Correlated Molecular Structural Motions for Photoprotection after Deep

Apr 19, 2018 - Longteng TangLiangdong ZhuYanli WangChong Fang. The Journal of Physical Chemistry Letters 2018 9 (17), 4969-4975. Abstract | Full Text ...
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Letter Cite This: J. Phys. Chem. Lett. 2018, 9, 2311−2319

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Correlated Molecular Structural Motions for Photoprotection after Deep-UV Irradiation Longteng Tang,† Yanli Wang,† Liangdong Zhu,† Che Lee,‡ and Chong Fang* Department of Chemistry, Oregon State University, Corvallis, Oregon 97331, United States

J. Phys. Chem. Lett. 2018.9:2311-2319. Downloaded from pubs.acs.org by UNIV OF SOUTH DAKOTA on 08/23/18. For personal use only.

S Supporting Information *

ABSTRACT: Exposure to ultraviolet (UV) light could cause photodamage to biomolecular systems and degrade optoelectronic devices. To mitigate such detrimental effects from the bottom up, we strategically select a photosensitive molecule pyranine and implement femtosecond electronic and Raman spectroscopies to elucidate its ultrafast photoprotection mechanisms in solution. Our results show that pyranine undergoes excited-state proton transfer in water, while this process is blocked in methanol regardless of excitation wavelengths (267, 400 nm). After 267 nm irradiation, the molecule relaxes from a higher lying electronic state into a lower lying singlet state with a 12 000 cm−1 more energy than the 400 nm photon while ESPT is allowed in water but inhibited in methanol, how HPTS can efficiently release such a large amount of excess energy and undergo various photoinduced processes without breaking the “hot” molecule apart is intriguing. To elucidate the excited state reaction coordinates, we first performed fs-TA to focus on the electronic dynamics for HPTS in water and methanol (MeOH) following actinic photoexcitation. In water, upon 400 nm irradiation (Figure 2a), a strong excited-state absorption (ESA) band centered at 535 nm rises promptly from PA* and then shifts toward the shorter wavelength, while a prominent stimulated emission (SE) band emerges at 523 nm, indicating the accumulation of PB* species as a result of ESPT.23 With the deep-UV excitation at 267 nm (Figure 2b), the fs-TA spectra of HPTS retain similar spectral patterns, confirming the occurrence of ESPT, but the ESA band of PA* reaches its intensity maximum after a few hundred femtoseconds and is blue-shifted to 515 nm in this case. Also, because we covered a broader detection window with our improved white light probe (see the SI), a 442 nm SE band is observed that is close to the fluorescence peak wavelength (i.e., S1 → S0 or PA* → PA near 434 nm; Figure 1a). The comparative results suggest that the delayed PA* state we detected in fs-TA with the 267 nm pump is still an S1 state but it is lower in energy than the S1 state accessed by the 400 nm pump.23 In other words, once an HPTS molecule is excited to Sn by the 267 nm light irradiation, it quickly slides out of the FC region and relaxes into a different S1 state or a different part of the same multidimensional S1 state from the one populated in the 400 nm excitation case, which for simplicity reasons during discussion we generally term as the S1′ state after deepUV/267 nm excitation. For HPTS in methanol (Figure 2c,d), the ESA band appears at almost the same position at 555 and 558 nm with the 400 and 267 nm excitation, respectively, different from the notable ESA band frequency shift in water. The spectral pattern in methanol after 267 nm excitation suggests that the solute molecule relaxes out of the FC region in Sn and reaches a very similar S1 state, while no significant proton transfer is allowed.18 No new SE band is developed at later time, confirming that the ESPT reaction is blocked in this case. Regardless of the excitation wavelength, the ESA band exhibits a blue shift in methanol, with an increased shift magnitude after 267 nm excitation (Figure 2d). The time constant of the ESA band center wavelength shift from fs-TA data after 400 nm excitation was reported to be ∼9.4 ps,30 attributed to the methanol molecule reorientation process (typical solvation time). The center wavelength of the ESA band after 267 nm excitation is plotted in Figure S1 with a single exponential fitting time

Figure 1. Steady-state electronic spectroscopy and schematic potential energy surfaces of HPTS in solution. (a) Normalized UV−vis (black) and fluorescence (color-coded) spectra of HPTS in water at pH 4.5 and methanol upon 400 and 267 nm photoexcitation. Two possible proton-transfer and energy dissipation pathways (orange and green arrows) are depicted in panels b and c for HPTS in water after 267 nm light irradiation (upward violet arrow) in the electronic excited-state manifold (e.g., S1, Sn) back to the ground state (S0).

sections near 400 and 267 nm (see the sample concentration choice in Supporting Information). Regardless of the excitation wavelength, the main spontaneous emission (i.e., fluorescence) band is at 510 and 434 nm in water and methanol, respectively. These steady-state spectroscopic results show that changing the pump wavelength from near UV to deep UV does not affect the 2312

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Figure 2. Semilogarithmic contour plot of fs-TA spectra of HPTS in (a) H2O with 400 nm pump, (b) H2O with 267 nm pump, (c) MeOH with 400 nm pump, and (d) MeOH with 267 nm pump. The positive ESA (red) and negative SE (blue) bands evolve on ultrafast time scales, with the dashed arrows highlighting the ESA peak wavelength shift (it could involve different excited state species such as PA* and PB* as shown). The signal intensity (delta optical density/ΔOD) contour color bars are shown on the right. The concentration of HPTS is 1.5 and 0.4 mM in both solvents with the 267 and 400 nm pump, respectively.

Figure 3. Time-resolved FSRS elucidates the photochemical/physical reaction coordinates. Semilogarithmic contour plots of 1.5 mM HPTS in (a) H2O and (b) MeOH after 267 nm photoexcitation show different vibrational dynamics. Raman gain (RG) is represented by the colorbar, and several marker bands are highlighted and labeled. Transient intensity plot of the characteristic (c) PA* 430 cm−1 and PB* 480 cm−1 modes in H2O and (d) PA* 430 cm−1 mode in MeOH. The retrieved time constants are denoted by the color-coded arrows.

constant of ∼9.1 ps, closely matching the aforementioned solvent reorientation time. Therefore, the solvent plays an important role in helping the photoexcited molecule to

dissipate energy in S1. Unlike the case of HPTS in methanol wherein the least-squares fit of the ESA peak shift leads to a good estimate of solvation time constant, the ESPT dynamics 2313

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The Journal of Physical Chemistry Letters in water are more complicated and cannot be accurately retrieved by fitting the ESA band shift due to a large overlap between the ESA and SE bands from diminishing PA* species and emerging PB* species. To address this issue, a detailed and accurate portrait can be unveiled by tracking the transient PA* and PB* vibrational marker bands in the electronic excited state.23,25 We therefore performed FSRS on HPTS in water and methanol after 267 nm photoexcitation. The contour plots of the time-resolved FSRS data are presented in Figure 3a,b. The excited-state Raman peaks in methanol are stronger than those in water, which could be explained by better resonance enhancement because our Raman pump at 580 nm is closer to the ESA band of HPTS in methanol (versus that in water; see Figure 2). In Figure 3a, several modes quickly reach their maximal intensity near 300 fs and then gradually decay, accompanied by the rise of some new peaks, supporting the PA* → PB* transition. In Figure 3b, because HPTS does not undergo ESPT in methanol, the PA* modes decay much slower with no obvious new peaks at later times. The rise of a mode at ∼578 cm−1 in methanol could be due to the formation of an HPTS−methanol S1 complex beyond the first solvation shell on the tens of picoseconds time scale.18 This mode is largely absent in the FSRS data with 400 nm actinic pump,30 which suggests that deep-UV excitation could promote the formation of this transient H-bonding complex with higher electric polarizability after the initial solvation process (see Figures S1 and S2 for the fs-TA peak wavelength and intensity dynamics) to help release the excess energy/heat from the chromophore. To reveal the PA* and PB* vibrational dynamics of HPTS in water, the time-resolved intensities of the 430 and 480 cm−1 modes after 267 nm excitation are plotted in Figure 3c. The 430 cm−1 PA* mode consists of the in-plane ring deformation based on the time-dependent density functional theory (TDDFT) calculation in Gaussian 09 software,31 and the mode shows a prompt rise and subsequent decay. The 480 cm−1 PB* mode is attributed to the ring out-of-plane (OOP) deformation of a deprotonated chromophore, which rises after a short dwell of ∼5 ps, indicating the existence of a distinct structural preparation stage for large-scale proton dissociation.17,23 Upon least-squares fit, the 430 cm−1 mode initial rise time constant of ∼300 fs could be attributed to the ultrafast Sn → S1′ transition (Figures 1b and 4) with concomitant electron and nuclear motions, in line with the proposed ultrafast nonradiative decay as an essential molecular survival mechanism in DNA bases.5 The biexponential decay time constants of 1.2 (50%) and 600 ps (50%) likely correspond to the solvent reorientation time (i.e., when HPTS is stabilized by the surrounding water molecules) and a long-time relaxation component, respectively. The PB* 480 cm−1 mode rises with a single-exponential time constant of 100 ps, which is slightly larger than the main ESPT reaction rate of ∼90 ps after 400 nm excitation, as reported in literature,17,26−28 including the observation of the same mode intensity rise in water.23 Therefore, the second decay time constant of 600 ps we observed in the 430 cm−1 mode (Figure 3c) cannot be just tracking ESPT, which instead could be attributed to the nonradiative relaxation of the remaining PA* species that does not donate a proton, so we can observe the large-scale H-bonding rearrangement/rotational diffusion of the still protonated chromophore and solvent molecules in the electronic excited state.27,32,33 This inability of undergoing ESPT can arise from the intrinsic structural inhomogeneity of a photoacid in solution, and, in addition, a specific subpopulation

Figure 4. Schematic excited-state pathways of HPTS in H2O after 267 nm photoexcitation. Anharmonic potential energy surfaces (black curves) are depicted with vibrational levels (horizontal bars). Vertical arrows represent the ground-state absorption (solid magenta, 267 nm), stimulated emission (dashed blue, 442 nm), excited-state absorption (dashed blue, 515 nm), nonradiative relaxation (wavy cyan, ∼600 ps time constant), and radiative relaxation (solid green, 510 nm). Internal conversion among transient PA* and PB* electronic states is shown by the semitransparent cyan arrows with the time constants listed. A different S1 state of PA* species after 400 nm photoexcitation is denoted by the dotted orange curve. The S1′ state could represent a different and lower-lying part of the S1 state prior to ESPT.

can be accessed by the incident laser pulses in FSRS with different wavelengths.6,34 Detailed excited-state processes of HPTS in water after 267 nm photoexcitation through the photochemical reaction are depicted in Figure 4. In comparison with the case of HPTS in water upon 400 nm excitation,14,17,23,35 the ESPT process we monitor under 267 nm laser irradiation exhibits some previously unknown distinct and interesting features. The synergistic data analysis and correlation from the electronic to vibrational domain enable us to investigate the pertinent structural motions and potential roles with reference to excited-state PESs illustrated in Figure 4. This experimental approach has been demonstrated as an effective strategy and powerful platform to enrich fundamental knowledge6,23,36 and guide practical applications.24,37 First, previous studies show that a contact-ion pair with charge-transfer character is formed between HPTS and a water molecule on the 2 to 3 ps time scale after 400 nm excitation,23,25−28 but this intermediate state is not observed after 267 nm excitation. Instead, a water solvation process is clearly observed (see Figure 3c). This could be due to the unique property of the newly discovered S1′ state, which does not require the formation of a contact-ion pair for ESPT. In other words, after HPTS relaxes from the initially populated Sn upon deep-UV excitation to the low-lying S1′ state, it may represent a more suitable PES to transfer the proton in comparison with the relatively higher lying S1 state reached after 400 nm excitation (Figure 4). Following the initial solvation process, the proton can be transferred effectively via a small energy barrier, leading to the PB* species accumulation on the ∼100 ps time scale as reported by the 480 cm−1 marker band (Figure 3c). Because the ESPT time constant after 267 nm excitation is very similar to that with the 400 nm pump (100 ps versus 90 ps) and the final PB* fluorescence state is 2314

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The Journal of Physical Chemistry Letters similar in both cases (see the almost identical fluorescence spectra in Figure 1a), the activation energy en route to PB* should be comparable regardless of the originating state of S1 or S1′. Second, a 420 cm−1 PA* mode is observed in FSRS after 400 nm excitation (in short, near-UV FSRS), which is 10 cm−1 lower than the 430 cm−1 mode in FSRS after 267 nm excitation (deep-UV FSRS). This result further indicates that the photoexcited molecule is in a different S1 state (i.e., S1′); otherwise, the Raman peak frequency in deep-UV FSRS is expected to be lower than 420 cm−1 because the molecule should first reach a hot vibrational level on the same S1 PES after relaxing down from Sn.38 Similarly, in methanol the PA* 420 cm−1 mode in near-UV FSRS is observed at 430 cm−1 in deep-UV FSRS, indicative of the involvement of a nearby S1′ state rather than the identical S1 state following excitation. Third, the 420 cm−1 mode in near-UV FSRS decays away with a 90 ps time constant, which matches the rise of the PB* 480 cm−1 mode, thus tracking ESPT.23 However, the 430 cm−1 mode in deep-UV FSRS exhibits clear intensity even after 600 ps (Figure 3a,c). Comparison between the fluorescence quantum yield (QY) of HPTS in water under two excitation wavelengths shows that the QY at 400 nm is ∼0.82 (ref 39) but ∼0.43 at 267 nm (measured in our lab), indicating that a notable amount of PA* population will not undergo ESPT after 267 nm irradiation and instead decay nonradiatively (Figure 4). In this case, excited-state FSRS can track the decay of the remaining PA* species on the ∼600 ps time scale with a sufficient signal-to-noise ratio, while the early portion of its dynamics could include contributions from the main ESPT process with the ∼100 ps time constant. Because a previous study showed that in bioluminescent organisms (e.g., fireflies) as well as human skin, the UVA light could promote the generation of reactive oxygen and nitrogen species and detrimental DNA photoproduct,40 our results on the photoacid pyranine show that the UVC light could enhance the nonradiative decay and reduce the potential intermolecular energy transfer and therefore mitigate the chemiexcitation to avoid biodamage. Notably, the 430 cm−1 mode of HPTS in methanol in deepUV FSRS rises with a 180 fs time constant, which is slightly shorter than 300 fs for HPTS in water and can be assigned to the Sn → S1 transition. This mode decays with an 8.1 ps (17% amplitude weight from the least-squares fitting) time constant, closely matching the 9.1 ps methanol reorientation time observed in fs-TA (Figure S1). The 1.1 ns (73%) time constant could arise from both radiative and nonradiative relaxation processes of HPTS in methanol (Figure S2). The fluorescence QY for HPTS in methanol with 267 nm excitation is measured to be 0.65, a bit smaller than the QY = 0.79 after 400 nm excitation.30,41 This is reasonable because the molecule rapidly relaxes into a very similar S1 state within 200 fs (corroborated by the fs-TA spectra in Figure 2c,d), and the excited-state population is mainly trapped in the PA* singlet state that emits blue fluorescence because ESPT is inhibited. While the mode intensity dynamics report on major temporal processes with population conversion, they could involve contributions from the change of resonance conditions and electric polarizabilities as the molecular system navigates the multidimensional PES.16,23 In comparison, transient mode frequency dynamics probe the reaction coordinate with more specificity and precision due to its vibrational quantum energy level nature in an anharmonic PES regardless of probing laser

wavelengths. Figure 5 presents the frequency dynamics of the 430, 680, and 1520 cm−1 marker bands of HPTS in water and

Figure 5. Excited-state vibrational frequency dynamics of the (a) 430, (b) 680, and (c) 1520 cm−1 mode of HPTS in H2O and MeOH on ultrafast time scales after deep-UV (DUV) and near-UV excitation. The multiexponential fits are color-coded in solid (267 nm excitation) and dashed (400 nm excitation) curves and overlaid with spectral data points. The pertinent atomic motions of each Raman mode are shown in the inset of each panel.

methanol after 267 and 400 nm photoexcitation. These characteristic vibrational mode frequency shifts far from equilibrium in the electronic excited state, when considered as a whole for direct comparison and in close correlation with each other, provide rich information about the photoprotection mechanism of HPTS under deep-UV irradiation. The 430 cm−1 mode red shifts in both solvents (water and methanol) with 267 nm excitation (Figure 5a), so this behavior is not directly related to ESPT. Because of the mode 2315

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whereas a similar magnitude of blue shift (677 to 688 cm−1, 11 cm−1) with a ∼130 ps time constant is observed after 400 nm excitation. The deviation from the main ESPT time constant can be understood as a “counteractive” competition between two ultrafast processes: chromophore distortion that leads to the mode frequency red shift and ESPT that results in the mode frequency blue shift.23,30,44 Therefore, an overall frequency shift time constant longer than ∼100 ps in Figure 5b is retrieved after 267 or 400 nm excitation of HPTS in water. In addition, a larger contribution from the chromophore distortion that further lengthens the apparent time constant (i.e., 170 ps >130 ps) is expected when significant excess energy is available from deep-UV excitation. Regarding a high-frequency marker band, we showed that HPTS in water with 400 nm excitation displays a blue shift (1527 to 1559 cm−1) of the ∼1530 cm−1 mode (ring CC stretching and phenolic COH rocking) as ESPT proceeds. However, the biexponential blue-shift time constants are ∼2.5 ps (34%) and 45 ps (66%), and the latter one is twice as fast as the main ESPT time constant of ∼90 ps.23 Upon changing the pump wavelength to 267 nm in water, the blue-shift trend (1500 to 1559 cm−1; see Figures 3a and 5c) holds but with a significantly increased magnitude. The excellent match of mode frequency (1559 cm−1) at 600 ps time delay after both excitation wavelengths confirms that the chromophore reaches the same PB* state. However, the retrieved time constants of ∼1.3 ps (53%) and 25 ps (47%) are still faster than main ESPT reaction, suggesting that this mode frequency dynamics not only tracks ESPT but also reflects vibrational cooling, which leads to the mode frequency blue shift in an anharmonic PES.25,45−47 As a control, the observed mode frequency dynamics in methanol corroborates our speculation. After 400 nm excitation, this mode shows a slight blue shift (1528 to 1530 cm−1, 2 cm−1), whereas after 267 nm excitation, the blue shift increases dramatically (1506 to 1525 cm−1, 19 cm−1). This makes sense because vibrational cooling should be more significant after the deep-UV (267 nm) excitation, which has much more energy than the near-UV (400 nm) light. Along the same line, the observed blue-shift time constants of the aforementioned 1530 cm−1 mode in water are shorter after deep-UV excitation than those after near-UV excitation (i.e., 1.3 < 2.5 ps, 25 < 45 ps), which confirms the increased “additive” contribution from vibrational cooling on various time scales48,49 (faster than the main ESPT time constant of ∼90 ps) when more excess electronic energy is available. Notably, other highfrequency Raman bands at 1137 and 1204 cm−1 in methanol also exhibit a blue shift (Figure 3b), suggesting that a number of localized atomic motions could facilitate the energy relaxation process through vibrational cooling with at least two channels on the few picoseconds and tens of picoseconds time scales. They are likely associated with intramolecular vibrational relaxation/energy relaxation within the first solvation shell and thermal energy transfer to the bulk solvent, respectively.23,25,49 Such a wealth of spectral information allows us to gain deep insights into how the chromophore responds to photoexcitation with significant excess energy. In particular, for HPTS in water, after the initial subpicosecond relaxation out of the FC region toward a lower lying electronic state, the water molecular reorientation time within the first solvation shell becomes dominant to stabilize the chromophore after deep-UV excitation. This important process is revealed by the 1.2 ps time constant from the PA* 430 cm−1 mode intensity decay (Figure

composition (in-plane ring deformation; see Figure 5a inset), it could be highly sensitive to structural changes of the chromophore. Although HPTS has a conjugated four-ring system, the ring coplanarity could be broken by some skeletal motions impulsively excited by the femtosecond actinic pump.16−18,23 The frequency shift magnitude of 3 cm−1 in methanol (430 to 427 cm−1) is smaller than 7 cm−1 in water (430 to 423 cm−1), which shows that methanol is a relatively bulky solvent and could restrict the chromophore motions to a larger extent than water. This red-shift trend holds for HPTS in water after 400 nm photoexcitation, but the shift magnitude of 4 cm−1 is reduced (420 to 416 cm−1), while no obvious shift is observed in methanol. A plausible explanation is that the deepUV excitation with higher photon energy can distort the chromophore more, thus leading to more significant frequency changes. The overall red-shift trend is consistent with a larger quantum box for the electron redistribution as the H-bonding network around the chromophore is rearranged in the photoexcited state. Besides dissipating photoexcitation energy in methanol, in the case of HPTS in water, the conformational change on ultrafast time scales could also help the chromophore to reach a more suitable geometry for ESPT reaction to the solvent.17,23,42 Moreover, the red shift of the 430 cm−1 mode of HPTS in water after 267 nm excitation can be fitted with a biexponential decay of 400 fs (32%) and 33 ps (68%). The first time constant has been attributed to some structural changes at the phenolic hydroxyl end,17,23 and the second time constant reflects further chromophore distortion on the tens of picoseconds time scale,16 which likely accompanies the thermal energy transport to bulk solvent for the remaining PA* species in the S1′ state in parallel with the ESPT reaction generating PB* species.23,25 In methanol, this mode exhibits a single exponential red-shift time constant of ∼150 ps after 267 nm excitation, indicative of some large-scale H-bonding network rearrangement.18,43 These contrasting results suggest that although the photoexcited chromophore deviates from the four-ring coplanarity in both solvents, the process shows different time constants with dependence on the solvent molecular properties including size, dielectric constant, viscosity, H-bonding strength, ESPT capability, and so on. Interestingly, in Figure 5b, the 680 cm−1 mode displays an opposite trend in water (blue shift) and methanol (red shift) after 267 or 400 nm excitation. Because this mode is a ring hydrogen-out-of-plane (HOOP) with small phenolic COH rocking motion (Figure 5b inset), the frequency red-shift behavior in methanol could be attributed to the chromophore distortion from the four-ring coplanarity, similar to the aforementioned 430 cm−1 mode in Figure 5a. Experimental support is as follows. First, the red-shift time constant is ∼140 ps, closely matching the red-shift time constant of the 430 cm−1 mode (∼150 ps) in deep-UV FSRS. Second, the red-shift magnitude of this mode after 267 nm excitation (681 to 678 cm−1, 3 cm−1) is larger than that after 400 nm excitation (674 to 673 cm−1, 1 cm−1), displaying the same trend as the 430 cm−1 mode. These results imply that the 680 cm−1 mode frequency red shift in methanol tracks the chromophore conformational dynamics. On the contrary, we have shown that adding acetate ions to methanol causes this mode frequency to blue shift, which is due to the ESPT reaction because acetate can accept the proton from HPTS even in methanol.30 The blue shift of this mode in water after 267 nm excitation (681 to 690 cm−1, 9 cm−1) is fitted with a 170 ps time constant, 2316

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conformational change and vibrational cooling become prominent in both solvents after irradiation by more energetic UV photons as we tune the 400 nm pump to 267 nm. We also reveal that after deep-UV excitation solvation of HPTS by adjacent water molecules on the ∼1 ps time scale serves as an effective relaxation channel for the chromophore moving out of the FC region, which differs from the ∼3 ps contact-ion formation after near-UV excitation, before the main ESPT step as the system undergoes further relaxation. These photoinduced processes are likely involved in photoprotection of biomolecules such as melanins and nucleobases. Moreover, our work highlights the multidimensional PESs from the first to higher lying electronic excited states. Molecular systems in nature evolve to protect themselves under many different circumstances by navigating alternative reaction paths on the nonequilibrium PESs after photoexcitation without accumulation of photodegraded species. For example, deep-UV irradiation pumps molecules to Sn, which could relax into a different S1 state or region to help dissipate energy more effectively therein instead of going through the same S1 state accessed by a near-UV or visible excitation. A higher starting point in the PES manifold likely allows molecules to undergo a different and efficient energy relaxation pathway versus that from a lower starting point, which are all governed by the light−matter interaction and molecular Hamiltonian including the system, the bath, and their interactions. Fortunately, the combination of fs-TA and FSRS with wavelength tunability opens the door to track the molecular evolution along the nonequilibrium potential energy landscape. These findings lead to new knowledge about the photoprotection mechanism of molecules under UV radiation, which could enrich the rational design principles to improve efficiency and durability of functional molecular machines like artificial light-harvesting complexes and organic solar cells.

3c) and substantiated by the 1.3 ps time constant from the 1530 cm−1 mode frequency blue shift (Figure 5c). The distinct solvation step with energy stabilization effect is in accord with the lower lying S1′ with respect to S1 (Figure 4), which also supports ultrafast vibrational cooling of the chromophore within the first solvation shell. In sharp contrast, after 400 nm excitation without a notable amount of excess energy, HPTS displays a time constant of 3 ps from the PA* 420 cm−1 mode intensity decay, corroborated by the time constant of 2.5 ps from the 1530 cm−1 mode frequency blue shift (Figure 5c).23 This specific process has been attributed to the formation of a contact-ion pair between HPTS and adjacent water molecules with charge-transfer character, which is a preparatory step beyond the ∼1 ps water reorientation time to facilitate efficient ESPT reaction from the PA* S1 state to the PB* fluorescent state (Figure 4). The overall importance of water motions along the energy dissipation pathways is consistent with a recent microsolvation study of a sunscreen chromophore, which forms a complex with water molecules after UVB excitation in promoting internal conversion back to the electronic ground state.7 As further kinetic analysis, after 400 nm excitation the same ∼1520 cm−1 marker band of HPTS in methanol (Figure 5c) shows a single exponential time constant of ∼13 ps but biexponential time constants of ∼370 fs (45%) and 34 ps (55%) after 267 nm excitation. Because ESPT is inhibited for HPTS in methanol, these time constants are associated with various energy relaxation channels including the FC dynamics within the HPTS−methanol H-bonding complex, methanol reorientation/solvation time, and thermal energy transfer to bulk solvent, on the order of increasing time constants.13,18,25 Moreover, the high-frequency modes likely contribute more to intramolecular and intermolecular vibrational cooling following photoexcitation, whereas the more delocalized low-frequency skeletal motions (both out-of-plane and in-plane) become increasingly susceptible to conformational dynamics as the vibrational mode frequency decreases further (e.g, Figure 5b to a). The site-specific addition or modification of functional groups (e.g., electron-withdrawing or -donating, hydrophilic) on or near the chromophore rings could then be an effective strategy in controlling photoacidity, ESPT, fluorescence, and other energy relaxation pathways.33,37 In particular, the fluorescence QY decreases after UVC excitation due to an enhancement of chromophore conformational dynamics and vibrational cooling (see Figure 5), as these atomic motions and processes likely facilitate nonradiative decay in solution environment. In summary, this advanced spectroscopic work provides a holistic view of the energy relaxation pathways of an organic molecule after UV irradiation and uncovers its intrinsic photoprotection mechanism starting from photoexcitation time zero. Depending on its local environment and incident photon energy, the molecule could select or enhance a certain pathway for energy dissipation. From a comprehensive investigation of transient Raman marker bands upon electronic excitation, we reveal that the photochemical reaction (particularly ESPT), solvent molecular reorientation, solute structural distortion (particularly breaking the conjugated ring coplanarity), and vibrational cooling all play an intricate and functional role on ultrafast time scales. The main photochemical reaction coordinate of ESPT (yes or no) is not affected by the wavelength of the UV radiation in the same environment (water or methanol). However, the chromophore

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ASSOCIATED CONTENT

* Supporting Information S

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.jpclett.8b00999. Sample preparation, femtosecond transient absorption (fs-TA), femtosecond stimulated Raman spectroscopy (FSRS), computational method, discussion of significance, Figures S1 and S2 on fs-TA dynamics of HPTS in methanol, additional references, and the full authorship of Gaussian 09 software (PDF)

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AUTHOR INFORMATION

Corresponding Author

*E-mail: [email protected]. Tel: 541-737-6704. ORCID

Longteng Tang: 0000-0001-9316-188X Chong Fang: 0000-0002-8879-1825 Present Address ‡

C.L.: Department of Chemical Engineering and Materials Science, University of Minnesota, Minneapolis, Minnesota 55455, United States. Author Contributions †

L.T., Y.W., and L.Z. contributed equally to this work.

Notes

The authors declare no competing financial interest. 2317

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ACKNOWLEDGMENTS This work is supported in part by the NSF CAREER grant (CHE-1455353), Oregon Medical Research Foundation New Investigator Grant (2016-2017), and OSU Research Equipment Reserve Fund (Spring 2014) to C.F. We thank Cheng Chen and Taylor Krueger for helpful discussions.

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