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A first detection of singlet to triplet conversion from the 11Bu− to the 13Ag state and triplet internal conversion from the 13Ag to the 13Bu state in carotenoids: dependence on the conjugation length
Chemical Physics Letters 376 (2003) 292–301 www.elsevier.com/locate/cplett
A first detection of singlet to triplet conversion 3 from the 11B u to the 1 Ag state and triplet internal conversion from the 13Ag to the 13Bu state in carotenoids: dependence on the conjugation length Ferdy S. Rondonuwu a, Yasutaka Watanabe a, Ritsuko Fujii b, Yasushi Koyama b,* a b
Department of Physics, Faculty of Science and Technology, Kwansei Gakuin University, 2-1 Gakuen, Sanda 669-1337, Japan Department of Chemistry, Faculty of Science and Technology, Kwansei Gakuin University, 2-1 Gakuen, Sanda 669-1337, Japan Received 22 January 2003; in final form 21 April 2003 Published online: 2 July 2003
Abstract Subpicosecond time-resolved absorption spectra were recorded in the visible region for a set of photosynthetic carotenoids having different numbers of conjugated double bonds (n), which include neurosporene (n ¼ 9), spheroidene (n ¼ 10), lycopene (n ¼ 11), anhydrorhodovibrin (n ¼ 12) and spirilloxanthin (n ¼ 13). Singular-value decomposition and global fitting of the spectral-data matrices lead us to a branched relaxation scheme including both (1) the singlet 1 1 1 internal conversion in the sequence of 11 Bþ u ! 1 Bu ! 2 Ag ! 1 Ag (ground), and (2) the singlet-to-triplet conversion 1 3 3 of 1 Bu ! 1 Ag followed by triplet internal conversion of 1 Ag ! 13 Bu . Ó 2003 Elsevier B.V. All rights reserved.
1. Introduction All-trans carotenoids are selectively bound to the antenna complexes mainly for the light-harvesting function [1–4]. Their conjugated chain has approximate C2h symmetry, which gives rise to the 1 1 þ 1 þ singlet states of k1 A g , l Bu , m Ag and n Bu type. (Here, Ô1Õ signifies the singlet states, + and ) are PariserÕs signs showing the symmetry of electronic
*
Corresponding author. Fax: +81-79-565-9077. E-mail address: [email protected] (Y. Koyama).
configurations [5,6], and k, l, m and n are the labeling of a series of electronic states having the same symmetry from the lower to the higher energy. Concerning optical transitions from the 1 þ 1 þ ground 11 A g state, the Ag and Bu states are classified into Ôoptically allowedÕ states, whereas 1 the 1 A g and Bu states to the Ôoptically forbiddenÕ states.) Tavan and Schulten [7,8] calculated the state energies of low-lying singlet states for shorter polyenes having the number of conjugated double bonds n ¼ 5–8, and exhibited their linear relations as functions of 1=ð2n þ 1Þ. The slopes of the linear relations were shown to be in the ratio 2:3.1:3.7 for
0009-2614/03/$ - see front matter Ó 2003 Elsevier B.V. All rights reserved. doi:10.1016/S0009-2614(03)00983-7
F.S. Rondonuwu et al. / Chemical Physics Letters 376 (2003) 292–301 1 1 the covalent 21 A g , 1 Bu and 3 Ag states, reflecting the momentum quantum number of 2, 3 and 4, respectively. Measurements of resonance-Raman excitation profiles (RREPs) for carotenoids with n ¼ 9–13 lead us to a first spectroscopic identification of 1 the 11 B u and 3 Ag states [9–11] in addition to the well-documented 11 Bþ and 21 A states [1–4] u g (shown in Fig. 1). The arrangement of the four singlet excited states was in good agreement with that obtained by extrapolation of the above linear
1 1 1 Fig. 1. An energy diagram for the 11 Bþ u , 3 Ag , 1 Bu and 2 Ag singlet states for crystalline mini-9-b-carotene (n ¼ 9), spheroidene (n ¼ 10), lycopene (n ¼ 11), anhydrorhodovibrin (n ¼ 12) and spirilloxanthin (n ¼ 13) determined by measurements of resonance-Raman excitation profiles [9–11] and for the 13 Bu (T1 ) state for neurosporene (n ¼ 9), spheroidene (n ¼ 10) and lycopene (n ¼ 11) bound to the LH2 complexes determined by emission spectroscopy (Rondonuwu et al., unpublished).
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1 relations; their slopes for the 21 A g , 1 Bu and 1 3 Ag states turned out to be in the ratio 2:3.1:3.8, establishing the state energies determined by RREPs. Visible [12] and near-infrared [13] subpicosecond time-resolved absorption spectroscopy as well as subpicosecond time-resolved Raman spectroscopy [14] identified internal conversion processes in neurosporene (n ¼ 9) that were in accord with the state ordering shown in the energy diagram, 1 1 1 i.e., 11 Bþ (see Fig. 1). u ! 1 Bu ! 2 Ag ! 1 Ag Further, near-infrared, subpicosecond time-resolved absorption spectroscopy for a series of carotenoids (n ¼ 9–13) [15] identified two different pathways of internal conversion that were also in accord with the energy diagram, i.e., 11 Bþ u ! 1 1 11 B ! 2 A !1 A for carotenoids with n ¼9 u g g 1 1 1 and 10, whereas 11 Bþ ! 3 A ! 2 A ! 1 A u g g g for carotenoids with n ¼ 11–13. Recently, van Grondelle and co-workers [16,17] have proposed an alternative pathway of relaxation, i.e., singlet-to-triplet conversion starting from an ÔS*Õ state. In the case of spirilloxanthin [16], it was reported that this state functioned as a precursor of the triplet state when bound to the LH1 complex from Rhodospirillum rubrum, whereas it directly relaxed to the ground state when free in solution. The S* ! T transformation in the antenna complex took only 12 ps. In the case of spheroidene bound to the LH2 complex from Rhodobacter sphaeroides also [17], the generation of the S* state and subsequent transformation into the triplet state was observed. Deep insight into the above results by the authors, taking into account the theoretical analysis of shorter polyenes by Tavan and Schulten [7,8], lead them to ascribe the above S* ! T reaction to a singlet-to-triplet conversion in the individual carotenoid molecule. The authors assessed that the S* state likely corresponds to the 11 B u state, although they excluded the possibility that the 1 þ 11 B u state is located in-between the 1 Bu and the 1 1 þ 1 2 Ag states, mediating the 1 Bu ! 2 Ag internal conversion [9,10]. Their interpretation was based on the 10-fs time-resolved absorption data then available [18]; now the presence of an intermediate state, i.e., Ôthe Sx state of 11 B u symmetryÕ, is proposed, instead [19].
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Since the generation of the 13 Bu (T1 ) state by direct photo-excitation of carotenoids was observed free in solution by picosecond Raman [20] and absorption [21] spectroscopies, and since the above singlet-to-triplet fission reaction was ascribed to an intramolecular reaction in nature [16,17], we started searching for this reaction in solution. We have addressed the following three specific questions: (1) what is the S* state? By definition it is a singlet state that facilitates carotenoidto-bacteriochlorophyll singlet-energy transfer [17], but its spectrum so far presented is somewhat similar to a triplet spectrum [16,17]. Is that really the 11 B u state that have been already identified in neurosporene [12]? If the answer is ÔyesÕ, then (2) what kind of triplet state(s), i.e., 13 Ag (T2 ) and/or 13 Bu (T1 ), can be directly generated from the 11 B u singlet state? Because of the symmetry relation, 3 3 11 B u ¼ 1 Ag 1 Bu , both triplet species can be generated in principle [8]. If the still unidentified 13 Ag (T2 ) state is found, then (3) does the internal conversion in the triplet manifold, i.e., 13 Ag (T2 ) ! 13 Bu (T1 ), actually take place to generate the well-documented 13 Bu (T1 ) state?
2. Experimental All-trans carotenoids (hereafter, Ôall-trans’ will be abbreviated throughout this Letter) were prepared as described previously [15]. In time-resolved absorption measurements, neurosporene and spheroidene were dissolved in n-hexane; lycopene and anhydrorhodovibrin were dissolved in a mixture of benzene and n-hexane (5:95 v/v); and spirilloxanthin was dissolved in a mixture of benzene and n-hexane (50:50 v/v). The concentration of each carotenoid solution was adjusted to OD ¼ 5 cm1 at the absorption maximum, corresponding to the concentrations of 3.1, 2.9, 2.7, 2.9 and 3.3 105 M for neurosporene, spheroidene, lycopene, anhydrorhodovibrin and spirilloxanthin, respectively. Each solution (30 ml) was circulated between a quartz flow cell (optical pathlength, 1 mm) and a reservoir that was cooled in ice-water. Each carotenoid was excited to the 11 Bþ u ðv ¼ 0) vibronic level at the following wavelength: neurosporene (467 nm), spheroidene (483 nm), lycopene
(501 nm), anhydrorhodovibrin (515 nm) and spirilloxanthin (536 nm). Subpicosecond time-resolved absorption spectra in the 400–700 nm region were recorded as described previously [22] except for the following modifications: a 1-cm water cell was used to generate the visible 400–700 nm Ôwhite continuumÕ for probing. The pumping energy was adjusted to 0.6 lJ/pulse at the sample cell corresponding to a photon density of 1.5 1014 photon cm2 . Each time-resolved spectrum in the )2 to 50 ps region was obtained by accumulating the data of 400 pulses, while that in the 25 ps to 1 ns region was obtained by accumulating the data of 50 400 pulses. The procedure of singular-value decomposition (SVD) and global fitting used for spectral analyses was basically the same as describe previously ([22] and references therein): analyzed were data matrices in the 400–700 nm spectral and the )2 to 50 ps delay-time regions, whose dimensions being 1105 275 for neurosporene, spheroidene and lycopene, and 1105 237 for anhydrorhodovibrin and spirilloxanthin. We have picked up the major four components that were obtained by SVD in order to accommodate the four different spectral patterns recognized in the raw time-resolved data. They were further analyzed by global fitting to obtain species-associated difference spectra (SADS) and time-dependent changes in population. In the global fitting, we eventually used a branched relaxation scheme, consisting of a sequential singlet 1 1 1 internal conversion (11 Bþ u ! 1 Bu ! 2 Ag ! 1 Ag ), and intramolecular singlet-to-triplet conversion 3 (11 B u ! 1 Ag ) followed by triplet internal conver3 sion (1 Ag ! 13 Bu ). Before reaching to this scheme, we have tried various relaxation schemes, including (i) sequential scheme with three (11 Bþ u ! 1 3 1 þ 1 11 B !2 A + 1 A !Þ and four (1 B ! 1 B g u g u u ! 3 21 A ! 1 A !Þ components, (ii) a scheme brang g ched from the 21 A g state with four components 1 1 3 (11 Bþ ! 1 B ! 2 Ag ! plus 21 A u u g ! 1 Ag !Þ, 1 and (iii) a scheme branching from 1 Bu and re1 þ turning to 21 A g with four components (1 Bu ! 1 1 1 3 1 1 Bu ! 2 Ag ! plus 1 Bu ! 1 Ag ! 2 Ag ). Those unsuccessful models caused strong mixing among SADS and/or negative population for some component(s).
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3. Results and discussion 3.1. Time-resolved absorption spectroscopy in the subpicosecond to decapicosecond time regime: identification of a relaxation scheme branching from the 11 B u state (i) Characterization of the time-resolved spectra. Fig. 2 (the top panels) shows time-resolved spectra in the 0–15 ps region for a set of carotenoids, including (a) neurosporene (n ¼ 9), (b) spheroidene (n ¼ 10), (c) lycopene (n ¼ 11), (d) anhydrorhodovibrin (n ¼ 12) and (e) spirilloxanthin (n ¼ 13). Time-dependent spectral changes are similar to one another among all the carotenoids, and the sequence can be characterized as follows based on the results of neurosporene in n-hexane [12]: first,
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stimulated emission from the optically allowed 11 Bþ u state appears with vibrational progression. Second, a broad transient absorption from the optically forbidden 11 B u state extending to the red appears together with the bleaching of the groundstate 11 Bþ 11 A u g absorption (shown on the top of each set of time-resolved spectra). Third, sharp transient absorption from the 21 A g state, which has been well-documented [21,23,24], appears accompanying the bleaching of the ground-state absorption. Almost in parallel, an indication of triplet absorption appears as a shoulder on the blue side of the 21 A g transient absorption. A set of time-resolved spectra after long delay times (the central panels) clearly exhibit the differencespectrum pattern due to a triplet state; at those delay times, the contribution of the 21 A g transient
Fig. 2. Subpicosecond, time-resolved absorption spectra in the 0–15 ps region (the top panels) for (a) neurosporene and (b) spheroidene, (c) lycopene, (d) anhydrorhodovibrin and (e) spirilloxanthin. The ground-state 11 Bþ 11 A u g absorption spectra are shown on the top of each set of time-resolved spectra. The time-resolved spectra of the 13 Ag (T2 ) state obtained by direct photo-excitation after long delay times (the central panels) and those of the 13 Bu (T1 ) state obtained at 1.8 ls after triplet-sensitized excitation (the bottom panels) are also shown for comparison.
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absorption becomes minimum (in neurosporene and spheroidene) or negligible (in lycopene, anhydrorhodovibrin and spirilloxanthin). The parallel rise of the 21 A g -state and the triplet-state absorptions suggests that the particular triplet state is generated not from the 21 A g state but from the 11 B u state. The time scales of the above sequential changes vary systematically depending on the length of the conjugated chain: When n increases, the 11 Bþ u stimulated emission decays faster, the 11 B and 21 A u g transient absorptions rise and decay more rapidly, and the triplet absorption becomes clearer. Fig. 2 (the bottom panels) also exhibits the transient absorption spectra of the lowest triplet state, i.e., the 13 Bu (T1 ) state, that were recorded at 1.8 ls after excitation of the sensitizer, anthracene. The difference-spectrum patterns of the T1 state for those photosynthetic carotenoids have been well documented (see [25,26] for example). Importantly, the difference-spectrum patterns of the above triplet state generated by direct photo-excitation (the central panels) are completely different from those of the 13 Bu (T1 ) state that was generated by sensitized photo-excitation (the bottom panels). Tavan and Schulten [8] showed, based on theoretical considerations, (1) the 11 B u state has the 13 Ag 13 Bu character in symmetry, and therefore, both of the triplet states can be 3 generated from the 11 B u state; and (2) the 1 Ag 3 and the 1 Bu states are energetically the T2 and T1 states, respectively. Thus, a most plausible assignment of the newly identified triplet state is the 13 Ag (T2 ) state. (ii) Singular-value decomposition and global fitting of the time-resolved spectra in the )2 to 50 ps time region. After trying several relaxation schemes (see Section 2), we have eventually reached to a branched relaxation scheme, including (1) the 1 1 1 11 Bþ u ! 1 Bu ! 2 Ag ! 1 Ag singlet internal con1 version and (2) the 1 Bu ! 13 Ag (T2 ) singlet-totriplet conversion followed by the 13 Ag (T2 ) ! 13 Bu (T1 ) triplet internal conversion. In order to build this branched relaxation scheme also, it was necessary to introduce the 13 Ag (T2 ) state based on the kinetic and energetical considerations: (1) in building such a scheme, a triplet state that is generated from the 11 B u state and
decays in 9–10 ps was necessary to be introduced. Such a triplet state can not be the 13 Bu (T1 ) state that decays in decamicroseconds [25,26]. (2) The energy of such a triplet state should be lower than, or equal to, the 11 B u states of all the set of carotenoids. Based on the 13 Bu energies determined for carotenoids with n ¼ 9–11 and extrapolated to those with n ¼ 12 and 13, the only triplet state that satisfies the above conditions is the 13 Ag (T2 ) state. Fig. 3 presents the SADS (the upper panels) and time-dependent changes in population (the lower panels) that have been obtained as the result of global fitting by the use of the above branched scheme for (a) neurosporene, (b) spheroidene, (c) lycopene, (d) anhydrorhodovibrin and (e) spirilloxanthin. SADS have extracted a set of clear 1 difference-spectrum patterns for the 11 Bþ u , 1 Bu , 1 3 2 Ag and 1 Ag (T2 ) states, which commonly appear in all the carotenoids, in the sequence of: (1) stimulated emission from the 11 Bþ u state consisting of a vibrational progression. (2) Transient absorption from the 11 B u state plus bleaching of the ground-state absorption. The maxima of this transient absorption are as follows: neurosporene (520 nm), spheroidene (536 nm), lycopene (555 nm), anhydrorhodovibrin (572 nm) and spirilloxanthin (601 nm). (3) Transient absorption from the 21 A g state plus bleaching of the ground-state absorption. The maxima of this particular transient absorption are: neurosporene (512 nm), spheroidene (529 nm), lycopene (557 nm), anhydrorhodovibrin (574 nm) and spirilloxanthin (603 nm). It is to be noted that, in comparison to the 1 21 A g transient absorption, the 1 Bu transient absorption is definitely shifted to the red in the case of neurosporene and spheroidene, but it is slightly shifted to the blue in the case of lycopene, anhydrorhodovibrin and spirilloxanthin (this may reflect the contribution of the 31 A g state; see Fig. 1). 1 Thus, the 11 B and 2 A transient absorptions are u g different from each other, both in the spectral profile and in the absorption maximum, for all the carotenoids examined. (4) Transient absorption from the 13 Ag (T2 ) state (as a direct product from the 11 B u state) and the bleaching of the groundstate absorption. The SADS of the last species is not presented for neurosporene, because it is not reliable at all due to the extremely low population
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Fig. 3. SADS (the upper panels) and time-dependent changes in population (the lower panels) for (a) neurosporene, (b) spheroidene, (c) lycopene, (d) anhydrorhodovibrin and (e) spirilloxanthin that have been obtained by the SVD and global-fitting analyses of the time-resolved data matrices by the use of a relaxation scheme shown in Fig. 4.
(see the lower panel). The last SADS of the other carotenoids are in general agreement with the difference spectra recorded after long delay times (Fig. 2, the central panels). Time-dependent changes in population proves that the sequence of events is basically the same among all the set of carotenoids: (1) the 11 Bþ u state rises and decays extremely fast. (2) When the 11 B u 3 state decays, both the 21 A g state and the 1 Ag (T2 ) state rise almost in parallel; later, the former decays faster than the latter. The time-dependent changes in population also shows that the relative population and the decay time scale of each state vary systematically depending on the conjugation length: When n increases, (10 ) the population of the 3 21 A g state is suppressed, whereas that of the 1 Ag 0 (T2 ) state is enhanced; and (2 ) the decay of the 1 1 11 Bþ u , 1 Bu and 2 Ag states becomes faster, although the decay of the 13 Ag (T2 ) state is almost the same. Fig. 4 shows the above-mentioned relaxation schemes for the set of carotenoids. The state energies are depicted proportional to the ordinate
1 1 scale: The energies of the 11 Bþ u , 1 Bu , 3 Ag and 1 2 Ag states are transferred from those in Fig. 1. The energies of the 13 Bu (T1 ) state were determined by emission spectroscopy of neurosporene, spheroidene and lycopene bound to the LH2 complexes (see Fig. 1); the 13 Bu (T1 ) energies of anhydrorhodovibrin and spirilloxanthin were estimated by extrapolation. The energy of each 13 Ag (T2 ) state was assumed to be twice of the energy of the 13 Bu (T1 ) state. This assumption may be too simple, but there are no experimental data available at this moment. (Much weaker electronic interactions in the triplet states, in comparison to those in the covalent singlet states, may justify this assumption.) The decay time constants for those electronic states, as determined by the SVD and global fitting analyses, are also shown: they vary systematically depending on the conjugation length. (1) 1 The time constants of the 11 B u ! 2 Ag and the 1 1 2 Ag ! 1 Ag singlet internal conversions decrease with n in accord with the decrease in the relevant energy gaps. (2) The time constants of the
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Fig. 4. Branched relaxation schemes for the set of carotenoids including the processes of internal conversion in the singlet and triplet manifolds as well as intramolecular singlet-to-triplet conversion, as determined by the SVD and global-fitting analyses. The relevant time constants are also shown. The state energies are transferred from Fig. 1; the 13 Bu energies of anhydrorhodovibrin and spirilloxanthin were extrapolated as a function of 1=ð2n þ 1Þ.
1 11 Bþ u ! 1 Bu internal conversion are an exception; those of neurosporene and spheroidene are practically the same, and those of lycopene, anhydrorhodovibrin and spirilloxanthin are very similar or even become smaller in this order. The results strongly suggest that, in carotenoids with n ¼ 11– 1 13, not the 11 Bþ u ! 3 Ag internal conversion but 1 1 the 3 Ag ! 1 Bu internal conversion plays a major role in determining the time constant of the ap1 parent Ô11 Bþ u ! 1 Bu Õ internal conversion. (3) The time constants of the 13 Ag (T2 ) ! 13 Bu (T1 ) internal conversion are practically the same for all the carotenoids due to the similar energy gaps. (4) Most importantly, the time constant of the singlet3 to-triplet (11 B u ! 1 Ag ) conversion decreases with n according to the energy gap between those states. It is as large as 20 ps in neurosporene, whereas it is less than 1 ps in spirilloxanthin. As a result, the partition to the triplet manifold is less than 3% in neurosporene, but it becomes more than 25% in spirilloxanthin (see Table 1). 3 It is to be noted that the rate of the 11 B u ! 1 Ag 1 1 singlet-to-triplet conversion (s in ps ) can be
approximately expressed as a function of the energy gap (DE in cm1 ) s1 ¼ 1:48 expðDE=1509Þ;
ð1Þ
as shown in Table 1 (in parenthesis). (One of the reviewers has pointed out that the energy-gap law should not be applied when the energy gap is much smaller than the phonon energy, 1509 cm1 . The applicability of the energy-gap law should be discussed when 13 Ag (T2 ) energies become available. Until then, Eq. (1) should be regarded just as an empirical equation based on the assumed 13 Ag energies.) 3.2. Time-resolved absorption spectroscopy in the decapicosecond to nanosecond time regime: identification of the 13 Ag ! 13 Bu triplet internal conversion Fig. 5 shows the time-resolved spectra of (a) lycopene (n ¼ 11) and (b) spirilloxanthin (n ¼ 13) in the 25 ps to 1 ns region; the spectra at 1.8 ls after triplet-sensitized excitation are
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Table 1 1 Dependence of the state energies, energy gaps, time constants and partitions, concerning the 11 B u ! 2 Ag internal conversion and the 3 1 3 11 B ! 1 A and 1 B ! 1 B internal conversion, on the length of conjugated chain g u u u Carotenoids (n)
Neurosporene (9)
Spheroidene (10)
Lycopene (11)
Anhydrorhodovibrin (12)
Spirilloxanthin (13)
19 800 15 300 (14 094) 7047
17 800 14 200 (13 764) 6882
16 000 13 300 (13 708) 6854
14 900 12 500 (13 512) 6756
13 600 11 900 (13 383) 6692
Energy gaps, DE (cm1 ) 1 4500 11 B u $ 2 Ag 3 11 B (5706) u $ 1 Ag 3 11 B 12 753 u $ 1 Bu
3600 (4036) 10 918
2700 (2292) 9146
2400 (1388) 8144
1700 (217) 6909
Time constants, s (ps) 1 0.56 11 B u ! 2 Ag 3 11 B ! 1 Ag 20 (29)a u 3 11 B (3019)a u !1 Bu
0.46 8.5 (9.7)a (901)a
0.38 3.6 (3.1)a (280)a
0.33 1.6 (1.7)a (145)a
0.28 0.78 (0.78)a (64)a
Partitions (%) 1 11 B u !2 Ag 3 11 B u !1 Ag 3 11 B u ! 1 Bu
94.86 5.09 (0.05)
90.27 9.60 (0.12)
82.92 16.90 (0.19)
73.00 25.67 (0.32)
State energies (cm1 ) 11 B u 21 A g 13 Ag 13 Bu
a
97.25 2.74 (0.02)
Estimated values are shown in a pair of parentheses. Calculated by the use of Eq. (1), i.e., s1 ¼ 1:48 expðDE=1509Þ.
Fig. 5. The raw time-resolved spectra, i.e., difference spectra of the triplet minus the ground state (the left panels), and the time-resolved absorption spectra of the triplet state obtained by subsidizing the bleaching of the ground-state absorption (the right panels), in 25 ps to 1 ns region, for (a) lycopene and (b) spirilloxanthin. The pair of the spectra (1.8 ls) shown in Fig. 2 (the bottom panels) is reproduced for comparison.
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also shown for comparison (the bottom spectra). We have chosen these two carotenoids as typical examples (because of the time necessary for data accumulation; see Section 2). In both carotenoids, the raw difference spectra (the left panels) clearly exhibit spectral changes from the 13 Ag (T2 ) to the 13 Bu (T1 ) state: (In the case of spirilloxanthin in n-hexane solution, no 13 Ag (T2 ) ! 13 Bu (T1 ) internal conversion was observed.) The initial 13 Ag (T2 ) spectra are in good agreement with those shown in the central panels of Fig. 2 (in lycopene, the contribution of the 21 A g transient absorption still remains) and those shown at the bottom of the upper panels of Fig. 3, whereas the final spectra 13 Bu (T1 ) are in good agreement with those shown in the bottom panels of Fig. 2. The time-resolved spectra of pure triplet species that were obtained by subsidizing the bleaching of the ground-state 11 Bþ 11 A u g absorption (the right panels) show that, in each carotenoid, the 13 Ag (T2 ) and the 13 Bu (T1 ) transient absorptions are practically the same in energy. The subsidized time-resolved spectra also show that the relative intensities of the vibrational progressions are completely different between the Tm T2 and Tn T1 transient absorption spectra, reflecting different Franck–Condon overlaps between the states relevant to the transitions. Most importantly, the time-resolved spectra evidence the internal conversion in the triplet manifold from 13 Ag (T2 ) to 13 Bu (T1 ). It seems that mainly the 13 Ag state is generated from the 11 B u state, although a small contribution of the latter state in the time-resolved spectra can not be excluded completely. In addition, based on our empirical equation, it can be shown that the amounts of the 13 Bu state generated must be very small: Table 1 lists the time constants and the 3 partitions of the direct 11 B u ! 1 Bu singlet-totriplet conversion reaction when Eq. (1) is applied. It turns out that, in each carotenoid, the time constant becomes very long, and the partition becomes negligibly small for the direct 3 11 B u !1 Bu (T1 ) conversion, when compared to 3 those for the 11 B u ! 1 Ag (T2 ) conversion that has been actually identified in the present investigation.
3.3. Implications of the results of the present investigation In the present investigation, a branched scheme 1 of relaxation, including the 11 Bþ u ! 1 Bu ! 1 21 A ! 1 A singlet internal conversion, the g g 3 11 B ! 1 A (T ) singlet to triplet conversion and g 2 u the 13 Ag (T2 ) ! 13 Bu (T1 ) triplet internal conversion, has been identified by the SVD and globalfitting analyses of visible time-resolved absorption data for neurosporene (n ¼ 9), spheroidene (n ¼ 10), lycopene (n ¼ 11), anhydrorhodovibrin (n ¼ 12) and spirilloxanthin (n ¼ 13) in solution. The relaxation scheme branching from the 11 B u state is first proposed, and the 13 Ag (T2 ) state has been identified for the first time. Thus, the following answers to the questions addressed in Section 1 have been obtained: (1) the S* state proposed by van Grondelle and co-workers [16,17] is most likely the 11 B u state that had already been identified in neurosporene [12]. (2) The 13 Ag (T2 ) state is generated directly from the 11 B u state. (3) The 13 Ag (T2 ) ! 13 Bu (T1 ) internal conversion does take place. The present results on carotenoids in solution confirm the intramolecular, singlet to triplet conversion reaction proposed for carotenoids bound to the antenna complexes [16,17]. However, our present relaxation scheme branching from the 11 B u state contradicts to their relaxation scheme branching from the 11 Bþ u state. Further investigation on carotenoids bound to antenna complexes is necessary to solve this contradiction.
Acknowledgements The authors would like to thank Prof. Hiroyoshi Nagae for reading the manuscript and for stimulating discussion. Contribution of Dr. JianPing Zhang and Mr. Tohru Inaba at an early stage of this investigation is acknowledged. This work has been supported by a grant from Ministry of Education, Science, Sport and Culture (Open Research Center Project) and a grant from NEDO (New Energy and Industrial Technology Development Organization, International Joint Research Grant).
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[15] R. Fujii, T. Inaba, Y. Watanabe, Y. Koyama, J.-P. Zhang, Chem. Phys. Lett. 369 (2003) 165. [16] C.C. Gradinaru, J.T.M. Kennis, E. Papagiannakis, I.H.M. van Stokkum, R.J. Cogdell, G.R. Fleming, R.A. Niederman, R. van Grondelle, Proc. Natl. Acad. Sci. USA 98 (2001) 2364. [17] E. Papagiannakis, J.T.M. Kennis, I.H.M. van Stokkum, R.J. Cogdell, R. van Grondelle, Proc. Natl. Acad. Sci. USA 99 (2002) 6017. [18] G. Cerullo, G. Lanzani, M. Zavelani-Rossi, S. De Silvestri, Phys. Rev. B 63 (2001) 241104. [19] G. Cerullo, D. Polli, G. Lanzani, S. De Silvestri, H. Hashimoto, R.J. Cogdell, Science 298 (2002) 2395. [20] H. Hashimoto, Y. Koyama, Chem. Phys. Lett. 162 (1989) 523. [21] H. Hashimoto, Y. Koyama, Y. Hirata, N. Mataga, J. Phys. Chem. 95 (1991) 3072. [22] J.-P. Zhang, R. Fujii, P. Qian, T. Inaba, T. Mizoguchi, Y. Koyama, K. Onaka, Y. Watanabe, H. Nagae, J. Phys. Chem. B 104 (2000) 3683. [23] M.R. Wasielewski, L.D. Kispert, Chem. Phys. Lett. 128 (1986) 238. [24] M.R. Wasielewski, D.G. Johnson, E.G. Bradford, L.D. Kispert, J. Chem. Phys. 91 (1989) 6691. [25] T.G. Monger, R.J. Cogdell, W.W. Parson, Biochem. Biophys. Acta 449 (1976) 136. [26] R. Fujii, K. Furuichi, J.-P. Zhang, H. Nagae, H. Hashimoto, Y. Koyama, J. Phys. Chem. A 106 (2002) 2410.
A first detection of singlet to triplet conversion 3 from the 11B u to the 1 Ag state and triplet internal conversion from the 13Ag to the 13Bu state in carotenoids: dependence on the conjugation length Ferdy S. Rondonuwu a, Yasutaka Watanabe a, Ritsuko Fujii b, Yasushi Koyama b,* a b
Department of Physics, Faculty of Science and Technology, Kwansei Gakuin University, 2-1 Gakuen, Sanda 669-1337, Japan Department of Chemistry, Faculty of Science and Technology, Kwansei Gakuin University, 2-1 Gakuen, Sanda 669-1337, Japan Received 22 January 2003; in final form 21 April 2003 Published online: 2 July 2003
Abstract Subpicosecond time-resolved absorption spectra were recorded in the visible region for a set of photosynthetic carotenoids having different numbers of conjugated double bonds (n), which include neurosporene (n ¼ 9), spheroidene (n ¼ 10), lycopene (n ¼ 11), anhydrorhodovibrin (n ¼ 12) and spirilloxanthin (n ¼ 13). Singular-value decomposition and global fitting of the spectral-data matrices lead us to a branched relaxation scheme including both (1) the singlet 1 1 1 internal conversion in the sequence of 11 Bþ u ! 1 Bu ! 2 Ag ! 1 Ag (ground), and (2) the singlet-to-triplet conversion 1 3 3 of 1 Bu ! 1 Ag followed by triplet internal conversion of 1 Ag ! 13 Bu . Ó 2003 Elsevier B.V. All rights reserved.
1. Introduction All-trans carotenoids are selectively bound to the antenna complexes mainly for the light-harvesting function [1–4]. Their conjugated chain has approximate C2h symmetry, which gives rise to the 1 1 þ 1 þ singlet states of k1 A g , l Bu , m Ag and n Bu type. (Here, Ô1Õ signifies the singlet states, + and ) are PariserÕs signs showing the symmetry of electronic
*
Corresponding author. Fax: +81-79-565-9077. E-mail address: [email protected] (Y. Koyama).
configurations [5,6], and k, l, m and n are the labeling of a series of electronic states having the same symmetry from the lower to the higher energy. Concerning optical transitions from the 1 þ 1 þ ground 11 A g state, the Ag and Bu states are classified into Ôoptically allowedÕ states, whereas 1 the 1 A g and Bu states to the Ôoptically forbiddenÕ states.) Tavan and Schulten [7,8] calculated the state energies of low-lying singlet states for shorter polyenes having the number of conjugated double bonds n ¼ 5–8, and exhibited their linear relations as functions of 1=ð2n þ 1Þ. The slopes of the linear relations were shown to be in the ratio 2:3.1:3.7 for
0009-2614/03/$ - see front matter Ó 2003 Elsevier B.V. All rights reserved. doi:10.1016/S0009-2614(03)00983-7
F.S. Rondonuwu et al. / Chemical Physics Letters 376 (2003) 292–301 1 1 the covalent 21 A g , 1 Bu and 3 Ag states, reflecting the momentum quantum number of 2, 3 and 4, respectively. Measurements of resonance-Raman excitation profiles (RREPs) for carotenoids with n ¼ 9–13 lead us to a first spectroscopic identification of 1 the 11 B u and 3 Ag states [9–11] in addition to the well-documented 11 Bþ and 21 A states [1–4] u g (shown in Fig. 1). The arrangement of the four singlet excited states was in good agreement with that obtained by extrapolation of the above linear
1 1 1 Fig. 1. An energy diagram for the 11 Bþ u , 3 Ag , 1 Bu and 2 Ag singlet states for crystalline mini-9-b-carotene (n ¼ 9), spheroidene (n ¼ 10), lycopene (n ¼ 11), anhydrorhodovibrin (n ¼ 12) and spirilloxanthin (n ¼ 13) determined by measurements of resonance-Raman excitation profiles [9–11] and for the 13 Bu (T1 ) state for neurosporene (n ¼ 9), spheroidene (n ¼ 10) and lycopene (n ¼ 11) bound to the LH2 complexes determined by emission spectroscopy (Rondonuwu et al., unpublished).
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1 relations; their slopes for the 21 A g , 1 Bu and 1 3 Ag states turned out to be in the ratio 2:3.1:3.8, establishing the state energies determined by RREPs. Visible [12] and near-infrared [13] subpicosecond time-resolved absorption spectroscopy as well as subpicosecond time-resolved Raman spectroscopy [14] identified internal conversion processes in neurosporene (n ¼ 9) that were in accord with the state ordering shown in the energy diagram, 1 1 1 i.e., 11 Bþ (see Fig. 1). u ! 1 Bu ! 2 Ag ! 1 Ag Further, near-infrared, subpicosecond time-resolved absorption spectroscopy for a series of carotenoids (n ¼ 9–13) [15] identified two different pathways of internal conversion that were also in accord with the energy diagram, i.e., 11 Bþ u ! 1 1 11 B ! 2 A !1 A for carotenoids with n ¼9 u g g 1 1 1 and 10, whereas 11 Bþ ! 3 A ! 2 A ! 1 A u g g g for carotenoids with n ¼ 11–13. Recently, van Grondelle and co-workers [16,17] have proposed an alternative pathway of relaxation, i.e., singlet-to-triplet conversion starting from an ÔS*Õ state. In the case of spirilloxanthin [16], it was reported that this state functioned as a precursor of the triplet state when bound to the LH1 complex from Rhodospirillum rubrum, whereas it directly relaxed to the ground state when free in solution. The S* ! T transformation in the antenna complex took only 12 ps. In the case of spheroidene bound to the LH2 complex from Rhodobacter sphaeroides also [17], the generation of the S* state and subsequent transformation into the triplet state was observed. Deep insight into the above results by the authors, taking into account the theoretical analysis of shorter polyenes by Tavan and Schulten [7,8], lead them to ascribe the above S* ! T reaction to a singlet-to-triplet conversion in the individual carotenoid molecule. The authors assessed that the S* state likely corresponds to the 11 B u state, although they excluded the possibility that the 1 þ 11 B u state is located in-between the 1 Bu and the 1 1 þ 1 2 Ag states, mediating the 1 Bu ! 2 Ag internal conversion [9,10]. Their interpretation was based on the 10-fs time-resolved absorption data then available [18]; now the presence of an intermediate state, i.e., Ôthe Sx state of 11 B u symmetryÕ, is proposed, instead [19].
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Since the generation of the 13 Bu (T1 ) state by direct photo-excitation of carotenoids was observed free in solution by picosecond Raman [20] and absorption [21] spectroscopies, and since the above singlet-to-triplet fission reaction was ascribed to an intramolecular reaction in nature [16,17], we started searching for this reaction in solution. We have addressed the following three specific questions: (1) what is the S* state? By definition it is a singlet state that facilitates carotenoidto-bacteriochlorophyll singlet-energy transfer [17], but its spectrum so far presented is somewhat similar to a triplet spectrum [16,17]. Is that really the 11 B u state that have been already identified in neurosporene [12]? If the answer is ÔyesÕ, then (2) what kind of triplet state(s), i.e., 13 Ag (T2 ) and/or 13 Bu (T1 ), can be directly generated from the 11 B u singlet state? Because of the symmetry relation, 3 3 11 B u ¼ 1 Ag 1 Bu , both triplet species can be generated in principle [8]. If the still unidentified 13 Ag (T2 ) state is found, then (3) does the internal conversion in the triplet manifold, i.e., 13 Ag (T2 ) ! 13 Bu (T1 ), actually take place to generate the well-documented 13 Bu (T1 ) state?
2. Experimental All-trans carotenoids (hereafter, Ôall-trans’ will be abbreviated throughout this Letter) were prepared as described previously [15]. In time-resolved absorption measurements, neurosporene and spheroidene were dissolved in n-hexane; lycopene and anhydrorhodovibrin were dissolved in a mixture of benzene and n-hexane (5:95 v/v); and spirilloxanthin was dissolved in a mixture of benzene and n-hexane (50:50 v/v). The concentration of each carotenoid solution was adjusted to OD ¼ 5 cm1 at the absorption maximum, corresponding to the concentrations of 3.1, 2.9, 2.7, 2.9 and 3.3 105 M for neurosporene, spheroidene, lycopene, anhydrorhodovibrin and spirilloxanthin, respectively. Each solution (30 ml) was circulated between a quartz flow cell (optical pathlength, 1 mm) and a reservoir that was cooled in ice-water. Each carotenoid was excited to the 11 Bþ u ðv ¼ 0) vibronic level at the following wavelength: neurosporene (467 nm), spheroidene (483 nm), lycopene
(501 nm), anhydrorhodovibrin (515 nm) and spirilloxanthin (536 nm). Subpicosecond time-resolved absorption spectra in the 400–700 nm region were recorded as described previously [22] except for the following modifications: a 1-cm water cell was used to generate the visible 400–700 nm Ôwhite continuumÕ for probing. The pumping energy was adjusted to 0.6 lJ/pulse at the sample cell corresponding to a photon density of 1.5 1014 photon cm2 . Each time-resolved spectrum in the )2 to 50 ps region was obtained by accumulating the data of 400 pulses, while that in the 25 ps to 1 ns region was obtained by accumulating the data of 50 400 pulses. The procedure of singular-value decomposition (SVD) and global fitting used for spectral analyses was basically the same as describe previously ([22] and references therein): analyzed were data matrices in the 400–700 nm spectral and the )2 to 50 ps delay-time regions, whose dimensions being 1105 275 for neurosporene, spheroidene and lycopene, and 1105 237 for anhydrorhodovibrin and spirilloxanthin. We have picked up the major four components that were obtained by SVD in order to accommodate the four different spectral patterns recognized in the raw time-resolved data. They were further analyzed by global fitting to obtain species-associated difference spectra (SADS) and time-dependent changes in population. In the global fitting, we eventually used a branched relaxation scheme, consisting of a sequential singlet 1 1 1 internal conversion (11 Bþ u ! 1 Bu ! 2 Ag ! 1 Ag ), and intramolecular singlet-to-triplet conversion 3 (11 B u ! 1 Ag ) followed by triplet internal conver3 sion (1 Ag ! 13 Bu ). Before reaching to this scheme, we have tried various relaxation schemes, including (i) sequential scheme with three (11 Bþ u ! 1 3 1 þ 1 11 B !2 A + 1 A !Þ and four (1 B ! 1 B g u g u u ! 3 21 A ! 1 A !Þ components, (ii) a scheme brang g ched from the 21 A g state with four components 1 1 3 (11 Bþ ! 1 B ! 2 Ag ! plus 21 A u u g ! 1 Ag !Þ, 1 and (iii) a scheme branching from 1 Bu and re1 þ turning to 21 A g with four components (1 Bu ! 1 1 1 3 1 1 Bu ! 2 Ag ! plus 1 Bu ! 1 Ag ! 2 Ag ). Those unsuccessful models caused strong mixing among SADS and/or negative population for some component(s).
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3. Results and discussion 3.1. Time-resolved absorption spectroscopy in the subpicosecond to decapicosecond time regime: identification of a relaxation scheme branching from the 11 B u state (i) Characterization of the time-resolved spectra. Fig. 2 (the top panels) shows time-resolved spectra in the 0–15 ps region for a set of carotenoids, including (a) neurosporene (n ¼ 9), (b) spheroidene (n ¼ 10), (c) lycopene (n ¼ 11), (d) anhydrorhodovibrin (n ¼ 12) and (e) spirilloxanthin (n ¼ 13). Time-dependent spectral changes are similar to one another among all the carotenoids, and the sequence can be characterized as follows based on the results of neurosporene in n-hexane [12]: first,
295
stimulated emission from the optically allowed 11 Bþ u state appears with vibrational progression. Second, a broad transient absorption from the optically forbidden 11 B u state extending to the red appears together with the bleaching of the groundstate 11 Bþ 11 A u g absorption (shown on the top of each set of time-resolved spectra). Third, sharp transient absorption from the 21 A g state, which has been well-documented [21,23,24], appears accompanying the bleaching of the ground-state absorption. Almost in parallel, an indication of triplet absorption appears as a shoulder on the blue side of the 21 A g transient absorption. A set of time-resolved spectra after long delay times (the central panels) clearly exhibit the differencespectrum pattern due to a triplet state; at those delay times, the contribution of the 21 A g transient
Fig. 2. Subpicosecond, time-resolved absorption spectra in the 0–15 ps region (the top panels) for (a) neurosporene and (b) spheroidene, (c) lycopene, (d) anhydrorhodovibrin and (e) spirilloxanthin. The ground-state 11 Bþ 11 A u g absorption spectra are shown on the top of each set of time-resolved spectra. The time-resolved spectra of the 13 Ag (T2 ) state obtained by direct photo-excitation after long delay times (the central panels) and those of the 13 Bu (T1 ) state obtained at 1.8 ls after triplet-sensitized excitation (the bottom panels) are also shown for comparison.
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absorption becomes minimum (in neurosporene and spheroidene) or negligible (in lycopene, anhydrorhodovibrin and spirilloxanthin). The parallel rise of the 21 A g -state and the triplet-state absorptions suggests that the particular triplet state is generated not from the 21 A g state but from the 11 B u state. The time scales of the above sequential changes vary systematically depending on the length of the conjugated chain: When n increases, the 11 Bþ u stimulated emission decays faster, the 11 B and 21 A u g transient absorptions rise and decay more rapidly, and the triplet absorption becomes clearer. Fig. 2 (the bottom panels) also exhibits the transient absorption spectra of the lowest triplet state, i.e., the 13 Bu (T1 ) state, that were recorded at 1.8 ls after excitation of the sensitizer, anthracene. The difference-spectrum patterns of the T1 state for those photosynthetic carotenoids have been well documented (see [25,26] for example). Importantly, the difference-spectrum patterns of the above triplet state generated by direct photo-excitation (the central panels) are completely different from those of the 13 Bu (T1 ) state that was generated by sensitized photo-excitation (the bottom panels). Tavan and Schulten [8] showed, based on theoretical considerations, (1) the 11 B u state has the 13 Ag 13 Bu character in symmetry, and therefore, both of the triplet states can be 3 generated from the 11 B u state; and (2) the 1 Ag 3 and the 1 Bu states are energetically the T2 and T1 states, respectively. Thus, a most plausible assignment of the newly identified triplet state is the 13 Ag (T2 ) state. (ii) Singular-value decomposition and global fitting of the time-resolved spectra in the )2 to 50 ps time region. After trying several relaxation schemes (see Section 2), we have eventually reached to a branched relaxation scheme, including (1) the 1 1 1 11 Bþ u ! 1 Bu ! 2 Ag ! 1 Ag singlet internal con1 version and (2) the 1 Bu ! 13 Ag (T2 ) singlet-totriplet conversion followed by the 13 Ag (T2 ) ! 13 Bu (T1 ) triplet internal conversion. In order to build this branched relaxation scheme also, it was necessary to introduce the 13 Ag (T2 ) state based on the kinetic and energetical considerations: (1) in building such a scheme, a triplet state that is generated from the 11 B u state and
decays in 9–10 ps was necessary to be introduced. Such a triplet state can not be the 13 Bu (T1 ) state that decays in decamicroseconds [25,26]. (2) The energy of such a triplet state should be lower than, or equal to, the 11 B u states of all the set of carotenoids. Based on the 13 Bu energies determined for carotenoids with n ¼ 9–11 and extrapolated to those with n ¼ 12 and 13, the only triplet state that satisfies the above conditions is the 13 Ag (T2 ) state. Fig. 3 presents the SADS (the upper panels) and time-dependent changes in population (the lower panels) that have been obtained as the result of global fitting by the use of the above branched scheme for (a) neurosporene, (b) spheroidene, (c) lycopene, (d) anhydrorhodovibrin and (e) spirilloxanthin. SADS have extracted a set of clear 1 difference-spectrum patterns for the 11 Bþ u , 1 Bu , 1 3 2 Ag and 1 Ag (T2 ) states, which commonly appear in all the carotenoids, in the sequence of: (1) stimulated emission from the 11 Bþ u state consisting of a vibrational progression. (2) Transient absorption from the 11 B u state plus bleaching of the ground-state absorption. The maxima of this transient absorption are as follows: neurosporene (520 nm), spheroidene (536 nm), lycopene (555 nm), anhydrorhodovibrin (572 nm) and spirilloxanthin (601 nm). (3) Transient absorption from the 21 A g state plus bleaching of the ground-state absorption. The maxima of this particular transient absorption are: neurosporene (512 nm), spheroidene (529 nm), lycopene (557 nm), anhydrorhodovibrin (574 nm) and spirilloxanthin (603 nm). It is to be noted that, in comparison to the 1 21 A g transient absorption, the 1 Bu transient absorption is definitely shifted to the red in the case of neurosporene and spheroidene, but it is slightly shifted to the blue in the case of lycopene, anhydrorhodovibrin and spirilloxanthin (this may reflect the contribution of the 31 A g state; see Fig. 1). 1 Thus, the 11 B and 2 A transient absorptions are u g different from each other, both in the spectral profile and in the absorption maximum, for all the carotenoids examined. (4) Transient absorption from the 13 Ag (T2 ) state (as a direct product from the 11 B u state) and the bleaching of the groundstate absorption. The SADS of the last species is not presented for neurosporene, because it is not reliable at all due to the extremely low population
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Fig. 3. SADS (the upper panels) and time-dependent changes in population (the lower panels) for (a) neurosporene, (b) spheroidene, (c) lycopene, (d) anhydrorhodovibrin and (e) spirilloxanthin that have been obtained by the SVD and global-fitting analyses of the time-resolved data matrices by the use of a relaxation scheme shown in Fig. 4.
(see the lower panel). The last SADS of the other carotenoids are in general agreement with the difference spectra recorded after long delay times (Fig. 2, the central panels). Time-dependent changes in population proves that the sequence of events is basically the same among all the set of carotenoids: (1) the 11 Bþ u state rises and decays extremely fast. (2) When the 11 B u 3 state decays, both the 21 A g state and the 1 Ag (T2 ) state rise almost in parallel; later, the former decays faster than the latter. The time-dependent changes in population also shows that the relative population and the decay time scale of each state vary systematically depending on the conjugation length: When n increases, (10 ) the population of the 3 21 A g state is suppressed, whereas that of the 1 Ag 0 (T2 ) state is enhanced; and (2 ) the decay of the 1 1 11 Bþ u , 1 Bu and 2 Ag states becomes faster, although the decay of the 13 Ag (T2 ) state is almost the same. Fig. 4 shows the above-mentioned relaxation schemes for the set of carotenoids. The state energies are depicted proportional to the ordinate
1 1 scale: The energies of the 11 Bþ u , 1 Bu , 3 Ag and 1 2 Ag states are transferred from those in Fig. 1. The energies of the 13 Bu (T1 ) state were determined by emission spectroscopy of neurosporene, spheroidene and lycopene bound to the LH2 complexes (see Fig. 1); the 13 Bu (T1 ) energies of anhydrorhodovibrin and spirilloxanthin were estimated by extrapolation. The energy of each 13 Ag (T2 ) state was assumed to be twice of the energy of the 13 Bu (T1 ) state. This assumption may be too simple, but there are no experimental data available at this moment. (Much weaker electronic interactions in the triplet states, in comparison to those in the covalent singlet states, may justify this assumption.) The decay time constants for those electronic states, as determined by the SVD and global fitting analyses, are also shown: they vary systematically depending on the conjugation length. (1) 1 The time constants of the 11 B u ! 2 Ag and the 1 1 2 Ag ! 1 Ag singlet internal conversions decrease with n in accord with the decrease in the relevant energy gaps. (2) The time constants of the
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Fig. 4. Branched relaxation schemes for the set of carotenoids including the processes of internal conversion in the singlet and triplet manifolds as well as intramolecular singlet-to-triplet conversion, as determined by the SVD and global-fitting analyses. The relevant time constants are also shown. The state energies are transferred from Fig. 1; the 13 Bu energies of anhydrorhodovibrin and spirilloxanthin were extrapolated as a function of 1=ð2n þ 1Þ.
1 11 Bþ u ! 1 Bu internal conversion are an exception; those of neurosporene and spheroidene are practically the same, and those of lycopene, anhydrorhodovibrin and spirilloxanthin are very similar or even become smaller in this order. The results strongly suggest that, in carotenoids with n ¼ 11– 1 13, not the 11 Bþ u ! 3 Ag internal conversion but 1 1 the 3 Ag ! 1 Bu internal conversion plays a major role in determining the time constant of the ap1 parent Ô11 Bþ u ! 1 Bu Õ internal conversion. (3) The time constants of the 13 Ag (T2 ) ! 13 Bu (T1 ) internal conversion are practically the same for all the carotenoids due to the similar energy gaps. (4) Most importantly, the time constant of the singlet3 to-triplet (11 B u ! 1 Ag ) conversion decreases with n according to the energy gap between those states. It is as large as 20 ps in neurosporene, whereas it is less than 1 ps in spirilloxanthin. As a result, the partition to the triplet manifold is less than 3% in neurosporene, but it becomes more than 25% in spirilloxanthin (see Table 1). 3 It is to be noted that the rate of the 11 B u ! 1 Ag 1 1 singlet-to-triplet conversion (s in ps ) can be
approximately expressed as a function of the energy gap (DE in cm1 ) s1 ¼ 1:48 expðDE=1509Þ;
ð1Þ
as shown in Table 1 (in parenthesis). (One of the reviewers has pointed out that the energy-gap law should not be applied when the energy gap is much smaller than the phonon energy, 1509 cm1 . The applicability of the energy-gap law should be discussed when 13 Ag (T2 ) energies become available. Until then, Eq. (1) should be regarded just as an empirical equation based on the assumed 13 Ag energies.) 3.2. Time-resolved absorption spectroscopy in the decapicosecond to nanosecond time regime: identification of the 13 Ag ! 13 Bu triplet internal conversion Fig. 5 shows the time-resolved spectra of (a) lycopene (n ¼ 11) and (b) spirilloxanthin (n ¼ 13) in the 25 ps to 1 ns region; the spectra at 1.8 ls after triplet-sensitized excitation are
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Table 1 1 Dependence of the state energies, energy gaps, time constants and partitions, concerning the 11 B u ! 2 Ag internal conversion and the 3 1 3 11 B ! 1 A and 1 B ! 1 B internal conversion, on the length of conjugated chain g u u u Carotenoids (n)
Neurosporene (9)
Spheroidene (10)
Lycopene (11)
Anhydrorhodovibrin (12)
Spirilloxanthin (13)
19 800 15 300 (14 094) 7047
17 800 14 200 (13 764) 6882
16 000 13 300 (13 708) 6854
14 900 12 500 (13 512) 6756
13 600 11 900 (13 383) 6692
Energy gaps, DE (cm1 ) 1 4500 11 B u $ 2 Ag 3 11 B (5706) u $ 1 Ag 3 11 B 12 753 u $ 1 Bu
3600 (4036) 10 918
2700 (2292) 9146
2400 (1388) 8144
1700 (217) 6909
Time constants, s (ps) 1 0.56 11 B u ! 2 Ag 3 11 B ! 1 Ag 20 (29)a u 3 11 B (3019)a u !1 Bu
0.46 8.5 (9.7)a (901)a
0.38 3.6 (3.1)a (280)a
0.33 1.6 (1.7)a (145)a
0.28 0.78 (0.78)a (64)a
Partitions (%) 1 11 B u !2 Ag 3 11 B u !1 Ag 3 11 B u ! 1 Bu
94.86 5.09 (0.05)
90.27 9.60 (0.12)
82.92 16.90 (0.19)
73.00 25.67 (0.32)
State energies (cm1 ) 11 B u 21 A g 13 Ag 13 Bu
a
97.25 2.74 (0.02)
Estimated values are shown in a pair of parentheses. Calculated by the use of Eq. (1), i.e., s1 ¼ 1:48 expðDE=1509Þ.
Fig. 5. The raw time-resolved spectra, i.e., difference spectra of the triplet minus the ground state (the left panels), and the time-resolved absorption spectra of the triplet state obtained by subsidizing the bleaching of the ground-state absorption (the right panels), in 25 ps to 1 ns region, for (a) lycopene and (b) spirilloxanthin. The pair of the spectra (1.8 ls) shown in Fig. 2 (the bottom panels) is reproduced for comparison.
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also shown for comparison (the bottom spectra). We have chosen these two carotenoids as typical examples (because of the time necessary for data accumulation; see Section 2). In both carotenoids, the raw difference spectra (the left panels) clearly exhibit spectral changes from the 13 Ag (T2 ) to the 13 Bu (T1 ) state: (In the case of spirilloxanthin in n-hexane solution, no 13 Ag (T2 ) ! 13 Bu (T1 ) internal conversion was observed.) The initial 13 Ag (T2 ) spectra are in good agreement with those shown in the central panels of Fig. 2 (in lycopene, the contribution of the 21 A g transient absorption still remains) and those shown at the bottom of the upper panels of Fig. 3, whereas the final spectra 13 Bu (T1 ) are in good agreement with those shown in the bottom panels of Fig. 2. The time-resolved spectra of pure triplet species that were obtained by subsidizing the bleaching of the ground-state 11 Bþ 11 A u g absorption (the right panels) show that, in each carotenoid, the 13 Ag (T2 ) and the 13 Bu (T1 ) transient absorptions are practically the same in energy. The subsidized time-resolved spectra also show that the relative intensities of the vibrational progressions are completely different between the Tm T2 and Tn T1 transient absorption spectra, reflecting different Franck–Condon overlaps between the states relevant to the transitions. Most importantly, the time-resolved spectra evidence the internal conversion in the triplet manifold from 13 Ag (T2 ) to 13 Bu (T1 ). It seems that mainly the 13 Ag state is generated from the 11 B u state, although a small contribution of the latter state in the time-resolved spectra can not be excluded completely. In addition, based on our empirical equation, it can be shown that the amounts of the 13 Bu state generated must be very small: Table 1 lists the time constants and the 3 partitions of the direct 11 B u ! 1 Bu singlet-totriplet conversion reaction when Eq. (1) is applied. It turns out that, in each carotenoid, the time constant becomes very long, and the partition becomes negligibly small for the direct 3 11 B u !1 Bu (T1 ) conversion, when compared to 3 those for the 11 B u ! 1 Ag (T2 ) conversion that has been actually identified in the present investigation.
3.3. Implications of the results of the present investigation In the present investigation, a branched scheme 1 of relaxation, including the 11 Bþ u ! 1 Bu ! 1 21 A ! 1 A singlet internal conversion, the g g 3 11 B ! 1 A (T ) singlet to triplet conversion and g 2 u the 13 Ag (T2 ) ! 13 Bu (T1 ) triplet internal conversion, has been identified by the SVD and globalfitting analyses of visible time-resolved absorption data for neurosporene (n ¼ 9), spheroidene (n ¼ 10), lycopene (n ¼ 11), anhydrorhodovibrin (n ¼ 12) and spirilloxanthin (n ¼ 13) in solution. The relaxation scheme branching from the 11 B u state is first proposed, and the 13 Ag (T2 ) state has been identified for the first time. Thus, the following answers to the questions addressed in Section 1 have been obtained: (1) the S* state proposed by van Grondelle and co-workers [16,17] is most likely the 11 B u state that had already been identified in neurosporene [12]. (2) The 13 Ag (T2 ) state is generated directly from the 11 B u state. (3) The 13 Ag (T2 ) ! 13 Bu (T1 ) internal conversion does take place. The present results on carotenoids in solution confirm the intramolecular, singlet to triplet conversion reaction proposed for carotenoids bound to the antenna complexes [16,17]. However, our present relaxation scheme branching from the 11 B u state contradicts to their relaxation scheme branching from the 11 Bþ u state. Further investigation on carotenoids bound to antenna complexes is necessary to solve this contradiction.
Acknowledgements The authors would like to thank Prof. Hiroyoshi Nagae for reading the manuscript and for stimulating discussion. Contribution of Dr. JianPing Zhang and Mr. Tohru Inaba at an early stage of this investigation is acknowledged. This work has been supported by a grant from Ministry of Education, Science, Sport and Culture (Open Research Center Project) and a grant from NEDO (New Energy and Industrial Technology Development Organization, International Joint Research Grant).
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