Elucidation and Control of an Intramolecular Charge Transfer

Femtosecond pump–probe measurements were based on a mode-locked Ti:Sapphire regenerative amplifier (Spectra Physics, Hurricane-X).(19) Visible ...
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Elucidation and Control of an Intramolecular Charge Transfer Property of Fucoxanthin by a Modification of Its Polyene Chain Length Daisuke Kosumi,*,† Takayuki Kajikawa,‡ Satoshi Okumura,‡ Mitsuru Sugisaki,§ Kazuhiko Sakaguchi,∥ Shigeo Katsumura,‡ and Hideki Hashimoto*,†,§ †

Osaka City University Advanced Research Institute for Natural Science and Technology (OCARINA), 3-3-138 Sugimoto, Sumiyoshi-ku, Osaka 558-8585, Japan ‡ Department of Chemistry, School of Science and Technology, Kwansei Gakuin University, Gakuen, Sanda, Hyogo 669-1337, Japan § Department of Physics, Graduate School of Science, Osaka City University, 3-3-138 Sugimoto, Sumiyoshi-ku, Osaka 558-8585, Japan ∥ Department of Chemistry, Graduate School of Science, Osaka City University, 3-3-138 Sugimoto, Sumiyoshi-ku, Osaka 558-8585, Japan S Supporting Information *

ABSTRACT: Fucoxanthin is an essential pigment for the highly efficient light-harvesting function of marine algal photosynthesis. It exhibits excited state properties attributed to intramolecular charge transfer (ICT) in polar environments due to the presence of the carbonyl group in its polyene backbone. This report describes the excited state properties of fucoxanthin homologues with four to eight conjugated double bonds in various solvents using the femtosecond pump−probe technique. The results clarified that fucoxanthin homologues with longer polyene chains did not possess pronounced ICT spectroscopic signatures, while the shorter fucoxanthin homologues had a strong ICT character, even in a nonpolar solvent. On the basis of the observations, we quantitatively correlated the ICT character in the excited state to the conjugated polyene chain lengths of fucoxanthin molecules. SECTION: Spectroscopy, Photochemistry, and Excited States

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highly efficient in several photosynthetic antennas from purple bacteria.2,3 On the other hand, carotenoids containing a carbonyl group in their conjugated polyene backbone, such as fx and peridinin, generate the intramolecular charge transfer (ICT) state below S1 in polar environments, forming the strongly coupled S1/ICT state.7 Consequently, the S0−S1/ICT transition dipole moment of carbonyl carotenoids increases due to their charge transfer character, and efficient energy transfer from carbonyl carotenoids to (bacterio)chlorophyll a via S1/ ICT is realized in light-harvesting photosynthetic antennas.8−12 The excited state dynamics of carbonyl carotenoids in solution and bound to pigment−protein complexes have been investigated intensively by ultrafast spectroscopic techniques.7−21 Although naturally occurring carbonyl carotenoids do not include an effective electron donor in their chemical structures, the critical factors for generating an ICT character have not yet been determined. Recent ultrafast spectroscopic

arine algae such as brown algae and diatoms play major roles in oceanic biochemical cycles and primary biomass productions.1 Fucoxanthin (fx) is the most abundant and naturally occurring carotenoid on the earth, which is a photosynthetic pigment from marine algae. It absorbs light in the blue-green region of the spectrum and transfers to chlorophyll rapidly and efficiently in their photosynthetic antennas,2,3 and the transferred energy is eventually converted to electro-chemical energy in reaction centers. The excited states of carotenoids are described traditionally by a threeelectronic level system (S0, S1, and S2).4 The optically allowed S2 (11Bu+) state is generated by a one-photon transition from the S0 ground state (11Ag−), and rapidly decays to the lowerlying S1 (21Ag−) state with ∼100 fs.2,3,5,6 A nonradiative relaxation from S1 to S0 is comparatively slower (ps−ns),2 while the S1−S0 transition is optically forbidden because of the same symmetry of their wave functions.4 The optically forbidden character (S1) of carotenoids appears to not function as an effective energy donor in terms of a Förster-type energy transfer mechanism with a weak Coulomb interaction. Indeed, excitation energy transfer from the carotenoid S1 state to (bacterio)chlorophyll is often inefficient, even though that is © 2014 American Chemical Society

Received: January 6, 2014 Accepted: February 10, 2014 Published: February 10, 2014 792

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constant of 60 fs and decays with time constants of 0.35 and 2.1 ps, while a blue-side (2.48 eV) of the transient absorption has slow rise components of 0.35 and 2.1 ps. The decay of the transient absorption signal probed at 2.48 eV was associated with the decay of the S1/ICT stimulated emission (10.4 ps). Therefore, the transient absorption at 2.3 eV was assigned to the transition from S1/ICT to a higher excited state. The determined S1/ICT lifetime of 10.4 ps for C32fx in methanol was much shorter than that of native C40fx in methanol (18.2 ps).19−21 The 0.35 and 2.1 ps components are assignable to vibrational relaxation processes in the S1/ICT state because the amplitudes of these components depend on a probe energy. The appearance of the two time-constants of 0.35 and 2.1 ps during thermal equilibrium in the S1/ICT state may be interpreted as the two potential energy landscapes with the different curvatures owing to the strong coupling between the S1 and ICT states, as shown in Figure 2C. Figure 3A represents a series of the steady-state and PIA spectra of the fx homologues. The steady-state absorption bands, corresponding to the S0−S2 transitions, red-shifted with an increase in n, following the relation E = 1/(2n + 1) between an excited state energy E and n.4 The absorption bands became broader with solvent polarity, owing to the ICT character of both the ground and excited states.7,34 In the PIA spectra, the transient absorption of the native fucoxanthin (C40fx) in cyclohexane contained a monotonic band attributed to the transition from S1 to a higher Sn (n1Bu+) state,2 while an additional band just below the S1 transient absorption band, assigned to the ICT-like band,14,19−21 increased with solvent polarity, suggesting that the ICT state is stabilized in polar environments.7 In the longest C42fx, the only S1-like transient absorption band appeared even in polar solvents, due to insufficient stabilization of the ICT state even though the S1 transient absorption band broadened with an increase in solvent polarity. In contrast, both of the S1 and ICT-like transient absorption bands were observed clearly in the shorter C37 fx in all solvents; the transient absorption bands of C35fx and C32fx became monomeric in polar solvents. By extrapolation of the ICT-like transient absorption energies of C37fx and C40fx in polar solvents, the monomeric absorption bands of C32fx and C35fx observed in polar solvents were assigned to the ICT-like transient absorption because the S1 transient absorption energies of C32fx and C35fx should appear above 2.5 eV. In addition, the ICT-like transient absorption band predominated, and the stimulated emission from S1/ICT was observed in the shortest C32fx, even in cyclohexane. These results suggest that the shorter fx homologues possess a stronger ICT character and that the monomeric band in C32fx and C35fx was due to a sufficiently stabilized ICT state (energetically much lower than S1), forming a monominimum potential energy surface of the strongly coupled S1/ICT state as shown in Figure 2C. Figure 3B shows a series of kinetic traces of the S1/ICT transient absorption of the fx homologues with varying n in different solvents. The solid lines represent the best-fit curves for the rise and decay phases convoluted with the instrumental response function. The kinetic traces were analyzed globally. Although the kinetic traces include the S2 lifetime, the S1/ICT lifetime, and vibrational relaxation in S1/ICT, special attention was paid to the longest time constants attributed to the S1/ICT lifetimes (see the Supporting Information for the timeconstants of other components). In all fx homologues, the S1/ICT lifetimes decreased with an increase in solvent polarity.

investigations on carbonyl carotenoids have suggested that ICT character depends on the carbonyl group position,22 the asymmetry of a carbonyl group rather than asymmetry of the entire molecule,23−27 and the conjugation length of polyene chain.13,15,28−30 The present study focused on the ICT character of fx homologues that could be correlated to conjugated polyene chain lengths. Femtosecond pump−probe spectroscopic measurements with 100 fs time-resolution19,31 were performed on fx homologues with varying numbers of conjugated double bonds (4−8)32,33 as illustrated in Figure 1.

Figure 1. Chemical structures of fx series.

An ICT character of carbonyl carotenoids has often been estimated by (1) solvent polarity-dependent S1/ICT lifetimes, (2) amplitudes of the ICT transient absorption and stimulated emission bands, and (3) a dipole moment of the ICT state. In this study, ICT properties of fx homologues are characterized by the S1/ICT lifetimes and the transient absorption and stimulated emission bands due to the S1/ICT state. Figure 2 shows the photoinduced absorption (PIA) spectra and corresponding kinetic traces of the shortest fx homologue (C32fx) in methanol excited into the S2 band. As shown in Figure 2A, a strong transient absorption appeared ca. 2.3 eV and its red-tail extended to 1.8 eV at a delay time of 0.1 ps. This red-tail subsequently translated to a negative signal at 0.3 ps, assigned to stimulated emission from the strongly coupled S1/ ICT state due to an increase in a charge transfer character.14 An appearance of the transient absorption below 2.1 eV before the formation of the S1/ICT state suggests that this is assignable to the S2 transient absorption. The kinetic trace at 2.03 eV shows that the S2−S1/ICT internal conversion occurs with a timeconstant of 60 fs (Figure 2B). The prominent transient absorption band at 2.3 eV became narrower and blue-shifted with an increase in a delay time. The red-side (2.17 eV) of the prominent transient absorption band formed with a time793

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Figure 2. (A) Steady-state and PIA spectra of C32fx in methanol given by excitation at 3.18 eV and (B) their kinetic traces. (C) A schematic representation of the excited state dynamics of the C32fx in methanol.

Figure 3. (A) Steady-state and PIA spectra of fx homologues in several solvents. PIA spectra were recorded at 3.0 ps after excitation into the S2 state. Arrows indicate excitation energies. (B) Kinetic traces of the S1/ICT transient absorption of fx homologues in several solvents.

This polarity-induced modulation of the S1/ICT lifetimes became pronounced with decrease of n, except for C32fx. Furthermore, the S1/ICT lifetimes did not exhibit a monotonic dependence on n, i.e., they had the longest lifetimes with n = 6 in polar solvents (methanol: 22.4 ps and acetone: 94 ps) or with n = 5 in nonpolar solvent (cyclohexane: 182 ps). Figure 4A represents the S1/ICT nonradiative relaxation rates (an inverse number of lifetime) of the fx homologues as a function of 1/(2n + 1). The nonradiative relaxation rate of an

excited state in a molecular system often is expressed through the energy gap law defined as: k = A exp( −BΔE)

(1)

where A, B, and ΔE denote the coupling strength between electronic states, the coefficient related to vibrational frequency coupled to an electronic state, and an energy gap between electronic states, respectively.35 The S1 nonradiative relaxation rates of carotenoids without a carbonyl group are generally accepted to decrease monotonically with n because the S1−S0 794

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which is associated with the enhancement of the S1/ICT nonradiative relaxation rate. It should be noted that ϕ does not reflect a charge transfer character of the ICT state itself (such as the dipole moment strength of the ICT state or the S0−ICT transition dipole moment). Recent experimental and theoretical investigations confirmed that the ICT state has a large dipole change.22,30,38 However, it is difficult to determine the dipole moment change between the S0 and ICT state by pump−probe measurements. Therefore, we characterized ICT properties of the fx homologues by the S1/ICT coupling strength instead of the dipole moment change. Figure 4B is plotted ϕ as a function of n, where ϕ = 1 means that the S1 decay is not enhanced by the coupling to the ICT state. In methanol, ϕ monotonically increases from n = 8 to 4. In contrast, the coupling strength in acetone and cyclohexane is weak (ϕ ∼ 1) with n = 6−8, whereas it exhibits a large value at C32fx (n = 4) and C35fx (n = 5). It has been reported that the mixing of S2 (11Bu+) and S1 (21Ag−) can be generated in peridinin on a basis of quantumchemical calculations.38 The S2 and S1 mixing can also enhance the S1 decay and the S1 stimulated emission due to an increase of ionic character of the S1 state, and is more pronounced in short polyene molecules because of a small S2−S1 energy gap.30 Thus, the short S1/ICT lifetime of C32fx in a nonpolar solvent can be explained by a consideration of the S2−S1 mixing rather than a strong ICT character. On the other hand, the S2−S1 mixing should occur in short carotenoids without a carbonyl group, while the S1 decay of short carotenoids is well explained by the energy gap law,5 i.e., the S1 decay is not enhanced by the S2−S1 mixing. Thus, our results demonstrate that the strongly coupled S1/ICT state of the shorter C32fx and C35fx homologues was realized by stabilization of the ICT state, even in a nonpolar solvent. The strongly coupled S1/ICT states of C32fx and C35fx in cyclohexane are supported by the observation of monomeric transient absorption bands and the stimulated emission of S1/ICT, as shown in Figure 3A (see also Figures S1−S5 in the Supporting Information). The S2 and S1 energies of carotenoids obey the relation E = 1/(2n+1),4 despite the lack of clarification on how to physically describe the ICT state energy of carbonyl carotenoids. Niedzwiedzki et al. suggested that the ICT state energies of peridinin homologues with different n values (n = 5−8) are independent of conjugation length because the ICT state is highly localized around the carbonyl group.13 On the other hand, the authors recently showed the conjugation length dependence of the ICT states.30,37 Then, the data shown in Figure 4A imply that the energy of the ICT state of fx homologues may decrease with n, because the S1/ICT relaxation rates increase with a decrease in n. Naturally occurring carbonyl carotenoids, such as fucoxanthin and peridinin, do not have an effective electron donor,17 so electron density (charge) of the excited state is transferred from πelectrons in the polyene backbone to the carbonyl group.38 As a result, a larger perturbation of the π-electron distribution is formed in the rest of the polyene chain. This effect can be enhanced in the shorter fx homologues and can facilitate generation of the well-stabilized ICT state located much lower than S1, realizing a strong coupling of the S1 and ICT states, even in a nonpolar solvent. Unfortunately, our observations did not clarify whether the shorter fx homologues generate the ICT state with a larger dipole moment change or transition dipole moment between the S0 and ICT state than the longer fx homologues. In a future work, such parameters of the ICT state should be determined by quantum-chemical calculations to gain

Figure 4. (A) The nonradiative relaxation rates of S1/ICT as a function of 1/(2n + 1) or n. A solid line denotes a theoretical curve by the energy gap law. (B) The coupling strength of S1 and ICT states as a function of 1/(2n + 1) or n.

energy gap also decreases with n.2 The solid line in Figure 4(A) denotes the best-fit curve using eq 1 for the S1 nonradiative relaxation rates of β-carotene homologues (n = 7−15), as reported previously.36 The S1 lifetimes of fx homologues should obey the energy gap law if the S1 decay cannot be enhanced by coupling of the ICT state. The S1 (S1/ICT) lifetime of C42fx can be explained by the energy gap law, i.e., C42fx shows no ICT character, even in a polar solvent, consistent with a weak solvent polarity-dependence of the S1 (S1/ICT) lifetimes and the absence of the ICT-like band in the PIA spectra. By contrast, the S1/ICT lifetimes clearly deviate from the energy gap law with a decrease in n, suggesting that the S1/ICT lifetimes of the shorter fx homologues (n < 8 for methanol and n < 6 for acetone and cyclohexane) are enhanced by the strong coupling of the S1 and ICT states, even in a nonpolar solvent. In fact, the carbonyl carotenoids C29- and C33-peridinin homologues with conjugated double bonds (n = 4 and 5) equivalent to C32fx and C35fx had much longer lifetimes of 2.9 ns (C29-peridinin) and 4.0 ns (C35-peridinin) in a nonpolar solvent (hexane) than those of C32fx (56 ps) and C35fx (182 ps) in cyclohexane.13,30,37 Further, we examined to estimate the coupling strength of the S1 and ICT states quantitatively. With an assumption that the intrinsic S1 nonradiative relaxation rate kintrinsic of the fx homologues can be described by the energy gap law, we introduced ϕ = kS1/ICT/kintrinsic as the S1/ICT coupling strength, 795

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Notes

more insight into photophysical properties of fx. The results described here are clearly distinct from previously reported results of the conjugation length dependence of S1/ICT dynamics of the carbonyl carotenoid peridinin13,30,37 or apocarotenal,29 which did not exhibit strong ICT character in nonpolar solvents. Especially, by combination of transient absorption measurements and quantum-chemical calculations, Magdaong et al., suggest that C29-peridinin with n = 4 possesses a weaker ICT character than peridinin.30 The difference of the conjugation length dependent ICT characters between fucoxanthin and peridinin may originate from their chemical structures (see the Supporting Information). Further experimental and theoretical works should clarify the correlation between chemical structures of carbonyl carotenoids to the generation of their ICT character. Nevertheless, the findings obtained in this study shed light on the nature and origin of the ICT character, which is required to reveal the highly efficient energy transfer mechanisms of marine algal photosynthetic systems. Further, the results obviously demonstrate that the ICT character of fucoxanthin can be systematically controlled for a construction of artificial photosynthetic antennas, absorbing light with various wavelengths, by the modification of its polyene chain length.

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS This work was partially supported by Grant-in-Aids for Young Scientists (A) (No. 25707028 to D.K.) and Scienctic Research on Inovative Areas “All Nippon Artificial photosynthesis Project for Living Earth (AnApple)” (No. 24107002 to HH) from the Japan Society for the Promotion of science (JSPS).

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(1) Falkowski, P. G.; Barber, R. T.; Smetacek, V. Biogeochemical Controls and Feedbacks on Ocean Primary Production. Science 1998, 281, 200−206. (2) Polivka, T.; Sundstrom, V. Ultrafast Dynamics of Carotenoid Excited States-from Solution to Natural and Artificial Systems. Chem. Rev. 2004, 104, 2021−2071. (3) Polivka, T.; Frank, H. A. Molecular Factors Controlling Photosynthetic Light Harvesting by Carotenoids. Acc. Chem. Res. 2010, 43, 1125−1134. (4) Linear Polyene Electronic Structure and Potential Surfaces; Hudson, B. S.; Kohler, B. E.; Schulten, K., Eds.; Academic Press: New York, 1982; Vol. 6. (5) Polli, D.; Cerullo, G.; Lanzani, G.; De Silvestri, S.; Yanagi, K.; Hashimoto, H.; Cogdell, R. J. Conjugation Length Dependence of Internal Conversion in Carotenoids: Role of the Intermediate State. Phys. Rev. Lett. 2004, 93, 163002. (6) Kosumi, D.; Yanagi, K.; Fujii, R.; Hashimoto, H.; Yoshizawa, M. Conjugation Length Dependence of Relaxation Kinetics in β-Carotene Homologs Probed by Femtosecond Kerr-Gate Fluorescence Spectroscopy. Chem. Phys. Lett. 2006, 425, 66−70. (7) Bautista, J. A.; Connors, R. E.; Raju, B. B.; Hiller, R. G.; Sharples, F. P.; Gosztola, D.; Wasielewski, M. R.; Frank, H. A. Excited State Properties of Peridinin: Observation of a Solvent Dependence of the Lowest Excited Singlet State Lifetime and Spectral Behavior Unique among Carotenoids. J. Phys. Chem. B 1999, 103, 8751−8758. (8) Kosumi, D.; Kita, M.; Fujii, R.; Sugisaki, M.; Oka, N.; Takaesu, Y.; Taira, T.; Iha, M.; Hashimoto, H. Excitation Energy-Transfer Dynamics of Brown Algal Photosynthetic Antennas. J. Phys. Chem. Lett. 2012, 3, 2659−2664. (9) Gildenhoff, N.; Herz, J.; Gundermann, K.; Büchel, C.; Wachtveitl, J. The Excitation Energy Transfer in the Trimeric Fucoxanthin− Chlorophyll Protein from Cyclotella meneghiniana Analyzed by Polarized Transient Absorption Spectroscopy. Chem. Phys. 2010, 373, 104−109. (10) Papagiannakis, E.; van Stokkum, I. H. M.; Fey, H.; Buchel, C.; van Grondelle, R. Spectroscopic Characterization of the Excitation Energy Transfer in the Fucoxanthin-Chlorophyll Protein of Diatoms. Photosynth. Res. 2005, 86, 241−250. (11) Zigmantas, D.; Hiller, R. G.; Sundstrom, V.; Polivka, T. Carotenoid to Chlorophyll Energy Transfer in the PeridininChlorophyll-a-Protein Complex Involves an Intramolecular Charge Transfer State. Proc. Natl. Acad. Sci. U. S. A. 2002, 99, 16760−16765. (12) Slouf, V.; Chabera, P.; Olsen, J. D.; Martin, E. C.; Qian, P.; Hunter, C. N.; Polivka, T. Photoprotection in a Purple Phototrophic Bacterium Mediated by Oxygen-Dependent Alteration of Carotenoid Excited-State Properties. Proc. Natl. Acad. Sci. U. S. A. 2012, 109, 8570−8575. (13) Niedzwiedzki, D. M.; Chatterjee, N.; Enriquez, M. M.; Kajikawa, T.; Hasegawa, S.; Katsumura, S.; Frank, H. A. Spectroscopic Investigation of Peridinin Analogues Having Different π-Electron Conjugated Chain Lengths: Exploring the Nature of the Intramolecular Charge Transfer State. J. Phys. Chem. B 2009, 113, 13604− 13612. (14) Zigmantas, D.; Hiller, R. G.; Sharples, F. P.; Frank, H. A.; Sundstrom, V.; Polivka, T. Effect of a Conjugated Carbonyl Group on the Photophysical Properties of Carotenoids. Phys. Chem. Chem. Phys. 2004, 6, 3009−3016.

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EXPERIMENTAL METHODS Femtosecond pump−probe measurements were based on a mode-locked Ti:Sapphire regenerative amplifier (Spectra Physics, Hurricane-X).19 Visible excitation pulses were obtained from an optical parametric amplifier (Spectra Physics, OPA800CF) or obtained by the second harmonic generation using a 0.4 mm thick BBO crystal. A white light continuum probe pulse, generated using a 5.0 mm sapphire plate, was detected by a photodiode array through a spectrometer. The excitation pulses were modulated at 500 Hz by an optical chopper and the data output was synchronized with the laser repetition of 1 kHz.39 Excitation intensity was adjusted to 20 nJ/pulse. A relative polarization between the excitation and probe pulses was set to the magic angle (54.7°). The instrumental response function and the precise zero time delay at each probe energy of the system were determined by the cross-correlation between excitation and probe pulses which was better than 100 fs (typically 80 fs, but it depends on the pump and probe energies). After chirp compensation, the uncertainty in the zero time delay was better than 10 fs. Detailed descriptions of the total synthesis of the fx homologues are described elsewhere.32,33 Samples were dissolved in three different solvents (methanol, acetone, and cyclohexane) and were circulated in a flow cell.

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ASSOCIATED CONTENT

* Supporting Information S

Complete sets of the photoinduced absorption spectra of fucoxanthin homologues, the obtained time-constants, and comparison of the chemical structures of fucoxanthin and peridinin and their homologues with n = 4. This material is available free of charge via the Internet at http://pubs.acs.org.

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REFERENCES

AUTHOR INFORMATION

Corresponding Authors

*E-mail: [email protected]. *E-mail: [email protected]. 796

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