Ultrafast Dynamics of Long Homologues of Carotenoid Zeaxanthin

Article pubs.acs.org/JPCA

Ultrafast Dynamics of Long Homologues of Carotenoid Zeaxanthin Hristina Staleva,† Muhammad Zeeshan,‡ Pavel Chábera,§ Vassilia Partali,‡ Hans-Richard Sliwka,‡ and Tomás ̌ Polívka*,† Institute of Physics and Biophysics, Faculty of Science, University of South Bohemia, Branišovská 1760, 37005 Č eské Budějovice, Czech Republic ‡ Department of Chemistry, Norwegian University of Science and Technology, 7491 Trondheim, Norway § Department of Chemical Physics, Lund University, SE-221 00 Lund, Sweden †

S Supporting Information *

ABSTRACT: Three zeaxanthin homologues with conjugation lengths N of 15, 19, and 23 denoted as Z15, Z19, and Z23 were studied by femtosecond transient absorption spectroscopy, and the results were compared to those obtained for zeaxanthin (Z11). The energies of S2 decrease from 20 450 cm−1 (Z11) to 18 280 cm−1 (Z15), 17 095 cm−1 (Z19), and 16 560 cm−1 (Z23). Fitting the N dependence of the S2 energies allowed the estimation of E∞, the S2 energy of a hypothetical infinite zeaxanthin, to be ∼14 000 cm−1. Exciting the 0−0 band of the S2 state produces characteristic S1−Sn spectral profiles in transient absorption spectra with maxima at 556 nm (Z11), 630 nm (Z15), 690 nm (Z19), and 740 nm (Z23). The red shift of the S1−Sn transition with increasing conjugation length is caused by a decrease in the S1 state energy, resulting in S1 lifetimes of 9 ps (Z11), 0.9 ps (Z15), 0.35 ps (Z19), and 0.19 ps (Z23). Essentially the same lifetimes were obtained after excess energy excitation at 400 nm, but S1−Sn becomes broader, indicating a larger conformation disorder in the S1 state after 400 nm excitation compared to excitation into the 0−0 band of the S2 state. An S* signal was observed in all samples, but only for Z15, Z19, and Z23 does the S* signal decay with a lifetime different from that of the S1 state. The S* lifetimes are 2.9 and 1.6 ps for Z15 and Z19, respectively. In Z23 the S* signal needs two decay components yielding lifetimes of 0.24 and 2.3 ps. The S* signal is more pronounced after 400 nm excitation. assigns carotenoids to the C2h symmetry group.7 The S2 state is of Bu+ symmetry, allowing the S0−S2 transition, which results in a pronounced absorption band of carotenoids in the 400−550 nm region.8 Contrary to other conjugated π-electron systems, excited carotenoids are able to deactivate very quickly back to the ground state. The excited S2 state relaxes to the S1 state via internal conversion within a few hundred femtoseconds; the S1 state subsequently decays to the ground state on the picosecond time scale.8 Energies and lifetimes of carotenoid excited states depend on the number of conjugated CC bonds, N. With increasing N, the energies of the S2 and S1 states and the S1 lifetime decrease. The N dependence of the S2 lifetime is more intricate9 and is

1. INTRODUCTION Carotenoids are ubiquitous natural pigments found in essentially all living organisms. While in most organisms they function as efficient radical scavengers and colorants,1,2 in photosynthesis they are also crucial light-harvesting and photoprotective agents.3−5 Thus, the functioning of carotenoids in photosynthetic systems is inextricably related to their spectroscopic properties that have been the subject of numerous studies during the past two decades. Carotenoids exhibit almost no emission, which was explained by the presence of a low-lying excited state forbidden for one-photon transitions from the ground state.6 In a first approximation, the energy-level scheme of carotenoids is described by a three-level system consisting of the ground state (S0), the low-lying forbidden state (S1), and a strongly absorbing state (S2). The S0−S1 transition is forbidden since these states have the same symmetry (Ag−), a fact based on molecular structure that © 2015 American Chemical Society

Received: August 31, 2015 Revised: October 24, 2015 Published: October 26, 2015 11304

DOI: 10.1021/acs.jpca.5b08460 J. Phys. Chem. A 2015, 119, 11304−11312

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The Journal of Physical Chemistry A

the S* signal to a hot ground state. Later, numerous studies argued that the S* signal is associated with a conformational change in the carotenoid,17,26−29 yet the question of whether the S* signal has its origin in an excited state or in a hot ground state of a carotenoid remains unanswered. Experimental data on carotenoids dissolved in organic solvents show that the S* signal in various carotenoids can be consistently interpreted either as an excited state26−35 or as a hot ground state.36−38 Since the S* state in carotenoids bound to light-harvesting proteins was identified as a donor state in energy transfer to BChl,39,40 it must be an excited state in light-harvesting complexes. It was even hypothesized that the S* signal in isolated and protein-bound carotenoids has different origins.36 Thus, spectroscopic studies of long carotenoids promise to resolve important questions of carotenoid photophysics. However, detailed spectroscopic studies of carotenoids or polyenes having N > 13 are only scarcely reported.16,19 Carotenoids are synthesized via the Wittig reactions,41 but the stability of the elongated carotenoids decreases upon increasing the polyene chain length.42 Recently, Zeeshan et al. employing microwave-assisted Wittig reactions synthesized stable zeaxanthin homologues with conjugation lengths of up to N = 27,43 i.e., more than twice as long as normal zeaxanthin (N = 11). Here we compare ultrafast transient absorption data recorded for zeaxanthin (Z11) and three homologues with N = 15, 19, and 23 denoted as Z15, Z19, and Z23 (Figure 1).

most likely governed by the presence of dark states that exist within the S2−S1 energy gap.10,11 For linear carotenoids, going from N = 9 to N = 13 results in a shift of the S2 energy from 21 300 to 19 000 cm−1, the S1 energy decreases from ∼15 000 to 11 500 cm−1, and the S1 lifetime shortens from 23 to 1.3 ps.8 Most naturally occurring carotenoids are capped by various terminal cyclohexene rings. The ring double bond is not in full conjugation with the polyene chain due to steric deviations.12,13 To characterize the conjugation length of these carotenoids, a concept of effective conjugation, Neff, is often used. Systematic analysis of the behavior of linear conjugated carotenoids and polyenes led to the empirical observation that the S1 lifetime, the S2 energy, and the Raman frequency of the CC stretch in the ground state have a well-defined dependence on 1/N.13−16 Thus, knowing the value of one of these parameters for any carotenoid and comparing the value to that of a linear carotenoid allows us to obtain an effective value of Neff.13,15,17,18 In nature, only carotenoids with Neff ≤ 13 have so far been detected. Yet, it is desirable to study longer carotenoids and polyenes in order to obtain spectroscopic data and to examine the validity of theoretical models in the long conjugation limit.18 Studies of carotenoids with identical structure but different conjugation length demonstrated the usefulness of this approach. Experiments on elongated β-carotene,9,19 spheroidene,20 peridinin,21,22 and fucoxanthin23 homologues have provided a wealth of information about their N dependence of spectroscopic properties. Except for β-carotene, however, these studies were limited to Neff in the 7−13 range.20−23 A pioneering study of long β-carotene homologues by Andersson and Gillbro19 showed that the S1 lifetime decreases to 0.85 ps (N = 15) and even to 0.45 ps for the homologue with N = 19. Extrapolation of the measured S2 and S1 energies yielded values of 11 000 and 3500 cm−1, respectively, for a hypothetical infinite carotenoid. While Andersson et al. reported the extrapolated values from S2 and S1 energies obtained from measurements at 77 K,19 essentially the same values, 10 955 and 3800 cm−1, were obtained from fitting the roomtemperature data reported for a larger set of spheroidene analogs that covered conjugation lengths in the 7−13 range.20 Similar studies were also reported for polyenes with a broad range of N = 3−23,16,24 placing the N → ∞ limit for the S2 and S1 energies at 15 900 and ∼10 000 cm−1, respectively. Only polyenes with N ≤ 19 were studied by ultrafast transient absorption spectroscopy, confirming the S1 lifetime of ∼0.5 ps for the polyene with N = 19.16 Another interesting spectroscopic feature of carotenoids and polyenes with a long conjugation length is the presence of signals that appear in transient absorption spectra even after the S1 state has decayed. The S1 state is readily identified in transient absorption spectra via the S1−Sn excited absorption band peaking in the 500−600 nm spectral region, and it decays with the S1 lifetime.8 As first noted by Andersson and Gillbro19 for long β-carotene homologues, the S1−Sn band has a highenergy shoulder that has a lifetime of a few picoseconds, in contrast to the S1 lifetimes of 0.85 and 0.45 ps for N = 15 and 19. They assigned the origin of this signal to a hot ground state. This signal, now commonly referred to as the S* signal or the S* state, has been reported for a number of carotenoids with Neff > 11, and its origin remains a matter of considerable debate.10 In 2001, Gradinaru et al. reported the formation of a triplet state from the S* state in the linear carotenoid spirilloxanthin (N = 13) bound to the LH1 antenna complex from purple bacteria,25 challenging the original assignment of

Figure 1. Molecular structures of zeaxanthin and its homologues.

Extending ultrafast studies of carotenoids or polyenes to N = 23 allows the identification of subpicosecond S1 lifetimes and the assignment of the origin of pronounced S* signals.

2. MATERIALS AND METHODS 2.1. Sample Preparation. Zeaxanthin homologues Z15, Z19, and Z23 were synthesized as described in Zeeshan et al.43 Zeaxanthin Z11 was purchased from Sigma and repurified by HPLC. All samples were stored in the dark at −80 °C. Prior to experiments, each sample was dissolved in spectroscopic-grade tetrahydrofuran (THF) to yield an optical density of 0.2−0.4/ mm at the absorption maximum. 2.2. Spectroscopy. All spectroscopic studies were performed at room temperature. Steady-state absorption spectra were recorded on a PerkinElmer Lambda 35 absorption spectrometer. Transient absorption measurements were carried out in a standard pump probe configuration described in detail elsewhere.17 The pump pulse was generated in an optical parametric amplifier (Topas, Light Conversion) pumped by an amplified femtosecond laser system (Spectra-Physics) with a pulse repetition rate of 1 kHz. The probe pulse was produced by white light generation in a 2 mm sapphire plate. Prior to its arrival at the sample, the probe beam was split into two 11305


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The Journal of Physical Chemistry A identical beams. The first beam was overlapped at the sample with the pump beam and served as a probe, and the second beam was sent straight to the detection system and was used as a reference. The sample was placed in a 1 mm custom-built rotational cuvette and rotated during data collection to ensure that each pulse probes a fresh volume of the sample. Steadystate absorption spectra were collected before and after each transient absorption measurement to check for light-induced sample degradation. The time-resolved data were fitted globally (DAfit, Pascher Instruments) to a sum of exponentials using a sequential model with increasing lifetimes.

resolution of vibrational bands of the zeaxanthin homologues decreases with increasing N, which is opposite to that reported for apocarotenes with N = 5−11.12 However, for very long conjugated systems the conjugated chain takes an S shape43 which increases conformational disorder, leading to the observed decrease in resolution of vibrational bands when going from Z11 to Z23. The lowest-energy feature is readily assigned to the 0−0 band of the S0−S2 transition, and it is obvious that the S2 energy exhibits a strong N dependence. The position of the 0−0 band of the S0−S2 transition shifts from 489 nm (20 450 cm−1) for Z11 to 547 nm (18 280 cm−1, Z15), 585 nm (17 095 cm−1, Z19), and 604 nm (16 560 cm−1, Z23). While the Z11 absorption spectrum does not show any other spectral bands except the S0−S2 transition in the 300−700 nm spectral region, the absorption spectra of longer homologues contain multiple higher-energy bands. The band with the highest energy is associated with a transition to the 21Bu+ state (marked by a cross in Figure 2). For Z11, this transition has even higher energy and is found in the 220−280 nm region.44 The other band is due to a transition to the 11Ag+ state (marked by an asterisk in Figure 2), which is usually denoted as a cis peak.45 Since it was demonstrated that samples of long zeaxanthin homologues are dominated by the all-trans configuration,43 the presence of a cis peak in Z15, Z19, and Z23 likely reflects the higher flexibility of the long homologues compared to Z11, which does not show evidence of a cis peak (Figure 2). The increased flexibility of the conjugated backbone can make the cis peak partially allowed. This assumption is also supported by the increased intensity of the cis peak with increasing N. The cis peak of Z23 significantly overlaps with the S0−S2 band, suggesting a narrowing of the Bu+−Ag+ gap with increasing N. The energies of the various bands in the absorption spectra are summarized in Table 1. Figure 3 summarizes the transient absorption data recorded after excitation of the 0−0 band of the S0−S2 transition of zeaxanthin homologues dissolved in THF. Transient absorption spectra corresponding to the S1−Sn transition of all four samples are shown in Figure 3a. A red shift of the S1−Sn maximum with increasing N is obvious as the maximum shifts from 556 nm (Z11) to 630 nm (Z15), 690 nm (Z19), and further to 740 nm for the longest homologue Z23. The shoulder on the short-wavelength side of the S1−Sn maximum, which is usually assigned to the S* signal,10 becomes significantly more pronounced with increasing conjugation length. Kinetics measured at the maximum in the S1−Sn and S* bands are shown in Figure 3b,c. The S1 lifetimes decrease with increasing N, yielding 9 ps (Z11), 0.9 ps (Z15), 0.35 ps (Z19), and 0.19 ps (Z23), confirming the subpicosecond S1 lifetimes for N = 15 previously observed for β-carotene homologues9,19

3. RESULTS Absorption spectra of the four carotenoids in THF are shown in Figure 2. The spectra are dominated by the S0−S2 transition,

Figure 2. Steady-state absorption spectra of zeaxanthin Z11 and its homologues Z15, Z19, and Z23. Excitation wavelengths for the timeresolved studies are indicated by arrows. Solid arrows denote the excitation wavelength used to excite the (0−0) transition at 488 nm (Zea), 545 nm (Z15), 584 nm (Z19), and 604 nm (Z23). Dashed arrows indicate excitation in the UV region at 400 nm (Z15 and Z23) and at 375 nm (Z19). The spectral band associated with the cis peak is denoted by an asterisk, and the second allowed transition to a Bu+ state is marked with a cross for each zeaxanthin homologue. All spectra are normalized to the maximum.

which exhibits typical vibronic structure with three wellresolved vibrational bands due to the combination of the CC and C−C stretching modes of the carotenoid backbone.8 The

Table 1. Energies and Wavelengths of Various Transitions and S1 and S* Lifetimes of Zeaxanthin Homologs in THF molecule

S0−S2 (0−0) (cm−1, nm)

S1−Sn (max) (cm−1, nm)

S* (cm−1, nm)

1Ag+ (cis peak) (cm−1, nm)

2Bu+ (cm−1, nm)

Z11

20 550 487 18 350 545 17 250 580 16 800 595

18 000 556 15 850 631 14 500 690 13 500 740

19 230 520 17 240 580 16 000 625 15 620 640

29 850a 335 24 800 403 22 320 448 20 880 479

35 700b 280 30 000 333 26 660 375 24 570 407

Z15 Z19 Z23

a

τS1 (ps)

τS* (ps)

9

9

0.9

2.9

0.35

1.6

0.19

0.24c 2.3

From ref 45. bFrom ref 44. cFor Z23, the S* decay is multiexponential, and two components are necessary to fit the data. 11306


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Figure 3. (a) Transient absorption spectra of zeaxanthin homologues in THF measured at delay times of 1 ps (Z11) and 0.15 ps (Z15, Z19, and Z23) after excitation into the lowest-energy band of the S2 state. The maximum in the S* signal is marked by an asterisk. (b) Kinetics measured at the maximum in the S1−Sn transition at 557 nm (Z11), 625 nm (Z15), 690 nm (Z19), and 740 nm (Z23). (c) Kinetics recorded at the maximum in the S* signal at 530 nm (Z11), 580 nm (Z15), 625 nm (Z19), and 640 nm (Z23). Solid lines in panels (b) and (c) are fits extracted from global fitting. All data are normalized to the maximum.

Figure 4. EADS obtained from globally fitting the data obtained for zeaxanthin homologues after excitation into the lowest-energy band of the S2 state.

state, thus faster than in Z11 whose vibrationally hot S1 state decays in 350 fs (red EADS of Z11). The S1 state of Z11 decays in 9 ps while for Z15 the S1 decay is much faster, 0.9 ps. The blue shoulder of the S1−Sn transition of Z15 associated with the S* signal has a lifetime of 2.9 ps. Processes comparable to those in Z15 are identified in Z19; however, hot and relaxed S1 states cannot be resolved. Instead, EADS corresponding to the S1 state is generated within the excitation pulse and decays in 0.35 ps. The S* signal has a significantly longer lifetime of 1.6 ps. Three decay components are necessary to fit the Z23 data. The first EADS is due to the S1 state which decays in 190 fs, while the other two are associated with the S* signal. These two components have time constants of 0.24 and 2.3 ps. The Z15 and Z23 samples were also examined after excitation at 400 nm into high-energy bands. While for Z23 this excitation wavelength excites the band corresponding to a Bu+ state, it excites the cis peak for Z15. The experiment with 400 nm excitation was not carried out for Z19 as this molecule degraded significantly under 400 nm radiation. A comparison of transient absorption spectra measured after excitation into the S2 state and higher-energy bands is shown in Figure 5. The excitation of Z15 at 400 nm generates a slightly broader S1−Sn transition, which is likely caused by a larger distribution of various conformers that could be generated by excess energy

or polyenes.16 The kinetics in Figure 3b reveal a shortening of the rise of the S1−Sn signal with increasing N. While the S1−Sn band of Z11 is fully developed only after ∼1 ps due to vibrational relaxation in the S1 state,33,46 no such process is detected for Z19 and Z23, whose S1−Sn bands appear essentially within the excitation pulse. For Z15 the rise of the S1−Sn band is still resolved though it is much faster than for Z11. Kinetics measured at the S* maximum (Figure 3c) exhibit slower decays with time constants of 2.9 and 1.6 ps for Z15 and Z19, respectively. For Z23, the S* shoulder must be fitted by two components of 240 fs and 2.3 ps to achieve satisfying fits (see below global fitting). For Z11, though the S* shoulder is detected, it decays with the same lifetime as the S1 state.33,44 Excited-state dynamics of the zeaxanthin homologues are better visualized by the global fitting analysis shown in Figure 4. The global fitting analysis confirms the ultrafast depopulation of the S2 state of Z15, Z19, and Z23. Because of our limited time resolution (∼100 fs), we could not obtain the EADS corresponding to the S2 state in any of the samples except for Z11, whose first EADS (135 fs) has a shape characteristic of the S2 state. For Z15, the first EADS has a shape characteristic of a hot S1 state, which decays in 165 fs to form a relaxed S1 11307


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into the 0−0 band of the S0−S2 transition (Figure 4). However, for 400 nm excitation we could not resolve any dynamics prior to populating the S1 state, indicating that the high-energy Ag+ state (cis peak) decays to the S1 state within 100 fs. The S* signal is more pronounced after 400 nm excitation and decays in 4 ps. As reported earlier,17 populating the S* state results in increased resolution of vibrational peaks in the ground-state bleaching as compared to the molecule in the S1 state. Excitation of Z23 at 400 nm generates the S* signal directly. While the global fitting of the data excited at 604 nm resolves the S1−Sn signal peaking around 750 nm (Figure 4), no “pure” S1 spectrum is detected after 400 nm excitation. The first EADS contains the S* signal as the dominant feature (Figure 6), and its decay must be fit by two components, 280 fs and 2 ps, in agreement with the 604 nm excitation that yields the S* lifetimes of 240 fs and 2.3 ps (Figure 4). Excitation of both Z15 and Z23 at 400 nm produced long-lived transients as evidenced by the excited-state absorption signal below 550 nm (blue EADS in Figure 6). This signal most likely arises from degradation products with a shorter conjugation that could be excited at 400 nm. The signal in the 450−550 nm region decays in tens of picoseconds and could thus originate from an S1−Sn transition of these shorter products. Figure 5. Comparison of transient absorption spectra measured at a 300 fs delay after the excitation of Z15 (top) and Z23 (bottom) into the 0−0 band of the S0−S2 transition (black) and into higher-energy bands at 400 nm (red).

4. DISCUSSION Zeaxanthin homologues with conjugation lengths extending up to N = 23 offer a unique opportunity to explore the conjugation length dependence of various spectroscopic properties inaccessible to natural carotenoids. The data are summarized in Table 1 and Figure 7, showing the dependence of the S0−S2,

excitation. In agreement with earlier studies,44 excitation at 400 nm produces a transient spectrum with a more pronounced S* signal. A similar effect of the 400 nm excitation is observed for Z23 as the S*/S1−Sn magnitude ratio increased upon 400 nm excitation. Global fitting of the data measured after 400 nm excitation (Figure 6) provided further details. For Z15, the S1 lifetime of 1 ps well matches the 0.9 ps S1 lifetime obtained after excitation

Figure 7. Conjugation length dependence of S0−S2 (black), S1−Sn (red), and S* (blue) transitions for zeaxanthin homologues. The right axis shows the dependence of the S1 (red stars, dashed line) and S* (blue stars) lifetimes on the conjugation length. Since the extension of conjugation to a terminal ring shortens the conjugation by approximately 0.5,17 effective conjugation Neff = N − 1 is used for all molecules.

S1−Sn, and S* transitions and S1 and S* lifetimes on the conjugation length. The energy of the S0−S2 transition decreases with N, and fitting the N dependence to secondorder polynomial16,18,19 E = A + B/N + B/N2 gives an estimation of the S2 energy of the hypothetical infinite zeaxanthin, E  ≈ 14 000 cm−1. This is about 1500 cm−1 lower than for cyclopentene-constrained polyenes, but since the S2 energies of zeaxanthin homologues are systematically

Figure 6. EADS obtained from global fitting data measured for Z15 and Z23 after excitation at 400 nm. 11308


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The Journal of Physical Chemistry A lower than those of constrained polyenes with the same N,16 the difference in E  is expected. For N = 19, the S2 energy of the zeaxanthin homologue is 17 250 cm−1 (Table 1) whereas the cyclopentene polyene with N = 19 has an S2 energy of 18 400 cm−1.16 Figure 7 also shows that the difference between the S0−S2 and S1−Sn energies increases with increasing N. The Sn state must be of Bu+ symmetry to generate a strongly allowed transition from the S1 state of Ag− symmetry. Because all Bu+ states converge to a common E ,16 the energy of the Sn state has a much steeper N dependence than the S2 state even though both states have the same symmetry. The dependence of the S1 lifetime is nearly linear when related to 1/N, and the lifetimes of 0.9 and 0.35 ps for Z15 and Z19 reasonably match those obtained for elongated β-carotenes M15 and M19 with S1 lifetimes of 0.85 and 0.45 ps, respectively.19 Kosumi et al. reported an S1 lifetime of 1.1 ps for M15.9 This result is expected as the β-carotene homologues have nearly identical structure except for the hydroxyl groups attached to nonconjugated carbons 3 and 3′ in the terminal rings of zeaxanthins.47 The S1 lifetimes, however, also match those reported for long synthetic conformationally constrained polyenes whose S1 lifetimes are 1.1 and 0.5 ps for N = 15 and 19.16 Thus, while the molecular structure is an important factor affecting the S1 lifetime of carotenoids/polyenes with N < 11, the structural differences play a rather minor role for long conjugated systems. The zeaxanthin homologue with N = 23 confirms this trend and shows that the energy-gap law is applicable even for very long conjugation lengths. The N dependence of the S2 lifetime cannot be explained by the energy gap law because the S2 lifetime is shortened when N increases.9 Despite the S2 lifetime of Z11 being reported in a number of solvents to be in the range of 110−150 fs,33,44,46 we could not resolve this parameter for the zeaxanthin homologues with N = 15−23. The first spectrum that could be reliably resolved by global fitting (Figure 4) is clearly associated with the S1 state even though the molecules were excited into the S2 state. Given our time resolution of ∼100 fs, this means that the S2−S1 relaxation must be significantly faster than 100 fs. This is in line with the data measured on M15 and M19,19 for which the S2 lifetimes were also unresolved and estimated to be significantly less than 100 fs. This estimation was later confirmed by Kosumi et al.,9 who reported S2 lifetimes of 70 and 90 fs for M15 and M13, indicating that the S2 lifetimes of Z19 and Z23 may be as short as 50 fs. Interestingly, however, for conformationally constrained polyenes the measured S2 lifetimes are slightly longer, yielding 90 fs for N = 15 and even 120 fs for N = 13.16 Thus, while the molecular structure plays almost no role in the S1 lifetime of long carotenoids, for the S2 lifetime the conformational freedom is likely important. Since the S2−S1 relaxation was proposed to be driven by a conical intersection,48−50 the conformational space of the S2 state determines how fast the conical intersection can be reached. For the constrained cyclopentene polyenes reported by Christensen et al.16 this process is therefore slower, resulting in slightly longer S2 lifetimes. The energies and lifetimes of excited states remain unchanged if the molecules are excited into higher-energy bands at 400 nm (Figures 5 and 6). The 400 nm excitation, however, increases the magnitude of the S* signal and also increases the conformational disorder in the S1 state as evidenced by the broader S1−Sn band after 400 nm excitation (Figure 5). This shows that excess energy is partially used to generate various conformers in the S1 state, some of which may

be the precursors of the S* signal. (See the discussion of the S* signal below.) It is remarkable that the longest zeaxanthin homologue is able to release 25 000 cm−1 of excitation energy within just a few picoseconds (Figure 6). Since such large amount of energy cannot be effectively dissipated through solvent shells in such a short time, it suggests that solvent molecules in the vicinity of the solute will be very hot. This effect may be the origin of rather poor stability of long conjugated systems under 400 nm radiation. The important feature observed in transient absorption spectra of Z15, Z19, and Z23 is the appearance of the S* signal. This signal is readily identified as originating from an excitedstate absorption band occurring in the wavelength region between the ground-state bleaching and the S1−Sn band. For carotenoids with N > 11 this band decays with a lifetime longer than for the S1 state.14,17,19,25 The different S1 and S* lifetimes imply that the S* signal originates from a state different from S1, but the assignment of the S* state is a subject of ongoing debate. The S* signal was first reported for M15 and M19 βcarotene homologues and assigned to a hot ground state,19 but this hypothesis was later challenged by numerous studies assigning the S* state to an excited state related to S1;14,27−35 these studies attribute the S* signal to an S1 state of a specific carotenoid conformation. Recently, however, the hot ground state hypothesis has been invoked to explain data from βcarotene and aldehyde-substituted carotenes.37,38 The data on zeaxanthin homologues presented here provide information about the possible origin of the S* state. The N dependence of the S* signal energy shown in Figure 7 indicates that it behaves more like the S0−S2 transition than the S1−Sn transition. The energy gap between the 0−0 band of the S2 state and the S* signal remains nearly constant at ∼1200 cm−1. In contrast, the N dependence of the S1−Sn transition energy is different from that of the S* signal; the energy gap widens significantly especially for N = 23 for the reasons stated above. Similar behavior was reported for polyenes.16 Further complication in assigning the S* signal to an S1-like excited state is the N dependence of the S* lifetime. While the S1 lifetime reasonably follows the energy gap law, the S* lifetimes clearly do not depend linearly on 1/N (Figure 7). The S* signal of Z23 even needs two decay components to fit the data, which is apparently an intrinsic property of the very long systems since the same was reported for the cyclopentene polyene with N = 19.16 These observations suggest that spectroscopic properties of the S* state differ from those of the S1 state. An experimental issue that must be taken into account when interpreting the origin of the S* signal is the observation of more resolved vibrational bands in the ground-state bleaching when a carotenoid is in the S* state.17 This is also observed here, especially after 400 nm excitation (Figure 6). This means that the S* state is preferentially populated for a specific subset of ground-state conformations. Thus, regardless of the origin of the S* signal, the S* state can be populated only in a molecule having the proper ground-state conformation. The key role of different conformations is underlined by experiments carried out at low temperature showing that the S* formation is diminished under cryogenic temperatures.14,26 However, contrary to earlier assumptions proposing the “conformational branching” taking place during the S2−S1 relaxation,14 the route to the S* state is most likely already decided in the ground state.29 The possible ground-state conformations leading to the S* state were identified by quantum chemical calculations.27,28 11309


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than Z23 but still long enough to observe an S* signal with a lifetime longer than for the S1 state. In Z15, the S1 state decays in 0.9 ps, thus the S* signal should have a 0.9 ps rise component, which is clearly not the case (Figures 4 and 6). The same problem occurs for other carotenoids with a pronounced S* signal such as spirilloxanthin25 or rhodoxanthin.17 Whereas the S1 state decays in these carotenoids with 1.4 and 1.1 ps lifetimes and no corresponding rise of the S* signal is observed. Instead, the typical S* shoulder appeared with the S2 state lifetime.17,25 Even though it is in principle possible that under certain assumptions about magnitudes of extinction coefficients of the overlapping S* and S1−Sn transitions the decay of S1 and rise of S* cancel out,38 it is unlikely it would happen for all carotenoids with the S* signal. Thus, although spectroscopic data presented here for very long conjugated systems with N > 19 as well as the earlier reports on such long systems may be interpreted in terms of the S* signal originating from a hot ground state, the ultrafast route which populates the hot ground state in systems with N = 13−15 remains unexplained. Because it was proposed that the S* signal can be associated with a subset of molecules with a specific ground-state conformation,17,27,28 these conformations would have to be able to populate the hot ground state via the S1 state within a few hundred femtosecond after excitation. Recently, some reports showed that the S1 state is a complicated potential surface with multiple minima that can be populated if the S1 state is reached directly from the ground state instead of the standard route via the S2 state.51,52 The hypothesized specific ground-state conformations associated with the S* state may reach a part of the S1 potential surface that may be close to a conical intersection with the ground-state potential surface, opening an ultrafast “escape route” to a hot ground state. In such case, the S* signal would be generated within a few hundred of femtoseconds via the S1 state. Within this hypothesis, our observation that 400 nm excitation generates more S* signal would imply that excess energy excitation favors the relaxation channel toward the part of the S1 potential surface allowing the escape route to a hot ground state. Although such a scenario is in principle feasible, confirming this hypothesis requires precise calculations of the S1 potential surfaces for long conjugated systems, which is so far not achievable. Our results show that studies of long conjugated systems are crucial in resolving the origin of the S* signal in carotenoids. Only for conjugated systems with N > 13 it is possible to kinetically separate the S1 and S* signals and study spectral and dynamic properties of the S* signal without interference with the S1 state.14,16−19,25 The results presented here still cannot unequivocally assign the S* signal to either the excited state or the hot ground state. Both models are still capable of explaining the data. For the excited-state model, the major complication is that the S* lifetime does not exhibit any clear dependence on conjugation length. For the hot-ground-state model, ultrafast population from the S2 state for Z15 remains unexplained. It should be noted that the hot-ground-state model is more suitable to explaining data recorded for the longest conjugation lengths (N ≥ 19) while the excited-state model with a heterogeneous ground-state population proposed by Balevičius et al.29 better fits the data taken for N = 13−15. For even shorter conjugated systems such as β-carotene, explaining the S* signal does not require additional states, and the origin of the S* shoulder can be traced in the vibrational relaxation of the S1 state.29,30 This further underlines the fact that

Another argument that supports the properties of the S* signal being closely related to the carotenoid structure can be deduced from the S* lifetimes. The S* lifetime does not exhibit N dependence typical of the S1 state (Figure 7). Moreover, S* lifetimes measured for carotenoids/polyenes with comparable N values can have very different values depending on the structure of the molecule. The S* lifetime of 2.9 ps reported here for N = 15 is markedly shorter than 6.7 ps measured for the N = 15 cyclopentene polyene.16 The S* lifetimes of zeaxanthin homologues are also shorter than those reported for M19 and M15 carotenes.19 Since these authors did not use global fitting analysis, a direct comparison of the S* lifetimes is problematic. They reported S* lifetimes of M19 and M15 in the range of 5−15 ps; the S* lifetimes were also solventdependent.19 Thus, there is accumulating evidence confirmed also in this report that the S* signal is much more sensitive to molecular structure and its environment than the properties of the S1 state. Even though the N dependence of the S* lifetime is a strong argument against assigning the S* signal to an S1-like state, it does not rule out the possibility that the S* signal originates from an excited state. Certain excited-state conformations obtained by quantum chemical calculations may affect Neff significantly, which would explain the deviation of the S* lifetimes from the N dependence of the S1 lifetimes.14,29 However, the generation of the S* signal from the relaxed S1 state reported both here for Z23 and earlier for the N = 19 polyene16 does not fit into either the traditional S2 branching model, in which the S1 and S* states are populated directly from the S2 state,14,25,35 or the ground-state conformer model,27−29 which both rule out any population flow between S1 and S* states. Our data on Z23 matches models assigning the S* signal to a hot ground state.37,38 The major problem with the hot-ground-state hypothesis is explaining how the state would be populated because the S* signal has been always observed within the first 400 fs after excitation.10,17,25,28−31 Wohlleben et al.36 proposed the population of the hot ground state via impulsive stimulated Raman scattering (ISRS) that occurs within the excitation pulse. This mechanism was later ruled out by experiments employing spectrally narrow pulses for excitation.34 In the ISRS mechanism, the population of a hot ground state must decrease (or vanish completely) if spectrally narrow pulses are used for excitation. This was not observed as the S* signal was essentially the same in experiments using either broad or narrow excitation pulses.34 Another route for the hot ground state population was proposed by Lenzer et al., who suggested a model in which the hot ground state is populated from the S1 state.37,38 These authors showed that due to the significant overlap of ground-state bleaching, the S1−Sn transition, and the S* signal, the S* signal for some carotenoids can be modeled as being due to a hot ground state populated by “standard” S1 decay. The formation of the S* signal from the S1 state is also observed here, and it is especially pronounced for the longest homologue, Z23. Global fitting (Figure 4) shows that the S* signal of Z23 appears with the same time constant (190 fs) as the S1 state decays. The same was reported for the N = 19 polyene except that the S1−S* conversion was slightly longer, 0.5 ps.16 Although these observations support the assignment of the S* signal to a hot ground state populated via the S1−S* route as proposed by Lenzer et al.,37,38 it becomes more complicated for systems having conjugation lengths shorter 11310


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The Journal of Physical Chemistry A carotenoids with Neff ≤ 11 are not suitable models for studying the S* signal.

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States of Apo- and Diapocarotenes. J. Phys. Chem. A 1999, 103, 2399− 2407. (13) Fuciman, M.; Keşan, G.; LaFountain, A.; Frank, H. A.; Polívka, T. Tuning the Spectroscopic Properties of Aryl Carotenoids by Slight Changes in Structure. J. Phys. Chem. B 2015, 119, 1457−1467. (14) Niedzwiedzki, D.; Koscielecki, J. F.; Cong, H.; Sullivan, J. O.; Gibson, G. N.; Birge, R. R.; Frank, H. A. Ultrafast Dynamics and Excited State Spectra of Open-Chain Carotenoids at Room and Low Temperatures. J. Phys. Chem. B 2007, 111, 5984−5998. (15) Mendes-Pinto, M. M.; Sansiaume, E.; Hashimoto, H.; Pascal, A. A.; Gall, A.; Robert, B. Electronic Absorption and Ground State Structure of Carotenoid Molecules. J. Phys. Chem. B 2013, 117, 11015−11021. (16) Christensen, R. L.; Enriquez, M. M.; Wagner, N. L.; PeacockVillada, A. Y.; Scriban, C.; Schrock, R. R.; Polívka, T.; Frank, H. A.; Birge, R. R. Energetics and Dynamics of the Low-Lying Electronic States of Constrained Polyenes: Implications for Infinite Polyenes. J. Phys. Chem. A 2013, 117, 1449−1465. (17) Chábera, P.; Fuciman, M.; Hříbek, P.; Polívka, T. Effect of Carotenoid Structure on Excited State Dynamics of Carbonyl Carotenoids. Phys. Chem. Chem. Phys. 2009, 11, 8795−8803. (18) Christensen, R. L. The Electronic States of Carotenoids. In The Photochemistry of Carotenoids; Frank, H. A., Young, A. J., Britton, G., Cogdell, R. J., Eds.; Kluwer Academic Publishers: Dordrecht, The Netherlands, 1999; Vol. 8, pp 137−159. (19) Andersson, P. O.; Gillbro, T. Photophysics and Dynamics of the Lowest Excited Singlet-State in Long Substituted Polyenes with Implications to the Very Long-Chain Limit. J. Chem. Phys. 1995, 103, 2509−2519. (20) Frank, H. A.; Desamero, R. Z. B.; Chynwat, V.; Gebhard, R.; van der Hoef, I.; Jansen, F. J.; Lugtenburg, J.; Gosztola, D.; Wasielewski, M. R. Spectroscopic Properties of Spheroidene Analogs Having Different Extents of π-Electron Conjugation. J. Phys. Chem. A 1997, 101, 149−157. (21) 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. (22) Niedzwiedzki, D. M.; Kajikawa, T.; Aoki, K.; Katsumura, S.; Frank, H. A. Excited States Energies and Dynamics of Peridinin Analogues and the Nature of the Intramolecular Charge Transfer State in Carbonyl-Containing Carotenoids. J. Phys. Chem. B 2013, 117, 6874−6887. (23) Kosumi, D.; Kajikawa, T.; Okumura, S.; Sugisaki, M.; Sakaguchi, K.; Katsumura, S.; Hashimoto, H. Elucidation and Control of an Intramolecular Charge Transfer Property of Fucoxanthin by a Modification of Its Polyene Chain Length. J. Phys. Chem. Lett. 2014, 5, 792−797. (24) Christensen, R. L.; Faksh, A.; Meyers, J. A.; Samuel, I. D. W.; Wood, P.; Schrock, R. R.; Hultzsch, K. C. Optical Spectroscopy of Long Polyenes. J. Phys. Chem. A 2004, 108, 8229−8236. (25) Gradinaru, C. C.; Kennis, J. T. M.; Papagiannakis, E.; van Stokkum, I. H. M.; Cogdell, R. J.; Fleming, G. R.; Niederman, R. A.; van Grondelle, R. An Unusual Pathway of Excitation Energy Deactivation in Carotenoids: Singlet-to-Triplet Conversion on an Ultrafast Timescale in a Photosynthetic Antenna. Proc. Natl. Acad. Sci. U. S. A. 2001, 98, 2364−2369. (26) Cong, H.; Niedzwiedzki, D. M.; Gibson, G. N.; Frank, H. A. Ultrafast Time-Resolved Spectroscopy of Xanthophylls at Low Temperature. J. Phys. Chem. B 2008, 112, 3558−3567. (27) Lukeš, V.; Christensson, N.; Milota, F.; Kauffmann, H. F.; Hauer, J. Electronic Ground State Conformers of β-Carotene and Their Role in Ultrafast Spectroscopy. Chem. Phys. Lett. 2011, 506, 122−127. (28) Hauer, J.; Maiuri, M.; Viola, D.; Lukeš, V.; Henry, S.; Carey, A. M.; Cogdell, R. J.; Cerullo, G.; Polli, D. Explaining the Temperature

ASSOCIATED CONTENT

* Supporting Information S

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.jpca.5b08460. Transient absorption spectra of Z15 at different delay times (PDF)

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AUTHOR INFORMATION

Corresponding Author

*E-mail: [email protected]. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS We thank Harry Frank and Ronald Christensen for fruitful discussions and suggestions. The research in the Czech Republic was supported by the Czech Science Foundation (P501/12/G055) and project CZ.1.07/2.3.00/30.0049 (H.S.). M.Z. thanks the Higher Education Commission of Pakistan for a Ph.D. scholarship.

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REFERENCES

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Ultrafast Dynamics of Long Homologues of Carotenoid Zeaxanthin

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