Mechanism of the Intramolecular Charge Transfer State Formation in

Dec 11, 2014 - All the collected time-resolved data can be interpreted in the frame of a recently proposed relaxation scheme, according to which the m...
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Mechanism of the Intramolecular Charge Transfer State Formation in all-trans-β-Apo-8′-carotenal: Influence of Solvent Polarity and Polarizability Elena Ragnoni,†,‡ Mariangela Di Donato,*,†,‡,§ Alessandro Iagatti,†,‡ Andrea Lapini,†,‡,§ and Roberto Righini†,‡,§ †

LENS (European Laboratory for Non-Linear Spectroscopy) via N. Carrara 1, 50019 Sesto Fiorentino (Florence) Italy INO (Istituto Nazionale di Ottica), Largo Fermi 6, 50125 Firenze, Italy § Dipartimento di Chimica “Ugo Schiff”, Università di Firenze, via della Lastruccia 13, 50019 Sesto Fiorentino (Florence), Italy ‡

S Supporting Information *

ABSTRACT: In this work we analyzed the infrared and visible transient absorption spectra of all-trans-β-apo-8′-carotenal in several solvents, differing in both polarity and polarizability at different excitation wavelengths. We correlate the solvent dependence of the kinetics and the band shape changes in the infrared with that of the excited state absorption bands in the visible, and we show that the information obtained in the two spectral regions is complementary. All the collected time-resolved data can be interpreted in the frame of a recently proposed relaxation scheme, according to which the major contributor to the intramolecular charge transfer (ICT) state is the bright 1Bu+ state, which, in polar solvents, is dynamically stabilized through molecular distortions and solvent relaxation. A careful investigation of the solvent effects on the visible and infrared excited state bands demonstrates that both solvent polarity and polarizability have to be considered in order to rationalize the excited state relaxation of trans-8′-apo-β-carotenal and clarify the role and the nature of the ICT state in this molecule. The experimental observations reported in this work can be interpreted by considering that at the Franck−Condon geometry the wave functions of the S1 and S2 excited states have a mixed ionic/ covalent character. The degree of mixing depends on solvent polarity, but it can be dynamically modified by the effect of polarizability. Finally, the effect of different excitation wavelengths on the kinetics and spectral dynamics can be interpreted in terms of photoselection of a subpopulation of partially distorted molecules.

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light absorption are highly dependent on solvent polarity:12−15 the excited state lifetime decreases over 1 order of magnitude in long chain carotenals in polar solvents, as compared with the corresponding value in nonpolar media. Other solvent properties, such as polarizability, can also influence the photodynamics. The shift of the absorption band observed for nonpolar carotenoids has been correlated with the polarizabilty properties of the solvent;16 however, the combined effect of dipole−dipole and dispersion interactions on polar carotenoids has been less investigated and not yet fully rationalized. The peculiar behavior of carbonyl carotenoids has been ascribed to the presence of a low lying excited state with intramolecular charge transfer (ICT) character involved in the deactivation pathway following green light absorption. Although the occurrence of an ICT state is widely accepted in the literature, both its exact nature and the mechanism by

INTRODUCTION Carotenoids are widely distributed in nature, where they exploit multiple functions, which are principally connected to light harvesting and photoprotection from reactive radicals and singlet oxygen.1−5 The complex photophysical behavior of these molecules has been the object of numerous theoretical and experimental studies.6−10 The low lying excited states of carotenoids are usually described by taking as a reference the energy levels of linear polyenes.11 Within this frame, the intense green visible absorption of carotenoids is associated with their S0 → S2 electronic transition; the S0 → S1 transition is forbidden by symmetry rules. In fact, in a linear polyene, both S0 and S1 are classified as Ag− symmetry states, while S2 has Bu+ symmetry. In carotenoids, due to the presence of different substituents on the polyene chain, the symmetry rules are not strictly applicable, and other low lying excited states can possibly take part in the dynamic relaxation processes following photoexcitation. A particularly interesting case is that of carbonyl substituted carotenoids, such as carotenals (carotenoids containing an aldehyde functional group). In this case, the excited state lifetime and the relaxation dynamics following © 2014 American Chemical Society

Received: September 15, 2014 Revised: November 21, 2014 Published: December 11, 2014 420

DOI: 10.1021/jp5093288 J. Phys. Chem. B 2015, 119, 420−432

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The Journal of Physical Chemistry B which this state is populated are still strongly debated.10,17,18 In particular, it has not been clarified yet whether the ICT state is a further electronic state, separated from, although connected to the S1 (2Ag−) and the S2 (1Bu+) states, or if it exists as a unique low lying S1/ICT state, whose charge transfer character increases with the increasing solvent polarity. The most investigated carbonyl carotenoid is the naturally occurring peridinin19−23 found in the peridinin chlorophyll protein (PCP) complex. Carbonyl carotenoids are also found in the photosynthetic antennas of several green and brown algae, diatoms, and dinoflagellates, organisms often living in peculiar environments, such as deep water or other surroundings with low illumination conditions.24−26 It has been suggested that, in these systems, the ICT state can play an important role in enhancing the efficiency of energy transfer toward chlorophylls, also determining an increase of the absorption cross section of the antenna, thus of the photosynthetic activity, in low light conditions.27 A clear understanding of the photophysics of carbonyl carotenoids is important not only to clarify the mechanism leading to the efficient light harvesting of natural antennas, but also to develop synthetic molecular arrays able to mimic the natural systems to be used as building blocks for a new generation of bioinspired photovoltaic devices. Several examples of such carotenoid containing artificial antennas have been engineered,28−30 and it is clear that a deep understanding of the photophysics of their molecular constituents would help in the design of new systems with improved performances. Recently, we have analyzed the deactivation pathway of transβ-apo-8′-carotenal by means of visible pump/mid-IR probe spectroscopy and transient two-dimensional infrared (2DIR) spectroscopy.6 Data were recorded in two solvents with different polarities: the nonpolar cyclohexane and the slightly polar chloroform. On the basis of a global analysis of the timeresolved data and CASPT2/CASSCF (and TD-DFT) quantum chemical calculations of energies, vibrational frequencies, and possible decay paths, we have proposed a kinetic scheme for the polarity-dependent relaxation dynamics of this molecule and investigated the nature of its ICT state. According to our picture the major contributor to the ICT state is the bright 1Bu+ state, which, in polar solvents, is dynamically stabilized through molecular distortions and solvent relaxation. In this paper we extended the spectroscopic analysis to a series of solvents, differing in both polarity and polarizability, by measuring transient spectra in both the visible and mid-IR regions. We show that the information obtained in the two spectral regions is complementary, and that all the timeresolved data can be interpreted in the frame of the previously proposed relaxation scheme. Our study highlights that both solvent polarity and polarizability have to be considered in order to rationalize the time-dependent evolution of trans-βapo-8′-carotenal and clarify the role and the nature of the ICT state in this molecule and possibly in other similar carotenoids.

mm thick quartz cuvette and kept under constant stirring by a small magnet inserted inside the cell. All samples prepared for visible transient absorption measurements had an absorbance of 0.2−0.4 OD at the excitation wavelength. Experimental Setup. All static visible absorption spectra were recorded with a PerkinElmer LAMBDA 950 spectrophotometer with a 1 nm spectral resolution. The integrity of the sample was checked by Fourier transform infrared (FTIR) spectroscopy (Bruker Alpha-T) and visible absorption before and after the time-resolved measurements. All the measurements were carried out at room temperature. The experimental setups used for time-resolved infrared and visible measurements have been extensively described before.31,32 Briefly, in the case of infrared measurements, a portion of the output of a Ti:sapphire oscillator/regenerative amplifier, operating at 1 kHz and centered at 800 nm (Legend Elite, Coherent), was split in order to generate the mid-IR probe and the visible (vis) pump. The infrared probe had a spectral width of 200 cm−1 in the 6 μm region and was obtained by pumping a home-built optical parametric amplifier (OPA) with difference frequency generation. The output of the OPA was split into two beams of equal intensity, which were respectively used as probe and reference. The vis pump at 400 nm was generated by frequency doubling another portion of the laser fundamental beam in a BBO crystal. The excitation beam at 540 nm was generated by a homemade noncollinear optical parametric amplifier (NOPA). At both excitation wavelengths the vispump pulse was attenuated to provide 100−300 nJ and focused to a spot of ∼150 μm in diameter. The polarization of the pump beam was set to the magic angle with respect to the probe beam by rotating a λ/2 plate. A movable delay line made it possible to increase the time-of-arrival difference of the pump and probe beams up to 1.8 ns. After the sample, both probe and reference were spectrally dispersed in a spectrometer (TRIAX 180, HORIBA JobinYvon) and imaged separately on a 32 channel double array HgCdTe detector (InfraRed Associated Inc., USA) with a sampling resolution of 6 cm−1. Two spectral windows were separately recorded and then overlapped in order to cover the spectral region of 1450−1800 cm−1. Transient absorption spectra in the visible spectral range were acquired on a system based on a femtosecond Ti:sapphire laser system (BMI Alpha 1000) capable of producing 800 nm, 100 fs pulses with energy of 500 μJ/pulse at 1 kHz repetition rate. A full description of the system has been previously provided.32 Excitation pulses at 400 nm were generated by frequency doubling a portion of the laser fundamental beam in a BBO crystal. Pump pulses at 540 nm (energy = 150−200 nJ) were obtained by sum frequency generation of the signal output of a commercial optical parametric generator (TOPAS, Light Conversion33,34) with a portion of the fundamental output at 800 nm. A white-light continuum was generated by focusing a fraction of the 800 nm fundamental on a 3 mm thick CaF2 window. The white-light continuum was further split into two parts of equal intensity by a 50/50 fused-silica−Al beam splitter. One part, acting as probe beam, was spatially overlapped with the excitation beam in the sample. The second part crossed the sample in a different position and provided a convenient reference signal. The probe and reference beams were spectrally dispersed in a flat-field 25 cm Czerny−Turner spectrometer and detected by means of a homemade detector consisting of two linear CCD arrays with spectral response in the region 400−750 nm. A movable delay line made it possible to increase the time-of-arrival difference of the pump and probe

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MATERIALS AND METHODS Sample Preparation. trans-β-Apo-8′-carotenal and all solvents were purchased from Sigma-Aldrich and used without further purification. The sample cell for infrared measurements consists of two CaF2 windows of 2 mm thickness, separated by a 50 μm Teflon spacer. The cell was mounted on a movable stage in order to minimize sample degradation. For transient visible absorption measurements the sample was placed in a 2 421

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Figure 1. (A) (left panel) Static absorption spectra of all-trans-β-apo-8′-carotenal in solvents with similar polarizabilities and different polarities. (right panel) Solvents with similar polarities and different polarizabilities. (B) (left panel) Solvent groups according to the functions P(ε) and R(η), representing respectively a measure of solvent polarity and polarizability. The considered solvents can be classified as polar/polarizable solvents including DMSO, chloroform, tetrahydrofuran, and dichloromethane (circles); polar/nonpolarizable solvents including acetonitrile, methanol, diethyl ether (squares); and nonpolar solvents including cyclohexane, n-hexane, and carbon tetrachloride (triangles). (right panel) Distinct trends of the maximum absorption as a function of solvent polarizability. Straight lines are drawn as a guide for the eye.

actions, which affect the solvent polarity and polarizability, respectively. As shown in Figure 1B, all the considered solvents can be divided in three groups on the basis of their polarity: nonpolar solvents (n-hexane, cyclohexane, and carbon tetrachloride), slightly/moderately polar solvents (diethyl ether, chloroform, dichloromethane, and tetrahydrofuran), and polar solvents (acetonitrile, methanol, and dimethyl sulfoxide). The three groups are visualized by drawing horizontal lines on the panel. Notice that if the solvent polarity is expressed directly in terms of the dielectric constant ε, instead of the function P(ε), the relative positions of the various solvents as reported in Figure 1B do not change (in this case there is only a variation of the vertical axis scale, see Figure S1 and Table S1 in the Supporting Information). As concerns the polarizability, we notice that the polar solvents (those with P(ε) > 0.4, ε > 3) can be further divided into two groups: the slightly polarizable ones, with R(η) < 0.24, and the highly polarizable ones, with R(η) > 0.24 (see Table 1). As noticed in previous studies,42 in most cases the maximum absorption wavelength red shifts with increasing the solvent polarizability. In the case of peridinin it has been shown that the peak position of the absorption is a linear function of the polarizabilty only if P(ε) − R(η) < 0.6; otherwise no spectral shift is observed.19,41 In the case of trans-β-apo-8′-carotenal no simple relationship between absorption energy and solvent polarizability can be found. However, it is still possible to classify the properties of the static absorption spectra in dependence on the solvent polarizability, if also the polarity parameter is taken into account. As shown in the right panel of Figure 1B, for the polar/slightly polarizable solvents (diethyl ether, acetonitrile, and methanol) the absorption peak increases

beams up to 2.0 ns. The pump beam polarization was set to the magic angle with respect to the probe beam by rotating a λ/2 plate. The pump and probe beams were focused by a parabolic mirror in an almost collinear scheme. Data Analysis. Time resolved spectra recorded in both the infrared and visible regions have been analyzed applying a combined approach, consisting of singular values decomposition (SVD)35−37 and the simultaneous fitting of all the collected kinetic traces (global analysis). The aim of global analysis is to decompose the two-dimensional (time and wavelength) data matrix into time-independent spectra and wavelength-independent kinetics.38 Once the number of components is identified through the SVD decomposition, the time evolution of the spectral components can be parametrized. This was accomplished by assuming first-order kinetics and describing the overall temporal evolution as the sum or combination of exponential functions. Global analysis was performed using the GLOTARAN package (http:// glotaran.org),39,40 and employing a linear unidirectional “sequential” kinetic scheme.

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RESULTS Static UV−Vis Absorption. The static absorption spectra of trans-β-apo-8′-carotenal in some of the nine solvents considered in this work are shown in Figure 1A. In order to discuss the influence of the solvent on the photophysics of trans-β-apo-8′-carotenal, we classify the analyzed solvents in terms of their dipole−dipole and dispersion interactions. Following previous works13,41 we use the functions P(ε) = ε − 1/ε + 2 and R(η) = η2 − 1/η2 + 2 to take into account the dipole−dipole and dispersion inter422

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The Journal of Physical Chemistry B Table 1. Solvent Polarity P(ε), Solvent Polarizability R(η), and Static Absorption Maximum Position of all-trans-β-Apo8′-carotenal Solutionsa methanol (MetOH) acetonitrile (ACN) diethyl ether (DEE) n-hexane (nHex) tetrahydrofuran (THF) cyclohexane (C6H12) dichloromethane (CH2Cl2) carbon tetrachloride (CCl4) chloroform (CHCl3) dimethyl sulfoxide (DMSO) a

R(η)

P(ε)

abs S0−S2 (cm−1)

0.20 0.21 0.22 0.23 0.25 0.26 0.26 0.27 0.27 0.28

0.91 0.92 0.53 0.23 0.69 0.25 0.72 0.29 0.56 0.94

21 505 21 834 22 026 21 978 21 692 21 692 21 277 21 277 21 008 20 920

In order to identify the time scales of the significant spectral evolution in the system, we globally analyzed the transient data in all solvents, by imposing a sequential decay scheme with increasing lifetimes.38 In almost all cases three kinetic components were necessary to satisfactorily fit the data (in a few cases the quality of the fit was increased by adding a fourth kinetic component). The two shorter lifetime components extracted by global analysis did not show a high degree of variability among all the data sets, being respectively on the order of 100−250 fs and 1−4 ps. On the contrary, as expected, the longer lifetime was strongly dependent on the solvent polarity. We remark that the shortest lifetime component can be affected by an error relatively higher than the one affecting the longer lifetime components, as it is at the limit of our time resolution: in some cases its value has been fixed at 200 fs. The EADS (evolution associated difference spectra) obtained from global analysis for some representative measurements are shown in Figure 2; those referring to the other analyzed solvents are reported in the Supporting Information (Figure S6). All the spectra shown in Figure 2 present a negative signal below 500 nm, principally due to ground state bleaching, and a positive signal at longer wavelengths. The position of the most intense excited state absorption band depends on the solvent. In cyclohexane, the excited state absorption maximum is at 557 nm while among polar solvents

Solvents are ordered by increasing polarizability.

linearly in energy as the polarizability increases, while in the case of polar/polarizable solvents (chloroform, dichloromethane, tetrahydrofuran, and dimethyl sulfoxide) the opposite linear dependence is observed. In the case of the three nonpolar solvents considered (n-hexane, cyclohexane, and carbon tetrachloride) the peak frequencies decrease with the increasing polarizability, although no clear linear dependence is observed. Among solvents with similar polarizabilities, such as cyclohexane, dichloromethane, and thetrahydrofuran (THF) (see Figure 1A), the absorption band is more structured in less polar solvents, where a vibronic progression is well evident. As the polarity increases, the vibronic structure is lost and the band becomes significantly broader, possibly because many ground state conformers are allowed.9 Finally, it can be noticed that the red shifting of the maximum absorption is mainly regulated by the polarizability and much less by polarity: among solvents similar in polarity but differing in polarizability, such as dimethyl sulfoxide (DMSO) and acetonitrile (ACN), the absorption maximum is red shifted by ca. 20 nm in the more polarizable DMSO, while among similarly polarizable solvents the polarity induced shift is definitely smaller (e.g., the red shift in the polar DMSO with respect to the nonpolar carbon tetrachloride is only 8 nm). Transient UV−Vis Absorption. Transient absorption measurements have been performed at two different excitation wavelengths, 400 and 540 nm (or 530 nm in solvents where the absorption is blue shifted), corresponding to the blue and red edges of the absorption band, respectively. The solvent properties highly affect the band shape in the transient spectra and the kinetics of ground state recovery. In discussing the experimental results we follow the solvent classification shown in Figure 1B and we consider (i) polar/polarizable solvents (DMSO, CHCl3, CH2Cl2, THF), (ii) polar/slightly polarizable solvents (MetOH, ACN, DEE), and (iii) nonpolar solvents (nhexane, cyclohexane, and CCl4). Thresholds can be fixed around P(ε) = 0.4 for polarity and R(η) = 0.24 for polarizability. Representative transient spectra recorded upon excitation at 400 and 540 nm in all the considered solvents are reported in the Supporting Information (Figure S4), together with the kinetic traces and their fits obtained from global analysis (Figure S5). There, we also show Gaussian fits of the transient spectra acquired, in several solvents, at 2 ps delay with 400 nm excitation (see the Supporting Information, Figure S3 and Table S2).

Figure 2. Evolution associated difference spectra (EADS) resulting from global analysis on UV−vis transient absorption data. 423

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The Journal of Physical Chemistry B

significant difference is observed upon 400 nm excitation. These trends are magnified in solvents with intermediate polarity and opposite polarizability, such as chloroform and diethyl ether, as shown in Figure 3.

we clearly observe a gradual red shift (558 nm for acetonitrile, 573 nm for chloroform and DMSO) as the polarizability increases. As already noticed for the ground state absorption, solvent polarity has little effect on the red shift of the band maximum, which is nearly the same in acetonitrile and cyclohexane. Besides this intense excited state band, other positive components are visible above 600 nm, while a positive shoulder is observed around 520−530 nm, in nonpolar solvents. While the assignment of the most intense band around 550−570 nm to the S1 → Sn transition is so far accepted in the literature,9 the assignment of the other bands is still a matter of debate. The blue shoulder observed on the main S1 → Sn absorption has been ascribed to a so-called S* state, whose nature has been extensively discussed in the literature but is still controversial.43−46 Our data show that the kinetics of the S* band is not the same as that of the S1 band, as also noticed in previous work.43 A detailed investigation of the electronic origin of the S* state in all-trans-β-apo-8′-carotenal is however beyond the scope of this work, and will be possibly afforded in a future investigation. As to the positive bands located above 600 nm, our data unequivocally show that their intensity is extremely sensitive to the solvent, being enhanced when the polarity is higher. Their position shifts with the solvent properties similarly to what is observed for the S1 → Sn band. In nonpolar and moderately polar solvents a double band structure can be recognized in the absorption features above 600 nm, while in highly polar solvents a unique broad band is visible, whose intensity is almost comparable with that of the S1 → Sn band. Similar bands have been observed in peridinin and other carbonyl carotenoids and have been interpreted as characteristic for the ICT → Sn transition.13,47,48 The transient spectra recorded at the two different excitation wavelengths look qualitatively similar, but changes in the relative intensities of the S1 → Sn and ICT → Sn transient absorption bands are observed in polar solvents; see, for instance, spectra measured in chloroform, dimethyl sulfoxide, and acetonitrile with excitation at 400 and 540 nm reported in Figure 2. In the case of nonpolar solvents (irrespective of their polarizability) or diethyl ether (weakly polar/slightly polarizable), only small variations are observable. The ICT → Sn band intensity also increases remarkably in methanol, when it is excited on the red edge of its static absorption spectrum (see the Supporting Information, Figure S4). As is already well known from previous studies,9,13,48,49 the excited state lifetime of carbonyl carotenoids is highly dependent on solvent polarity. As expected, fitting the kinetic traces measured for trans-β-apo-8′-carotenal in the different analyzed solvents, we find that the S1 lifetime decreases from ca. 30 ps in nonpolar solvents up to 7−9 ps in the highly polar methanol or DMSO. Also, shifting the excitation wavelength toward the red often has the effect of further decreasing the excited state lifetime, particularly in the case of polarizable solvents. The ICT transient absorption bands have a slower rise component if compared to the S1 → Sn absorption in polarizable solvents. This is particularly evident in the case of 400 nm excitation, while no appreciable difference in the rise time of the two bands is observed when the excitation is at 540 nm. On the contrary, in the case of nonpolarizable solvents the opposite behavior is observed: the S1 → Sn band rises slower than the ICT bands when excited at 540 nm, while no

Figure 3. Kinetics of the S1 → Sn (555−575 nm) and ICT (627−665 nm) excited state absorption bands in chloroform and diethyl ether upon excitation at 400 nm (upper panel) and 540/525 nm (lower panel). Experimental data are shown as scattered points; the result of the fit is shown as a continuous line. The two reported kinetic traces behave differently in the two solvents: in chloroform the ICT band rises slower than the S1 → Sn band when the excitation is at 400 nm, while no significant difference is observed upon 540 nm excitation. On the contrary, in diethyl ether there is no appreciable difference at 400 nm excitation, while at 540 nm excitation the S1 → Sn band rises slower than the ICT band.

In the following we discuss the results of the global fitting procedure referring to the different groups of solvents. Nonpolar Solvents. In nonpolar solvents, such as cyclohexane, the first EADS (Figure 2, black line), which can be associated with the initially excited S2 state, shows a negative feature corresponding to ground state bleaching and S2 stimulated emission and a broad positive feature extending to the long wavelength side. The second spectral component, rising in ca. 200 fs, corresponds to the rise of the S1 → Sn excited state absorption band. It evolves in ca. 3 ps (2.0 ps upon 540 nm excitation) into the last spectral component, where a slight blue shift and some sharpening of the excited state absorption bands can be noticed, both attributable to vibrational cooling in the S1 excited state. The interpretation of the spectral evolution in this case is quite simple, and the dynamics of the system can be satisfactorily described by assuming a fast S2 → (hot) S1 transition occurring on a 200 fs time scale, followed by vibrational cooling on the S1 potential energy surface in 2−3 ps. Finally, ground state recovering occurs in ca. 25−30 ps. The ICT characteristic bands above 600 nm are weak, indicating that this state is not highly populated. The effect of changing the excitation wavelength is modest: exciting at 540 nm, we observe only a slight increase in intensity of the ICT absorption bands, if compared with the S1 → Sn excited state absorption, and no acceleration of the ground state recovery time. 424

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The Journal of Physical Chemistry B Polar/Highly Polarizable Solvents. When considering more polar and polarizable solvents, such as chloroform and DMSO, some differences can be noted. Besides the initial fast evolution (ca. 200 fs), which can be interpreted also in this case as the relaxation of the initially populated S2 excited state, the ICT bands above 600 nm grow on a 2−4 ps time scale. The second spectral component is thus not only related to the vibrational cooling in S1, but also to the population of the ICT state. The kinetics of ground state recovery is sensitive to the excitation wavelength, being faster with longer wavelength excitation. Polar/Slightly Polarizable Solvents. In the case of polar but less polarizable solvents, such as acetonitrile or diethyl ether, the ICT bands rise on the same fast time scale connected with the S2 evolution and start to decay within the first picoseconds, while the S1 → Sn absorption band grows in the 1−3 ps time scale. In methanol an additional rise of the ICT bands is observed on the time scale of a few picoseconds (see Figures S4−S6 in the Supporting Information), which can be related to the possibility of forming H-bonds, and to the population exchange between H-bonded and not H-bonded molecules. Upon 540 nm excitation, in acetonitrile and in methanol, the kinetics of ground state recovery are slightly faster and variations in the relative intensity of the S1 → Sn and ICT transient absorption bands can be observed. When the system is excited at 540 nm in methanol (see the Supporting Information), the ICT transient absorption bands are even higher in intensity than the S1 → Sn band. A similar behavior in methanol was previously reported for peridinin and ascribed to the influence of hydrogen bond formation:15 according to this interpretation a red-absorbing population of hydrogen-bonded molecules would decay faster than the non-hydrogen-bonded ones. The lifetimes of the spectral components extracted by global analysis of the data collected in all the analyzed solvents are summarized in Table 2.

In order to discuss the transient IR spectra, we briefly summarize the band assignment in the ground state and the expected band shifts upon visible excitation. In the ground state FTIR spectrum of trans-β-apo-8′carotenal measured in cyclohexane, five bands can be distinguished in the spectral region 1450−1800 cm−1: the CO stretching band (∼1680 cm−1), two asymmetric CC stretching bands (1615 and 1565 cm−1), and the symmetric CC stretching band (1530 cm−1). The peak position changes with the solvent polarity, and in polar solvents all these bands are red shifted up to ∼20 cm−1. The FTIR spectrum of the molecule is reported in Supporting Information, Figure S2. Upon visible excitation the IR marker bands upshift or downshift depending on the redistribution of the charge density on the molecular functional groups. In particular, the excited state IR spectrum shows an intense and broad absorption peak around 1700 cm−1, in a spectral region where no absorption is observed in the corresponding ground state spectrum. This band has been assigned on the basis of transient resonance Raman spectroscopy and of computational studies on polyene molecules, to the symmetric CC stretching in the S1 excited state,42,52−54 which has an unusually large upshift (ca. 180 cm−1) with respect to the corresponding absorption in the ground state (∼1530 cm−1). In the bright S2 excited state the symmetric CC stretching is also predicted to upshift with respect to S0, although to a minor extent.6 As concerns the other IR marker bands, the CO stretching is expected to downshift in the excited state because of the increased electron density on the carbonyl; indeed a recent computation predicts a 20−40 cm−1 downshift.6 The assignment is less straightforward in the low-energy part of the spectrum, because several excited state bands, mostly due to chain modes, overlap.6 The excited state infrared spectra change significantly with the increase of solvent polarity and as a function of the excitation wavelength. To highlight this effect, in Figure 4 we

Table 2. Lifetimes Extracted from Global Analysis on UV− Vis Transient Absorption Data in All Solvents 400 nm

540 nm

solvent

τ1 (ps)

τ2 (ps)

τ3 (ps)

τ1 (ps)

τ2 (ps)

τ3 (ps)

cyclohexane CCl4 diethyl ether MetOH ACN THF CH2Cl2 CHCl3 DMSO

0.20 0.20 0.20 0.20 0.11 0.24 0.20 0.17 0.14

2.9 3.5 3.1 2.9 0.8 2.5 1.7 3.9 1.9

26.2 32.2 24.4 8.4 8.1 25.4 16.8 22.4 9.0

0.2 0.2 0.2 0.13 0.15 0.2 0.2 0.2 0.12

2.0 2.3 1.7 2.0 0.7 1.9 1.2 2.9 1.2

26.3 25.7 24.5 7.1 7.3 25.1 11.2 22.0 7.8

Visible Pump−IR Probe Absorption. Transient infrared spectra (TRIR) have been collected in each solvent at two different excitation wavelengths (400 and 540 nm) in the midIR region from 1450 to 1800 cm−1. Spectra at selected time delays and representative kinetic traces are shown in Figures S7 and S8 in the Supporting Information. The role of solvent polarity in defining the infrared band shapes and their time evolution has been previously discussed in the literature, as well as the assignment of transient bands to specific vibrational transitions.6,42,50,51

Figure 4. Effect of different excitation wavelengths on the transient infrared spectra registered in cyclohexane and chloroform at 3 ps pump−probe delay and in DMSO at 1 ps pump−probe delay. All spectra are normalized on the 1680−1700 cm−1 band. 425

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The Journal of Physical Chemistry B report representative spectra recorded in cyclohexane, chloroform, and DMSO exciting the sample at 400, 500, and 550 nm. The spectra displayed for cyclohexane and chloroform refer to a pump−probe delay of 3 ps, while those shown for DMSO refer to a pump−probe delay of 1 ps. It can be clearly noticed that the band shape is highly affected by the solvent polarity. In the nonpolar solvent negative signals from depleted ground state bleaching are evident for both the symmetric CC and CO stretching. The excited state absorption bands are narrow, and two intense bands are observed around 1620 and 1755 cm−1. Changing the excitation wavelength yields only minor changes, mostly limited to short pump−probe delay times. In the first 2 ps, the bands measured with excitation at 540 nm are slightly broader than the corresponding bands upon excitation at 400 nm. In the polar solvents, bands are generally broader and the negative signals of the ground state bleaching can be distinguished only as dips in the overall positive signal due to excited state absorption. Unlike in cyclohexane, in polar and polarizable solvents changing the excitation wavelength has a remarkable effect, especially on the CC band around 1700 cm−1. In fact, when the excitation is set at 540 nm, this band is definitely narrower and red shifted in comparison to the transient spectra measured upon excitation at 400 nm. This effect is particularly evident in chloroform, while in DMSO also narrowing of the lower frequency bands (peaking at ca. 1550 cm−1) is observed. As will be shown in the following, this trend is observed in all polarizable solvents, but the effect is magnified in solvents with high polarizability and intermediate polarity, such as CHCl3, THF, and CH2Cl2 (see Figure 5 and the Supporting Information, Figures S7−S9). In order to extract the kinetic constants representative for the excited state evolution, we applied a global analysis modeling procedure also in the case of TRIR data. As in the case of visible spectra, we adopted a linear scheme with three kinetic components; in some cases the addition of a fourth long lifetime component improved the fit. The EADS obtained from global analysis for some representative solvents are shown in Figure 5 (at two excitation wavelengths). The results for the remaining solvents are reported in Supporting Information (Figure S9). In almost all cases the first spectral component (black line in Figure 5) decays in about 200 fs and is assigned to the initially populated S2 excited state. It presents a broad absorption feature in the 1680−1700 cm−1 region, whose exact position changes with the solvent polarity. This band, which has been assigned in previous work to the upshifted CC stretching in the S2 state,6,53 significantly upshifts and, in the case of polar solvents, broadens in the following EADS, signaling the rise of the S1 excited state. In nonpolar solvents, on a few picoseconds time scale, the excited state symmetric CC band subsequently undergoes a small blue shift and an appreciable narrowing, indicative of vibrational cooling. In a polar and polarizable solvent, such as chloroform, the excited state CC band gains intensity on the red side (a peak at 1685 cm−1 develops in chloroform). A similar spectral evolution is observed in the cases of THF, CH2Cl2, and DMSO (see EADS reported in the Supporting Information, Figure S9). However, if the polarizability is low, the opposite behavior is observed: in diethyl ether, for instance, the high frequency band significantly gains in intensity on its blue side. In the more polar acetonitrile a clear band shift is observed on the 200 fs time

Figure 5. EADS extracted from global analysis on transient IR absorption data.

scale; the broad blue-shifted band which appears in the second EADS shows at later times only a further slight blue shift, which is attributable to vibrational cooling. As previously suggested,6 the spectral evolution observed in polar solvents implies that two components, with different rising times, contribute to the 1680−1750 cm−1 broad absorption. This interpretation is supported by the inspection of the kinetic traces measured on the low and high frequency tails of the excited state CC band, shown in Figure 6 (see also Figure S8 in the Supporting Information). The kinetic traces reported in Figure 6 behave similarly to those reported in Figure 3 obtained from the visible transient spectra. In particular, the trace at 1685 cm−1 behaves like the visible kinetic traces above 600 nm, which strongly suggest its assignment to the ICT state. Moreover, the red and blue sides of the CC stretching band have an opposite behavior in diethyl ether and chloroform, as observed in the visible region for the S1−Sn and ICT bands. The lifetime of the last spectral component reflects the dependence on the solvent polarity of the S1 → ground state recovery time, which, in agreement with the pump−probe measurements presented in the previous paragraph and literature data, decreases as the solvent polarity increases. The shape and the time evolution of the transient spectra are affected by the excitation wavelength. Exciting at 540 nm in chloroform, as well as in other polar and polarizable solvents, the CC absorption band is narrower and blue shifted with 426

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Article

DISCUSSION

From all the time-resolved data reported in this paper, it is evident that the excited state relaxation pathway of trans-β-apo8′-carotenal is extremely sensitive to the solvent properties and that in order to understand its behavior both solvent polarity and polarizability have to be taken into account. As already pointed out in the literature,6,9,12,41,47−49,55 the excited state energy level scheme adopted for linear polyenes and based on the selection rules dictated by the C2h symmetry group appears too simplified in the case of carbonyl carotenoids. In the molecules of this family an excited state with intramolecular charge transfer character has to be considered in order to rationalize the dependence of the excited state lifetime on the solvent polarity. Furthermore, we remark that an important role is also played by the solvent polarizability, as previously reported16,56 and confirmed by our findings. The analysis of the time-resolved data presented in this paper and of previously reported results for other carbonyl carotenoids19,57 allows the identification of characteristic bands, in both the visible and infrared spectral ranges, signaling the presence of the ICT state. In the visible transient absorption spectra, the presence of an ICT state is evidenced by the rise of a broad excited state absorption band above 600 nm (see Figure 2), and of a stimulated emission band in the 800−900 nm region.48 The mid-IR spectra are particularly informative, since notable differences in band shapes are observed by changing both the solvent properties and the excitation wavelength.6,42,51 Here the most informative region is 1680−1750 cm−1, where the excited state CC stretching band (strongly upshifted with respect to ground state) is located. In polar solvents this band is much broader than in nonpolar ones: previous measurements6 and the results reported in this study indicate that two different peaks contribute to its broad envelope. As shown in the previous paragraphs, the behavior of the visible and infrared bands has a similar solvent dependence, so the measurements in the two spectral ranges can be correlated to discuss the solvent effects on the excited state potential energy surfaces of trans-β-apo-8′carotenal, and further clarify the nature of the ICT state. We recently reported on the role, nature, and population mechanism of the ICT state based on the analysis of transient one- and two-dimensional infrared spectra of trans-β-apo-8′carotenal.6 In that study we proposed a deactivation pathway, supported by quantum chemical computations, that explains the evolution of visible pump−IR probe and transient 2DIR spectra, measured in cyclohexane and chloroform upon 400 nm excitation. According to the proposed scheme, the radiationless

Figure 6. Kinetic traces recorded in chloroform and diethyl ether on the red and blue sides of the CC excited state absorption band as a function of the excitation wavelength (400 nm excitation is shown in the upper panel and 540 nm in the lower panel). Experimental data are shown as scattered points; continuous lines represent the fit obtained with global analysis. In chloroform the red tail of the band (1685 cm−1) rises slower than the blue tail (1715 cm−1) when the excitation is at 400 nm, while no significant difference is observed upon 540 nm excitation. On the contrary, in diethyl ether no significant difference is observed upon 400 nm excitation, while the blue tail of the band (1750 cm−1) rises slower than the red tail of the band (1700 cm−1) when the excitation is at 540 mm. Kinetic traces have been normalized on the long time decay.

respect to what is observed upon 400 nm excitation. On the other hand, in diethyl ether we observe, on a 1.3 ps time scale, a substantial decrease of the red-most part of the broad CC absorption, initially peaking around 1710 cm−1 (in the first and second EADS) and the rise of a blue component, peaking at ca. 1750 cm−1. Spectra in acetonitrile are less perturbed by changing the excitation wavelength: exciting at 540 nm in this solvent the first spectral component, which decays in 200 fs, is broader than in the case of 400 nm excitation. The shape of the high frequency band in the first EADS is very similar to that of the next two EADS. The spectral evolution in methanol is very similar to what is observed in acetonitrile (see the Supporting Information, Figures S7−S9), the difference being that in this case the kinetics of ground state recovery is shorter upon 540 nm excitation. The lifetimes obtained by global analysis of all the recorded data sets are summarized in Table 3.

Table 3. Lifetimes Extracted from Global Analysis of Transient IR Absorption Spectra in All Solvents 400 nm

540 nm

solvent

τ1 (ps)

τ2 (ps)

τ3 (ps)

τ1 (ps)

τ2 (ps)

τ3 (ps)

cyclohexane CCl4 diethyl ether MetOH ACN THF CH2Cl2 CHCl3 DMSO

0.20 0.30 0.20 0.2 0.17 0.28 0.20 0.20 0.20

2.3 2.4 1.9 1.8 2.1 2.7 1.2 4.0 1.7

25.0 30.5 26.8 7.8 8.4 (+17) 23.8 12.8 17.8 8.3

0.20 0.30 0.30 0.20 0.20 0.25 0.20 0.20 0.20

2.6 2.1 1.9 1.7 2.6 1.6 1.4 3.5 1.6

24.0 23.2 22.9 6.1 8.6 (+2500) 22.1 11.2 14.9 6.9

427

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two S1 and S2 excited states. In order to explain the experimental observations, we have to remark that in carbonyl carotenoids the symmetry rules are not strictly applicable. Previous computations6,10,20,58,59 have shown that at the Franck−Condon (FC) geometry there is a significant degree of mixing between the 1Bu+ and 2Ag− states and that the energy difference between the low lying excited states strongly depends on solvent polarity. The ionic 1Bu+ (S2) state is stabilized in polar solvents, and consequently, the S2−S1 energy gap strongly decreases in these media. Recently it has been shown8 that subtle geometrical variations can significantly alter the nature, energies, and electronic properties of the excited states, modifying the 2Ag−/ 1Bu+ degree of mixing. The transition oscillator strength, the ratio of single and double excitation character of the low lying excited states, and the dipole moment of the S1 and S2 excited states significantly depend on the bond length alternation (BLA) structural parameter. While the zero value of BLA corresponds to a completely delocalized charge all over the conjugated chain, small geometrical distortions leading to nonzero BLA values correspond to a less conjugated molecular form, where the single and double bond CC characters are more localized. Knecht et al.8 shown that, with increasing BLA, S1 gains more ionic character, while on the contrary S2 gains more doubly excited (i.e., covalent) contribution, with the electronic energy gap between the first two low-lying excited states getting smaller when their mixed nature increases. Polar solvents can stabilize conformations with increased BLA, since slightly distorted molecules, where the electronegative CO group is more isolated from the conjugated chain, can be stabilized in a polar environment. This implies that in highly polar solvents both S1 and S2 states have a large amount of ionic character already in the FC region, which explains the rather fast appearance of ICT spectral signatures and a limited spectral evolution in time. In less polar solvents, at the FC geometry, the weight of the covalent configuration is higher in S1, while in S2 the ionic character predominates. However, if the polarizability is sufficiently high, the ionic character of S1 can dynamically increase while moving out of the Franck−Condon region, because molecular distortions and subsequent solvent rearrangement can induce an increase in the molecule’s dipole moment. When the molecule is excited at 400 nm, the excess of energy provided can likely activate a molecular deformation, followed by a solvent reorganization. The polarizable solvents dynamically stabilize the ionic states, increasing the ionic contribution in the lower excited state, which can be seen as a repopulation of the 1Bu+ state.6 This explains the spectral evolution observed on a 2−4 ps time scale in solvents with intermediate polarity and sufficiently high polarizability and the observed rise of ICT signatures on this time scale (observed both in the 600−700 nm region in the visible and in the excited state CC stretching band around 1680−1700 cm−1 in the IR measurements). On the contrary, when the polarizability is low, a structural distortion leading to larger charge separation character is not favored by solvent rearrangements. The solvent reorganization will instead favor an increasing covalent character of the excited state, which explains the behavior of the transient spectra in diethyl ether. In fact, the relative increase in intensity of the S1 → Sn excited state absorption, evident in the third EADS in the visible spectra (Figure 2), and the growth of the IR band at 1750 cm−1, observed in the third EADS of Figure 5, are

decay in carbonyl carotenoids proceeds primarily via a conical intersection between the initially populated S2 (1Bu+) state and the symmetry forbidden S1 (2Ag−) state. In nonpolar solvents the 2Ag− state further decays directly to the ground state. In polar solvents the bright 1Bu+ state, which has been suggested to be the main contributor to the ICT state,6 is repopulated via a slightly activated mechanism, involving a molecular distortion, and in particular the rotation θ around one of the C−C bonds of the chain. A theoretical evaluation of the dependence of the energies of the 2Ag− and 1Bu+ states on the torsional angle θ showed that the ionic 1Bu+ state is stabilized below the 2Ag− state when θ is about 20°. The proposed kinetic scheme is graphically summarized in Scheme 1. We have shown that it is Scheme 1. Kinetic Scheme Proposed for the Excited State Relaxation Dynamics of all-trans-β-Apo-8′-carotenal in (a) Nonpolar Solvents and (b) Polar Solventsa

a

According to the proposed scheme, in polar solvents the ionic 1Bu+ state is stabilized on a few picoseconds time scale through a molecular distortion, resulting in the major contributor to the ICT state.

able of explaining the observed spectral evolution, and in particular the red−blue−red evolution of the CC excited state frequency observed in chloroform.6 By extending our investigation to a number of polarizable/ slightly polar solvents, here we show that the solvent effect on the spectral evolution of trans-β-apo-8′-carotenal is similar to what was previously observed in chloroform. Furthermore, in this work we also show that the visible transient spectra undergo a time evolution that can be correlated with what is observed in the infrared, thus strengthening our interpretation. In particular, we notice that, in the same polarizable/slightly polar solvents, the ICT bands above 600 nm rise on the same time scale (2−4 ps) on which the red−blue−red evolution in the ca. 1700 cm−1 region in the infrared occurs. When considering more polar solvents with high polarizability (DMSO, for instance), the spectral evolution observed in chloroform is less evident although still detectable in the high frequency region of the second and third EADS. This is a consequence of the significant population present in the ICT state already at early delay times after excitation, which determines a further broadening of the excited state CC band (at 1680−1700 cm−1, see Figures 4 and 5). In this case, the UV/vis data are more sensitive than transient infrared ones, since the evolution of the ICT bands absorbing at λ > 600 nm can be better resolved on the 1−2 ps time scale. The situation is different in less polarizable and slightly polar solvents, such as diethyl ether, where the opposite behavior is observed. Here, the high frequency side of the IR broad CC stretching band rises on a few picoseconds time scale. Comparatively, in the visible, the S1 → Sn excited state absorption band (peaking at 553 nm) gains in intensity on the same time scale; see Figure 2. Although apparently controversial, these observations can still be rationalized within a simplified scheme that includes only three electronic levels, namely the ground state and the 428

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The Journal of Physical Chemistry B fingerprints of the increasing contribution of covalent character in S1. Finally, independently of the polarizability, if the polarity of the solvent is sufficiently high, both S1 and S2 excited states have a significantly high covalent/ionic degree of mixing, since the S2/S1 energy gap at the FC geometry is very low. In this case the ICT bands appear in the transient spectra at early times, and both the spectral evolution and the band shape changes in time are comparatively less evident than in moderately polar but polarizable solvents. Looking at the second EADS from global analysis of visible data in acetonitrile and DMSO, reported in Figure 2, it is evident that the intensity of the 600−700 nm ICT bands is comparable to that of S1 → Sn already on a few picoseconds time scale, because of the mixed covalent/ionic nature of both S2 and S1 states. In the infrared (see Figure 5) bands are very broad in all EADS and only a modest spectral evolution is observed. As concerns the excitation wavelength dependence observed in our measurements, taking into account the effect of structural distortions on the excited state energies and electronic properties,6,8,48,49 the more natural explanation is to ascribe the excitation wavelength effects to structural inhomogeneity among ground state conformers,46 which is enhanced in polar solvents, but can still occur, although to a minor extent, even in nonpolar ones. We notice that even in cyclohexane, when exciting on the very red edge of its absorption band, spectral features indicating a higher degree of ICT character appear (see Figures 2 and 5). This is particularly evident in the infrared, where at early times the excited state bands are slightly broader when the molecule is excited at 540 nm with respect to what is observed when 400 or 500 nm excitation is used. In the visible, changes are less evident; nevertheless a small relative increase in intensity of the bands above 600 nm with respect to S1 → Sn absorption can be appreciated when exciting at 540 nm. In highly polar solvents both S2 and S1 excited states have a high ionic/covalent mixed character, so no relevant changes appear at different excitation wavelengths. If the polarizability is low, such as in acetonitrile, small effects are observed on the kinetics. In contrast, when the polarizability is high, such as in DMSO, the ground state recovery time is shorter when the sample is excited on the red edge of its absorption spectrum, since the amount of ionic character in S1 dynamically increases after photoexcitation, because of polarizability effects. In solvents with intermediate polarity once again the effect is magnified. In polarizable solvents (such as chloroform, THF, or CH2Cl2) a narrowing and red shifting of the excited state CC stretching IR band is observed. In chloroform, for instance, the frequency of the excited state CC stretching band is ca. 1680 cm−1, and it remains constants in all EADS when exciting at 540 nm (see Figure 5). In this case the red−blue−red evolution noticed with 400 nm excitation is not observed. It is evident that, when exciting at 400 nm, the system evolves toward a state, the ICT, whose major contributor has, according to our interpretation, 1Bu+ character and a distorted molecular configuration. This state can be directly populated when the excitation is at 540 nm, because at this wavelength a subpopulation of red-absorbing distorted molecules is photoselected. The same observation follows by looking at the visible spectra, where, upon 540 nm excitation, the bands above 600 nm are significantly more intense than in the case of 400 nm excitation at short pump−probe delays.

In less polarizable solvents (diethyl ether), once again the opposite behavior is observed. Looking at Figure 5, we observe a blue shift from 1680 to 1750 cm−1 upon 400 nm excitation in the evolution from the second to the third EADS, signaling the increase of covalent character in S1. When exciting at 540 nm, the photoselected distorted population gives a narrower and stronger signal at ca. 1700 cm−1 already at early times, which then upshifts further in the third EADS by the effect of vibrational cooling. The spectra measured in methanol, reported in the Supporting Information, deserve some further comment. Both polarity and polarizability of this solvent are similar to those of ACN; however, in this case the excitation wavelength effect on both the spectral shapes and kinetics is more marked (see the transient spectra and EADS reported in the Supporting Information). This is probably due to a further parameter affecting the photodynamics of the system in this solvent, connected to its ability of forming H-bonds. An acceleration of the excited state decay in methanol when exciting the system on the red edge of the absorption band has been previously reported in the case of peridinin and fucoxanthin.15,24,60 For these systems, this observation has been explained by assuming that the H-bonded molecules have a faster dynamics and a redshifted absorption, being thus selectively excited upon long wavelength excitation. Similar arguments could be invoked to explain the decrease of the excited state lifetime observed in this study in methanol upon 540 nm excitation. Finally, we remark that, as previously suggested,6 our model allows a rationalization of the behavior of carotenoid analogues with different chain lengths. As recently shown by several studies18,19,61 considering longer and shorter chain analogues of peridinin and fucoxanthin, the contribution of the ICT state in the excited state relaxation pathway is lower for long chain carotenoids and becomes predominant in the case of the shortest chain members of the analyzed series of molecules. This can be explained by a progressive decrease, with decreasing chain length, of the energy gap between the 2Ag− and 1Bu+ states allowing stronger excited state mixing and a substantial ionic contribution also in S1. In the case of the fucoxanthin analogues,18 only one excited state absorption band is observed in the transient spectra of the shorter chain analyzed molecule (C32fx), which has been assigned to the ICT state also in nonpolar solvents. However, it has to be remarked that, also in the short chain systems, the maximum of the excited state absorption band moves to the red in dependence on the solvent polarizability. This behavior can be observed in the spectra reported in ref 18, whose trend can be interpreted using the arguments presented in this work.

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CONCLUSIONS

The time-resolved measurements in the visible and infrared spectral ranges reported in this study indicate that the excited state relaxation dynamics of trans-β-apo-8′-carotenal depend on both polarity and polarizability of the solvent. In particular, the following observations can be made: 1. The excited state lifetime is shortened as a function of solvent polarity, due to the formation of an ICT state. 2. The characteristic transient bands assigned to the ICT state rise on a slower time scale than the S1 marker bands in solvents with sufficiently high polarizability, while an opposite behavior is observed when the solvent polarizability is low. 429

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(5) van Amerongen, H.; van Grondelle, R. Understanding the Energy Transfer Function of LHCII, the Major Light-Harvesting Complex of Green Plants. J. Phys. Chem. B 2001, 105, 604−617. (6) Di Donato, M.; Segado Centellas, M.; Lapini, A.; Lima, M.; Avila Ferrer, F. J.; Santoro, F.; Cappelli, C.; Righini, R. A Combination of Transient 2D-IR Experiments and Ab Initio Computations Sheds Light on the Formation of the Charge-Transfer State in Photoexcited Carbonyl Carotenoids. J. Phys. Chem. B 2014, 118, 9613−9630. (7) 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. (8) Knecht, S.; Marian, C. M.; Kongsted, J.; Mennucci, B. On the Photophysics of Carotenoids: A Multireference DFT Study of Peridinin. J. Phys. Chem. B 2013, 117, 13808−13815. (9) Polivka, T.; Sundstrom, V. Ultrafast Dynamics of Carotenoid Excited States. From Solution to Natural and Artificial Systems. Chem. Rev. 2004, 104, 2021−2072. (10) Enriquez, M. M.; Fuciman, M.; LaFountain, A. M.; Wagner, N. L.; Birge, R. R.; Frank, H. A. The Intramolecular Charge Transfer State in Carbonyl-Containing Polyenes and Carotenoids. J. Phys. Chem. B 2010, 114, 12416−12426. (11) Tavan, P.; Schulten, K. Electronic Excitations in Finite and Infinite Polyenes. Phys. Rev. B 1987, 36, 4337−4358. (12) Ehlers, F.; Wild, D. A.; Lenzer, T.; Oum, K. Investigation of the S1/ICT-S0 Internal Conversion Lifetime of 4′-apo-β-caroten-4′-al and 8′-apo-β-caroten-8′-al: Dependence on Conjugation Length and Solvent Polarity. J. Phys. Chem. A 2007, 111, 2257−2265. (13) Kopczynski, M.; Ehlers, F.; Lenzer, T.; Oum, K. Evidence for an Intramolecular Charge Transfer State in 12′-Apo-β-caroten-12′-al and 8′-Apo-β-caroten-8′-al: Influence of Solvent Polarity and Temperature. J. Phys. Chem. A 2007, 111, 5370−5381. (14) Wild, D. A.; Winkler, K.; Stalke, S.; Oum, K.; Lenzer, T. Extremely Strong Solvent Dependence of the S1-S0 Internal Conversion Lifetime of 12′-apo-β-caroten-12′-al. Phys. Chem. Chem. Phys. 2006, 8, 2499−2505. (15) Zigmantas, D.; Hiller, R. G.; Yartsev, A.; Sundstrom, V.; Polivka, T. Å. Dynamics of Excited States of the Carotenoid Peridinin in Polar Solvents: Dependence on Excitation Wavelength, Viscosity, and Temperature. J. Phys. Chem. B 2003, 107, 5339−5348. (16) Andersson, P. O.; Gillbro, T.; Ferguson, L.; Cogdell, R. J. Absorption Spectral Shifts of Carotenoids Related to Medium Polarizability. Photochem. Photobiol. 1991, 54, 353−360. (17) Polivka, T.; Kaligotla, S.; Chabera, P.; Frank, H. A. An Intramolecular Charge Transfer State of Carbonyl Carotenoids: Implications for Excited State Dynamics of Apo-Carotenals and Retinal. Phys. Chem. Chem. Phys. 2011, 13, 10787−10796. (18) 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. (19) 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. (20) Wagner, N. L.; Greco, J. A.; Enriquez, M. M.; Frank, H. A.; Birge, R. R. The Nature of the Intramolecular Charge Transfer State in Peridinin. Biophys. J. 2013, 104, 1314−1325. (21) Shima, S.; Ilagan, R. P.; Gillespie, N.; Sommer, B. J.; Hiller, R. G.; Sharples, F. P.; Frank, H. A.; Birge, R. R. Two-Photon and Fluorescence Spectroscopy and the Effect of Environment on the Photochemical Properties of Peridinin in Solution and in the Peridinin-Chlorophyll-Protein from Amphidinium Carterae. J. Phys. Chem. A 2003, 107, 8052−8066.

3. In highly polar solvents the intensity of the ICT bands is comparable to that of the S1 bands: the growth of the ICT bands in the time-resolved spectra is very fast. 4. Exciting the sample on the red edge of its absorption band induces a faster excited state relaxation in polar and polarizable solvents. Furthermore, a variation in the excited state band shape is observed, which is particularly evident in the IR, especially in polarizable solvents with intermediate polarity. All these observations can be rationalized by considering that at the FC geometry the wave functions of the S1 and S2 excited states have a mixed ionic/covalent character, whose relative weight depends on the solvent properties. The degree of mixing of ionic and covalent character in the FC region depends on solvent polarity, but it can be dynamically modified while the molecule evolves on the excited state potential energy surface by the effect of polarizability. In particular, in solvents with sufficiently high polarizability (>0.24), the contribution of ionic character in the low lying excited state dynamically increases, determining the appearance of spectral markers characteristic of the ICT state. A previous theoretical analysis6 has shown that the dynamic increase of ionic character in the lowest lying excited state occurs through a slightly activated mechanism involving molecular distortions. Moving along the torsion coordinate lowers the energy of S2 (1Bu+), making it similar to that of S1 (2Ag−) and allowing population transfer between these two states. Within the frame of this mechanism, the effect of different excitation wavelengths on the kinetics and spectral shapes reported in this work can be interpreted in terms of a photoselection of a subpopulation of partially distorted molecules.

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ASSOCIATED CONTENT

S Supporting Information *

Solvent dielectric constants; FTIR spectra; raw data from transient UV−vis and visible pump/IR probe spectra; selected kinetic traces and fit from global analysis; Gaussian fit of the transient spectra acquired at 2 ps delay, with 400 nm excitation, in several solvents. This material is available free of charge via the Internet at http://pubs.acs.org.

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AUTHOR INFORMATION

Corresponding Author

*E-mail: [email protected]fi.it. Tel.: +390554572483. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS The authors gratefully acknowledge support from the Italian MIUR: FIRB “Futuro in Ricerca 2010” Grant RBFR10Y5VW to M.D.D. and RBFR109ZHQ supporting A.L.; PRIN, 2010ERFKXL_004 to R.R.; and the Regione Toscana, Project EFOR-CABIR L. 191/2009 art. 2 comma 44.

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REFERENCES

(1) Demmig-Adams, B.; Adams, W. W. Photosynthesis: Harvesting sunlight safely. Nature 2000, 403, 371−374. (2) Edge, R.; McGarvey, D. J.; Truscott, T. G. The carotenoids as anti-oxidants: a review. J. Photochem. Photobiol., B 1997, 41, 189−200. (3) Polivka, T.; Frank, H. A. Molecular Factors Controlling Photosynthetic Light Harvesting by Carotenoids. Acc. Chem. Res. 2010, 43, 1125−1134. (4) Frank, H. A.; Cogdell, R. J. Carotenoids in Photosynthesis. Photochem. Photobiol. 1996, 63, 257−264. 430

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