J. Phys. Chem. C 2007, 111, 467-476
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Polarity-Tuned Energy Transfer Efficiency in Artificial Light-Harvesting Antennae Containing Carbonyl Carotenoids Peridinin and Fucoxanthin Toma´ sˇ Polı´vka,*,†,‡ Mathias Pellnor,§ Eurico Melo,| Torbjo1 rn Pascher,§ Villy Sundstro1 m,§ Atsuhiro Osuka,⊥ and K. Razi Naqvi# Institute of Physical Biology, UniVersity of South Bohemia, Czech Republic, Biological Center, Czech Academy of Sciences, Czech Republic, Chemical Physics, Lund UniVersity, Sweden, Institute of Chemical Technology and Biology, Oeiras, Portugal, Department of Chemistry, Graduate School of Science, Kyoto UniVersity, Japan, and Department of Physics, Norwegian UniVersity of Science and Technology, Trondheim, Norway ReceiVed: September 21, 2006; In Final Form: October 30, 2006
This study focuses on the mechanisms and pathways of energy transfer in two carotenoid-pyropheophorbide dyads serving as an artificial light-harvesting antenna. The dyads contain carbonyl carotenoids peridinin (dyad 1) and fucoxanthin (dyad 2). Studies of these carotenoids in solution showed a pronounced dependence of the excited-state lifetime on solvent polarity. This dependence was attributed to the presence of a state with intramolecular charge transfer (ICT) character in the excited-state manifold. Here we measured carotenoidpyropheophorbide energy transfer in solvents with different polarity. Energy transfer occurs on a time scale of 31-44 ps for dyad 1, but it is nearly an order of magnitude slower for dyad 2 (195-280 ps). Energy transfer efficiency varies with solvent polarity, reaching 80% in benzene, 69% in tetrahydrofuran, and 22% in acetonitrile for dyad 1 and 27% in benzene, 19% in tetrahydrofuran, and 13% in acetonitrile for dyad 2. The factors controlling this polarity dependence are (1) the competition of energy transfer rate with the S1/ICT lifetime, which, for carbonyl carotenoids, is significantly shorter in polar solvents, (2) the mutual orientation of the carotenoid and pyropheophorbide moieties, and (3) enhancement of the S1/ICT dipole moment by increasing the ICT character of the S1/ICT state in polar solvents. The possibility of tuning energy transfer through solvent polarity in combination with another spectroscopic feature of carbonyl carotenoids, efficient absorption of light in the spectral region close to the maximum of the solar irradiance curve (450-550 nm), makes these dyads attractive for potential application as artificial antenna.
1. Introduction The demand for clean and renewable energy sources has initiated many attempts at mimicking natural photosynthesis, a process that employs water and sunlight as primary energy sources.1 As in natural photosynthesis, the prospective artificial photosynthetic system should ideally contain two major functional parts: a reaction center, driving water splitting and charge separation, and a light-harvesting antenna, efficiently absorbing sunlight and transferring the energy to the reaction center. Efforts in recent years have made much progress in designing models of artificial reaction centers,1-4 antennas,5-8 and even coupled reaction center-antenna mimics,9-11 but no artificial photosynthetic system capable of fully mimicking its natural counterpart has been constructed so far. To economize synthetic efforts, it would be useful to utilize the same molecule for performing a dual role, acting both as an antenna and as the reaction center. This task has been achieved, for example, with ruthenium tris bipyridine based mimics, which have been shown to carry on both functions,12-14 or with carotenoid-based artificial systems, which have been shown to carry out, in addition to mimicking reaction center15,16 and antenna,17,18 the third crucial function * Corresponding author. E-mail:
[email protected]. † University of South Bohemia. ‡ Czech Academy of Sciences. § Lund University. | Institute of Chemical Technology and Biology. ⊥ Kyoto University. # Norwegian University of Science and Technology.
of natural photosynthesis, namely photoprotection.19-22 Therefore, carotenoids, which are fundamental components of photosynthetic apparatus of all photosynthetic organisms,23,24 hold promise to become key constituents of future artificial photosynthetic systems. As demonstrated in the past two decades, the most successful carotenoid-based mimics are dyads,17-19,.25 triads,15,16,26,27 and even pentads28 containing covalently linked carotenoid and porphyrin, phthalocyanine, or pyropheophorbide. For antenna function, which is the focus of this work, dyads have occupied the center stage and have been shown to achieve a wide range of efficiencies, approaching in some cases 100%.23 The reason for the large variability in energy transfer efficiency, which is also mirrored in natural photosynthetic systems, lies in specific spectroscopic properties of carotenoids. Carotenoids contain a conjugated carbon-carbon double bond chain with diverse end groups and substituents. Since their carbon backbone possesses C2h symmetry, the strong absorption in the spectral region of 420-550 nm results from a transition between the ground state S0 (1Ag- in the idealized C2h group) and the upper excited S2 (1Bu+) state. An optical transition between the S0 and S1 (2Ag-) states is forbidden by the symmetry selection rules.23 Whereas the S2 state undergoes fast internal conversion to the S1 state within a few hundred femtoseconds, the lifetime of the S1 state ranges from 1 to 200 ps depending on the number of conjugated carbon-carbon double bonds present in the molecule.23 Despite its rather short excited-state lifetime, a carotenoid can act as an energy donor in many natural systems, given appropriate
10.1021/jp066187j CCC: $37.00 © 2007 American Chemical Society Published on Web 12/07/2006
468 J. Phys. Chem. C, Vol. 111, No. 1, 2007 orientation and proximity to an acceptor molecule with an appropriate excitation energy.23,29,30 Both S2 and S1 states are active in energy transfer, with efficiencies of the two channels depending on energies and lifetimes of these states, which in turn depend on the number of conjugated CdC bonds. Consequently, the conjugation length is a key for understanding mechanisms and pathways of carotenoid-mediated energy transfer. Nevertheless, this rule is violated for a family of carotenoids containing a conjugated carbonyl group. Extension of conjugation to the carbonyl group induces formation of an additional singlet state with intramolecular charge-transfer character (SICT) in the excited-state manifold of carbonyl carotenoids, making their spectroscopic properties strongly dependent on the solvent polarity;31,32 thus, polarity becomes the key feature controlling energy transfer. Because these carotenoids are ubiquitous in marine photosynthetic organisms in which they act as very efficient light-harvesting pigments,33 employing carbonyl carotenoids in artificial antennas is of particular interest. From the point of view of potential application, the most attractive properties of carbonyl carotenoids are as follows: (1) shrinking the S2-S1 energy gap, leading to extension of the absorption spectrum beyond 550 nm while keeping the S1 state high enough to transfer energy efficiently to the Qy band of porphyrin-like acceptors.32 Accordingly, carbonyl carotenoids are capable of harvesting light in the 450-550 nm range, which corresponds to the maximum of solar irradiance curve. (2) Their behavior offers a possibility for tuning excited-state properties by changing the solvent polarity. (3) Employing carbonyl carotenoids in artificial systems can also provide an important feedback for understanding the roles of the SICT state in energy transfer in natural systems containing carbonyl carotenoids whose specific light-harvesting strategies have been revealed only recently,34-36 and details concerning the role of the SICT state are still a matter of debate.37-39 The use of carbonyl carotenoids in artificial systems has so far been limited to fucoxanthin- and peridinin-pyropheophorbide dyads synthesized about a decade ago.40,41 In both systems, energy transfer from carotenoid to pyropheophorbide was demonstrated by measurements of fluorescence excitation spectra.25,41 In addition, Osuka et al. have shown that both fucoxanthin and peridinin are able to quench triplet states of the attached pyropheophorbide,25 mimicking the photoprotective function of carotenoids in natural systems. Time-resolved spectroscopy was employed for a series of fucoxanthinpyropheophorbide dyads, and the energy transfer efficiency was shown to vary in the 12-44% range.18 Although these experiments unequivocally demonstrated that energy transfer from carotenoid to pyropheophorbide is active, they were performed and interpreted prior to the disclosure of polarity-driven behavior of carbonyl carotenoids,31,32 thus omitting the key spectroscopic features of carbonyl carotenoids. In this study, we focus on mechanisms and pathways of energy transfer in the peridinin-pyropheophorbide (hereafter denoted as dyad 1) and fucoxanthin-pyropheophorbide (dyad 2) dyads (see Chart 1) in solvents with different polarity and show, with the help of current knowledge about the photophysics of carbonyl carotenoids, that energy transfer in these dyads can be tuned by solvent polarity. This observation is in keeping with the behavior of natural light harvesting complexes containing the same carotenoids,34-36 which has been explained in terms of the active participation of the SICT state in the energy transfer process.
Polı´vka et al. CHART 1: Molecular Structures of the Peridinin-Pyropheophorbide (1) and the FucoxanthinPyropheophorbide (2) Dyads
2. Materials and Methods Sample Preparation and Spectroscopy. Both carotenoidpyropheophorbide dyads were synthesized and purified according to the procedures described elsewhere41 and prior to the experiments stored in the dark at -50°. Steady-state absorption measurements were performed on a Jasco-V-530 spectrophotometer in a 2-mm pathlength quartz cuvette. Fluorescence and fluorescence excitation spectra were recorded using a Spex Flurolog fluorimeter. For fluorescence and fluorescence excitation measurements, a 1-cm pathlength quartz cuvette was used and the optical density of the samples was kept below 0.1 OD/ cm. For transient absorption measurements, the dyads were dissolved in benzene, tetrahydrofuran (THF), and acetonitrile (all spectroscopic grade purchased from Sigma) and prior to the measurements loaded in a 2-mm pathlength quartz rotational cuvette to yield an optical density of 0.4-0.5 at the excitation wavelength. Femtosecond pulses were obtained from a Ti: sapphire oscillator pumped by the 5 W output of a CW frequency-doubled, diode-pumped Nd:YVO4 laser. The oscillator, operating at a repetition rate of 82 MHz, was amplified by a regenerative Ti:sapphire amplifier pumped by a Nd:YLF laser (1 kHz), producing ∼130 fs pulses with an average energy of ∼0.9 mJ/pulse and a central wavelength at 800 nm. The amplified pulses were divided into two paths: one to pump an optical parametric amplifier for generation of excitation pulses and the other to produce white-light continuum probe pulses in a 0.3 cm sapphire plate. The mutual polarization of the pump and probe beams was set to the magic angle (54.7°) using a polarization rotator placed in the pump beam. For signal detection, the probe beam and an identical reference beam (that had no overlap with the pump beam) were focused onto the entrance slit of a spectrograph, which then dispersed both beams onto a home-built dual photodiode array detection system. Each array contained 512 photodiodes and allowed a spectral range of ∼270 nm to be measured in each laser shot. The spectral resolution of the detection system was ∼80 cm-1 and the energy of excitation was attenuated by neutral density filters to ∼5. 1014 photons pulse-1 cm-2. Absorption spectra were measured before and after measurements to ensure that no permanent photochemical changes occurred over the duration of experiment. Analysis of Time-Resolved Spectra. To gain deeper insight into the excited-state dynamics, all transient spectra collected by the diode-array detection system were fitted globally. This approach allows more precise determination of the time constants of the excited-state processes and, more importantly,
Artificial Light-Harvesting Antennae
Figure 1. Absorption (thick solid), fluorescence (dashed), and fluorescence excitation spectra (symbols) of the dyad 1 (a) and 2 (b) in tetrahydrofuran. Absorption spectra are plotted as 1-T (T is transmittance) to allow calculation of energy transfer efficiencies by comparison with fluorescence excitation spectra. Fluorescence spectra were obtained after excitation at 490 nm. Detection wavelength for the fluorescence excitation spectra was 690 nm. For comparison, 1-T spectrum of pyropheophorbide in tetrahydrofuran is also shown (thin solid line).
assignment of spectral profiles of the intermediate excited-state species.42 The data were fitted to a sum of exponentials, including numerical deconvolution of the fwhm of the response function and a fourth degree polynomial describing the chirp. The fitting procedure used general linear regression for the amplitudes of the exponentials and the Nelder-Mead simplex method for the rate constants, the fwhm, and the chirp polynomial. To visualize the excited-state dynamics, we assume that the excited system evolves according to a sequential, irreversible scheme A f B, B f C, C f D, etc. The arrows represent increasingly slower monoexponential processes and the time constants of these processes correspond to lifetimes of the species A, B, C, D, etc. The spectral profiles of the species are called evolution-associated difference spectra (EADS), and provide information about the time evolution of the whole system.42 3. Results Absorption, fluorescence and fluorescence excitation spectra of the two dyads dissolved in THF are shown in Figure 1. The absorption spectra have three major spectral features: a broad absorption band in the 420-520 nm region, corresponding to the S2 r S0 transitions in the carotenoid moiety and two intense peaks (the Soret peak at 412 nm and the Qy at 668 nm) identifiable with the pyropheophrobide part. Upon comparing the absorption spectra of the dyad with the spectra of the constituent moieties, one sees that the absorption spectrum of each dyad corresponds closely to a sum of the absorption spectra
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Figure 2. (top) Absorption spectra of the dyad 1 in benzene (solid), tetrahydrofuran (dashed), and acetonitrile (dotted). The inset shows the solvent-induced shift of the Qy band of pyropheophorbide. (bottom) Fluorescence excitation spectra of the dyad 1 in benzene (solid), tetrahydrofuran (dashed) and acetonitrile (dotted). Detection wavelength was 690 nm. All spectra are normalized to the Soret band of pyropheophorbide.
of carotenoid and pyropheophorbide. The major difference between the two dyads is the ratio A465/A668 (where Aλ/nm denotes the absorbance at a monitoring wavelength λ), which equals 1.6 for dyad 1 but only 0.8 for dyad 2. The lower molar absorption coefficient of fucoxanthin, about 80% of that for peridinin,43 can account for only a part of the observed difference; it seems likely that the sample of dyad 2 examined in this study contained some free pyropheophorbide. When excited at 490 nm, where absorption by carotenoid dominates over that due to pyropheophorbide, each dyad exhibits a narrow emission band, peaking at 675 nm, that constitutes a mirror image of the Qy absorption of pyropheophorbide; this indicates that emission originates solely from pyropheophorbide and implicates carotenoid-pyropheophorbide energy transfer. Indeed, fluorescence excitation spectra show that the peridinin in dyad 1 contributes substantially to the observed signal (Figure 1a); for dyad 2, the efficiency of energy transfer from fucoxanthin is markedly lower; a finding that agrees with kinetic data presented later. Solvent effects on absorption and fluorescence excitation spectra of the two dyads are displayed in Figures 2 (dyad 1) and 3 (dyad 2). The spectral bands of pyropheophorbide exhibit a slight shift that depends on the polarizability of the solvent; the Qy absorption peak is located at 665 nm in acetonitrile, 668 nm in tetrahydrofuran, and 671 nm in benzene (inset of Figure 2). For the S2 r S0 transition in carotenoid, the vibrational bands suffer a loss of resolution in going from benzene to the more polar solvents tetrahydrofuran and acetonitrile. This effect is especially pronounced in dyad 1, where the vibrational bands of peridinin, clearly resolved in benzene, are smeared out in acetonitrile, the most polar of the three solvents used (Figure 2). This loss of vibrational structure is
470 J. Phys. Chem. C, Vol. 111, No. 1, 2007
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Figure 3. (top) Absorption spectra of the dyad 2 in benzene (solid), tetrahydrofuran (dashed), and acetonitrile (dotted). (bottom) Fluorescence excitation spectra of the dyad 2 in benzene (solid), tetrahydrofuran (dashed), and acetonitrile (dotted). Detection wavelength was 690 nm. All spectra are normalized to the Soret band of pyropheophorbide.
induced by solvent polarity, and is characteristic of a carotenoid with a conjugated carbonyl group.31,32 The dependence of the efficiency of carotenoid-pyropheophorbide energy transfer on the solvent polarity is especially noticeable for dyad 1 (Figure 2). The contribution made by peridinin to the excitation spectrum of dyad 1 clearly diminishes with increasing solvent polarity, indicating less-efficient energy transfer in polar solvents. In dyad 2, this trend, if present, is barely noticeable, and the overall fucoxanthin-pyropheophorbide energy transfer is rather inefficient, whatever the solvent polarity (Figure 3). This behavior is in agreement with previous studies of the fluorescence excitation spectra of the dyads in a slightly different set of solvents.25 Time-resolved data, obtained by exciting each dyad in the carotenoid spectral region and recording transient absorption spectra at different delays, provide further insight into the carotenoid-pyropheophorbide energy transfer. Results obtained for dyad 1 in solvents with different polarity, shown in Figure 4, underline the influence of solvent polarity on the excitedstate dynamics of peridinin. In all three solvents, the transient absorption spectra exhibit features typical of carbonyl carotenoids. Below 520 nm, one observes bleaching of the S2 r S0 band of peridinin. Changes at longer wavelengths are mainly due to excited-state absorption (ESA), but contrary to carotenoids lacking the conjugated carbonyl group, whose ESA is represented by a single spectral band due to the Sn r S1 transition, carbonyl carotenoids exhibit an additional, red-shifted ESA band.31,32 In peridinin, the Sn r S1 band occurs at 525 nm; it is more pronounced in nonpolar solvents and corresponds to the “normal” Sn r S1 transition; a broader, red-shifted band, appearing in the 550-650 nm region, represents the Sn r SICT transition.31,32,37 There is general agreement that the S1 and SICT states are coupled, but the exact nature of the coupling is still
Figure 4. Transient absorption spectra of the dyad 1 measured in three different solvents: benzene (top), tetrahydrofuran (middle), and acetonitrile (bottom). In all solvents, excitation was at 485 nm.
a matter of debate.38,39, 44 It is thought that, after initial SICT a S1 equilibration, these two states behave as a single hybrid state, with a complicated potential surface possessing S1 and SICT minima; this state will henceforth be designated as the S1/ICT state. Thus, the two ESA bands correspond to transitions from the S1-like and SICT-like minima belonging to the same potential surface;39 the intensity of the Sn r SICT band increases as the solvent polarity becomes larger, reflecting the stabilization of the SICT state of peridinin in polar solvents. The transient spectrum is dominated by the Sn r S1 transition in the nonpolar solvent benzene and by the Sn r SICT transition in the polar solvent acetonitrile; in the medium-polarity solvent tetrahydrofuran, both bands are present with approximately equal amplitudes. The foregoing assignment implies that, in contrast with the position of the Sn r S1 band, which should not show an appreciable solvent shift, the Sn r SICT band should undergo a pronounced blue shift in polar solvents, on account of the greater stabilization of the SICT state. This is borne out by the transient spectra, which show that the Sn r S1 band peaks at 525 nm in all solvents, but the Sn r SICT band moves, as the SICT minimum of the hybrid potential surface deepens with increasing solvent polarity, from 650 nm (benzene) to 630 nm (THF) or 590 nm (acetonitrile). The transient absorption spectra in all solvents contain, in addition to the peridinin spectral features, a narrow dip at around 670 nm, signifying the bleaching of the Qy band
Artificial Light-Harvesting Antennae
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Figure 6. EADS resulting from global fitting of data for dyads 1 (top) and 2 (bottom) in tetrahydrofuran. See text for details.
Figure 5. Transient absorption spectra of the dyad 2 measured in three different solvents: benzene (top), tetrahydrofuran (middle), and acetonitrile (bottom). In all solvents excitation was at 485 nm.
of pyropheophorbide as a result of carotenoid-pyropheophorbide energy transfer. In all three solvents, the dynamics during the first few picoseconds reflects the decay of the excited S2 state (
