (B)(Chl) molecules. In subsequent steps, the excitation energy is transported to the reaction center, where photochemical conversion takes place. 4 The energy of the photons made available this way accounts for a significant fraction of photosynthetic biomass production on earth. In addition to their light-harvesting function, carotenoids assume a number of photoprotective roles. Essentially all antenna and reaction center complexes bind carotenoids to protect the organism from oxidative damage, primarily by quenching harmful (B)Chl triplet and singlet oxygen species. Recently, it has been discovered that carotenoids can act as electron donors to reduce long-lived P680 + , and in such a way prevent damage to reactions centers of oxygenic photosynthetic organisms. 5,6 Moreover, carotenoids appear to play a large and thus far poorly understood role in the direct quenching of Chl singlet states in the xanthophyll cycle in Photosystem II of plants. 7 To perform this variety of functions, carotenoids are incorporated in photosynthetic pigment-protein complexes in close contact with (B)Chl. 8-11 The main feature in the molecular structure of carotenoids is a polyene chain of alternating carbon-carbon single and double bonds. Until recently, the electronic states involved in the LH function have been described by one high-lying optically allowed singlet excited state (S 2 ) and a low-lying, optically forbidden singlet excited state (S 1 ). Upon light absorption, the S 2 state relaxes to the optically forbidden S 1 state in 100-200 fs by internal conversion (IC), after which the S 1 state internally converts to the ground state on the picosecond time scale. 1,2 Recent work has shown that excited-state energy transfer (EET) from both the S 2 and S 1 states is required for efficient LH function. 12-15 The carotenoid to (B)Chl EET processes are thought to be governed by the Coulombic coupling and the spectral overlap between donor and acceptor states, 1,16,17 and the overall efficiency can vary from as low as 35%, for instance in the LH1 complex of Rhodospirillum (Rs.) rubrum 18 and the PSII core complex of oxygenic photosynthesis 19 to as much as 80% or more in the LHCII of plants, 14,20 the PSI complex of cyanobacteria 21,22 and various LH2 antennas of purple bacte- ria. 1,13,15,23 In recent years, it has become increasingly clear that the traditional description of the excited-state manifold of caro- * To whom correspondence should be addressed. E-mail: gerdenis@ asu.edu (G.K.); john@nat.vu.nl (J.T.M.K.). ² Arizona State University. ‡ Institute of Physics. § Vrije Universiteit. 414 J. Phys. Chem. B 2004, 108, 414-425 10.1021/jp036139o CCC: $27.50 © 2004 American Chemical Society Published on Web 12/10/2003