Hydrogen Bond Donors Accelerate Vibrational Cooling of Hot

Article pubs.acs.org/JPCA

Hydrogen Bond Donors Accelerate Vibrational Cooling of Hot Purine Derivatives in Heavy Water Yuyuan Zhang, Jinquan Chen, and Bern Kohler* Department of Chemistry and Biochemistry, Montana State University, Bozeman, Montana 59717, United States ABSTRACT: Natural nucleobases and many of their derivatives have ultrashort excited state lifetimes that make them excellent model systems for studying intermolecular energy flow from a hot solute molecule to the solvent. UV-pump/broadband-midIR-probe transient absorption spectra of canonical purine nucleobases and several xanthine derivatives were acquired in D2O and acetonitrile in the probe frequency range of 1500− 1750 cm−1. The spectra reveal that vibrationally hot ground state molecules created by ultrafast internal conversion return to thermal equilibrium in several picoseconds by dissipating their excess energy to solvent molecules. In acetonitrile solution, where hydrogen bonding is minimal, vibrational cooling (VC) occurs with the same time constant of 10 ± 3 ps for paraxanthine, theophylline, and caffeine within experimental uncertainty. In D2O, VC by these molecules occurs more rapidly and at different rates that are correlated with the number of N−D bonds. Hypoxanthine has a VC time constant of 3 ± 1 ps, while similar lifetimes of 2.3 ± 0.8 ps and 3.1 ± 0.3 ps are seen for 5′-adenosine monophosphate and 5′-guanosine monophosphate, respectively. All three molecules have at least two N−D bonds. Slightly slower VC time constants are measured for paraxanthine (4 ± 1 ps) and theophylline (5.1 ± 0.8 ps), dimethylated xanthines that have only one N−D bond. Caffeine, a trimethylated xanthine with no N−D bonds, has a VC time constant of 7.7 ± 0.9 ps, the longest ever observed for any nucleobase in aqueous solution. Hydrogen bond donation by solute molecules is proposed to enable rapid energy disposal to water via direct coupling of high frequency solute−solvent modes. subpicosecond S1 lifetimes in aqueous solution.8 These findings are similar to those for the canonical purines.10−13 It is important to consider the rate and mechanism of energy dissipation to the solvent because the threat of photodegradation does not end when the S0 state is first reached. At the instant an excited molecule passes through a conical intersection to S0, almost the entire photon energy resides in the ground state molecule as excess vibrational energy. This poses a potential risk, and experiments conducted under collision-free conditions have documented various dissociation channels for nucleobases.14−16 In solution, the solvent environment accepts the excess photon energy by intermolecular energy transfer (IET).17 The overall process by which a solute molecule with excess vibrational energy returns to thermal equilibrium is known as vibrational cooling (VC). Previous UV-pump/UV−visible-probe TA experiments on 9methyladenine have shown that the thermally equilibrated ground state is reached with time constants of 2.4, 4.5, and 13.1 ps in water, methanol and acetonitrile, respectively.18 Fast VC in water was rationalized by the number and strength of the solute−solvent hydrogen bonds, which have been suggested to facilitate vibrational energy transfer from the photoexcited chromophore to the surrounding solvent environment.18

1. INTRODUCTION Xanthine derivatives, including hypoxanthine, theophylline, theobromine, paraxanthine, and caffeine, are derivatives of purine and close relatives of the canonical DNA bases adenine and guanine. Oxidative deamination of adenine yields hypoxanthine, a mutagen that pairs with cytosine instead of thymine.1 Guanine deamination, however, produces xanthine, which can base pair with a broad array of natural and synthetic bases.2,3 Theophylline, theobromine, and paraxanthine are dimethyl-substituted xanthines, whereas the well-known stimulant caffeine is 1,3,7-trimethylxanthine. Theophylline and theobromine also exist in various plants and are pharmaceutically active.4 The role of xanthine and hypoxanthine in the prebiotic world has attracted much attention.5,6 Along with their molecular recognition properties, the ultrashort excited state lifetimes now observed for several xanthine derivatives7−9 suggest that these modified nucleobases may have been sufficiently photostable to survive the intense UV irradiation at the surface of the early Earth. UV-pump/visible-probe transient absorption (TA) studies have shown that hypoxanthine, theophylline, theobromine, paraxanthine, and caffeine have S1 lifetimes ranging from 130−540 fs in aqueous solution as a result of deactivation via S1/S0 conical intersections (CI).7 Inosine and its monophosphate salt IMP, the nucleoside and nucleotide of hypoxanthine, respectively, were also reported to have © 2013 American Chemical Society

Received: April 22, 2013 Revised: June 26, 2013 Published: July 1, 2013 6771

dx.doi.org/10.1021/jp4040002 | J. Phys. Chem. A 2013, 117, 6771−6780

The Journal of Physical Chemistry A

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Figure 1. Transient absorption spectra at selected pump−probe delay times following 265 nm excitation of D2O solutions of (a) 7.6 mM AMP (in 100 mM DPO42−/D2PO4− buffer, pD = 7.4); (b) 10 mM GMP (in 100 mM DPO42−/D2PO4− buffer, pD = 7.5); (c) saturated hypoxanthine (unbuffered, pD = 6.7); (d) 6.7 mM caffeine (unbuffered, pD = 7.7, no ionizable proton); (e) 5.5 mM paraxanthine (unbuffered, pD = 5.8); and (f) 6.7 mM theophylline (unbuffered, pD = 6.5). The baseline at t < 0 ps (gray) is included to mark ΔA = 0. Atomic numbering is shown for guanine and caffeine for convenience. The frequencies for the kinetic traces shown in Figure 2 are indicated in this figure by curved arrows.

2. EXPERIMENTAL SECTION The 265 nm pump wavelength (λpump) was generated by a white-light-seeded, two-stage optical parametric amplifier (OPerA Solo, Coherent). The OPA was pumped by 1 W of the 800 nm fundamental (3.5 W, 80 fs, 1 kHz) from a TiSapphire regenerative amplifier (Libra HE, Coherent). The prerequisite 530 nm was produced by sum-frequency mixing of a portion of the 800 nm beam with the signal beam at 1570 nm. The visible pulse was subsequently frequency-doubled to generate the deep-UV pump pulse. The arrival time of the pump beam was varied by a 60 cm translation stage, providing a maximum pump−probe time delay of ∼4 ns with a resolution of ∼8 fs. The pump pulses were attenuated to 1.5−3.5 μJ and focused to a spot size of 450−600 μm (fwhm) at the sample. An optical chopper operating at 500 Hz blocked every other pump pulse in order to measure the transmission of the probe with and without the pump (see eq 1 below). Mid-IR probe pulses were generated at ṽ = 1626 cm−1 (6150 nm) and 1667 cm−1 (6000 nm) for experiments in D2O and acetonitrile, respectively, using a second optical parametric amplifier (TOPAS-C, Light Conversion) that was pumped by 800 mW of the laser fundamental. The resulting signal and idler pulses were subsequently mixed noncollinearly in a GaSe crystal for difference frequency generation (NDFG, Light Conversion). Typically, 8−10 mW of mid-IR pulses with a bandwidth of 150−200 cm−1 were produced. A pair of CaF2 holographic wire-grid polarizers controlled the polarization and power of the probe pulses. The electric field vector of the mid-

Here, we report UV-pump/broadband-mid-IR-probe TA studies of 5′-adenosine monophosphate (AMP), 5′-guanosine monophosphate (GMP), hypoxanthine, and a series of methylated xanthines in acetonitrile and D2O (H2O is unsuitable due to its strong absorption in our spectral window). These compounds were selected because they all undergo ultrafast internal conversion (IC),7 a prerequisite for observing VC dynamics, and because the extent of methylation determines the number and types of hydrogen bonds with solvent molecules, interactions that are proposed to strongly affect vibrational energy transfer from solute to solvent. By directly probing the vibrational states following photoexcitation, this technique potentially provides a mode-specific view of how excess energy is dissipated to the solvent environment. Mid-IR probing is often preferable to UV−visible probing because the electronic transitions monitored with the latter methods usually result in broad and overlapping bands. For example, previous transient absorption experiments on the same class of molecules with excitation at 266 nm and probing at 250 nm yielded positive signals for all samples except hypoxanthine.7 The positive signals, which are a consequence of electronic absorption by hot ground state molecules, obscure the negative bleach recovery signals that probe all time scales needed for a molecule to return to the thermally equilibrated ground state following photoexcitation. To the best of our knowledge, the time-resolved vibrational spectra for hypoxanthine, paraxanthine, theophylline, and caffeine are reported for the first time. 6772



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Figure 2. Bleach recovery kinetics for (a) adenine ring vibration at 1623 cm−1; (b) guanine carbonyl stretch at 1662 cm−1; (c) hypoxanthine carbonyl stretch at 1673 cm−1; and (d−f) carbonyl stretch for methylated xanthines at ∼1640 cm−1. All data were obtained in D2O. The points are experimental data. The lines are the best exponential decay fit determined in Igor Pro. Only time constants (τ) larger than 1 ps are reported. Uncertainties associated with the time constants are 2× standard deviation. Vertical dashed−dotted lines denote the linear−logarithmic break.

were prepared in D2O (Cambridge Isotope Laboratories) or acetonitrile (Sigma-Aldrich). All chemicals were used as received. AMP and GMP solutions in D2O were adjusted to neutral pH with 100 mM D2PO4−/DPO42− buffer, whereas the hypoxanthine, paraxanthine, theophylline, and caffeine solutions were unbuffered. The pD values of unbuffered solutions were measured and found to range from 5.8 to 7.5. pD values were determined using the standard formula, pD = pH + 0.4, where pH is the reading made with a calibrated pH electrode.

IR probe and pump were set to magic angle (54.7°), and the power was attenuated to no more than 200 μW at the sample. The probe beam was divided into two, approximately equalpower portions by a 3 mm ZnSe beam splitter placed before the sample. The first portion, denoted “signal”, was focused to a spot size of ∼300 μm (fwhm) at the sample and overlapped with the pump pulse. The second portion, denoted “reference”, was also focused to the same spot size at the sample but vertically displaced by 7.5 mm below the signal beam. The reference was used to normalize the signal in order to reduce the effects of pulse-to-pulse noise. The signal and reference beams were recollimated after the sample and focused into an f = 190 mm spectrograph (Triax, Horiba) with a 0.75 mm entrance slit. The spectrometer was calibrated using known water vapor absorption frequencies. Frequencies are accurate to within 3−4 cm−1 in our probing range of 1500−1750 cm−1. Signal and reference beams were dispersed by a 100 lines/mm grating blazed for 6000 nm and projected onto a liquid nitrogen-cooled, dual-row 64-element (pixel) Mercury−Cadmium−Telluride detector (Infrared Systems Development). The lower row was used to measure the signal beam, while the top row was used to measure the reference beam. The absorbance change (ΔA) was calculated from the signal intensity I recorded at each pixel in the respective detector rows using the following equation: ⎛ Isignal,pump off /Ireference,pump off ⎞ ⎟⎟ ΔA = log⎜⎜ ⎝ Isignal,pump on /Ireference,pump on ⎠

3. RESULTS Figure 1a,b displays the TA spectra for AMP and GMP in D2O solution in the fingerprint region (1540 ≤ ṽ ≤ 1725 cm−1) following deep UV excitation (λpump = 265 nm). The TA spectra are similar to those recorded by Kuimova et al.,19 Towrie et al.,20 and Nielsen et al.21 The negative signals have center frequencies matching those observed in the FT-IR spectra, confirming that they originate from ground state bleaching. The 1623 cm−1 band for AMP is assigned to an adenine ring vibration.19,22,23 A similar assignment can be made for the 1571 cm−1 band observed in GMP (guanine ring vibration), whereas the 1662 cm−1 band is assigned to the carbonyl stretch (vCO).19,21−23 Two-dimensional IR experiments have shown that the vibrational modes in the fingerprint region are highly coupled;23 thus, the mode assignments discussed here refer to the dominant character of a particular mid-IR absorption band. Single wavelength fits to the bleach recovery signals for AMP and GMP at the band center frequencies yield time constants of 2.3 ± 0.8 and 3.1 ± 0.3 ps, respectively (see Figure 2a,b).24 Positive signals on the lower frequency side of the bleach signals are also observed. These features shift to higher frequencies as delay time increases and decay on a comparable time scale. Both the positive and negative signals completely disappear by t ≈ 15 ps after which time only a constant negative offset is observed across the TA spectrum. The pump pulse

(1)

The sample of interest was flowed through a 100 μm path length flow cell with CaF2 windows. The front window was thinner than the back (1 vs 2 mm) in order to minimize dispersive pulse broadening of the UV pump pulse. A total sample volume of 2 mL was recirculated at a linear flow rate of 0.1 m/s in order to minimize re-excitation. Five to 10 mM or saturated solutions of AMP, GMP, hypoxanthine, paraxanthine, theophylline, and caffeine (all obtained from Sigma-Aldrich) 6773



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Figure 3. Transient absorption spectra at the indicated pump−probe delay times following 265 nm excitation of acetonitrile solutions of (a) 7.6 mM caffeine and (b) 9.4 mM theophylline. The frequencies plotted in Figure 4a are indicated by arrows. The thick dashed line in each panel denotes ΔA = 0.

Figure 4. Bleach recovery kinetics for the carbonyl stretch (vCO) of methylated xanthines in (a) acetonitrile (single frequency kinetics at ∼1665 cm−1) and (b) D2O solution (single frequency kinetics at ∼1640 cm−1).

three methylated xanthines. The lower energy band, centered at ∼1640 cm−1, originates from one of the carbonyl stretch modes (vCO). However, the assignment of the higher energy band at ∼1695 cm−1 is uncertain. A combined FT-IR, Raman, and theoretical study assigned this peak to a CN stretch associated with ring in-plane vibration,27 but a later study assigned it to the second carbonyl stretch.26 We favor the carbonyl stretch assignment as the center frequencies of these two bands are remarkably similar to the two carbonyl stretches observed for uracil.22 Both bands exhibit identical kinetics in our TA experiments (data not shown). Bleach recovery kinetics at ∼1640 cm−1 for caffeine, paraxanthine, and theophylline in D2O are shown in Figure 2d−f, respectively. Although all three bleach signals can be fitted with single exponential functions, the time constants for theophylline and caffeine (5.1 ± 0.8 and 7.1 ± 0.9 ps, respectively) are significantly longer than those observed for adenine, guanine, and hypoxanthine (2−3 ps) in the same solvent. Caffeine in particular exhibits a recovery time at least twice as long as the canonical purine bases. Figure 3a,b displays the TA spectra in the range of 1580 ≤ ṽ ≤ 1770 cm−1 for caffeine and theophylline, respectively, in acetonitrile solution following 265 nm excitation. The spectra are similar in shape to those measured in D2O, but the twin peaks seen in this window are shifted to higher frequency, as seen in both the FT-IR and TA spectra. Furthermore, the ∼1665 cm−1 band assigned to one of the carbonyl stretches is slightly narrower than in D2O solution. The positive feature at the lower frequency edge of this ground state band is also narrower. Paraxanthine has a TA spectrum that closely

induces a weak temperature jump in the solvent, resulting in the difference spectrum at long times due to temperaturedependent mid-IR absorption by D2O.25 TA spectra of hypoxanthine in D2O solution following 265 nm excitation are displayed in Figure 1c at select pump−probe delay times. Once again, the center frequencies of the negative signals match ones seen in the FT-IR spectra. On the basis of combined theoretical studies and FT-IR measurements,26 the 1673 cm−1 feature originates predominantly from the carbonyl (C6O) stretch. The carbonyl stretch of GMP occurs at a similar frequency, supporting this assignment. The positive feature in the TA spectrum lies at a slightly lower frequency than the negative signal and shifts toward the band center as delay time increases. The rise, shift, and decay kinetics are similar to those observed for the canonical purines (see TA spectra shown in Figure 1). The bleach recovery for hypoxanthine at band center, as shown in Figure 2c, is well described by a single exponential function with a time constant of 3 ± 1 ps, which is identical to the lifetimes observed for adenine and guanine within experimental accuracy. It is noteworthy that at longer time delays (e.g., t > 15 ps) both positive and negative features have decayed completely, indicating that there are no long-lived excited electronic states. A negative offset was observed across the TA spectrum at t > 15 ps, which is again due to the heating of the D2O solvent as described above. Methylated xanthines have distinctive double-peak spectra between 1625 and 1725 cm−1 (see Figure 1d−f). The band centers of these two peaks occur at identical frequencies for all 6774



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Table 1. Excited State (S1) Lifetimes and Vibrational Cooling (VC) Lifetimes of Canonical Purines and Selected Xanthine Derivatives in Aqueous and Acetonitrile Solution number of H-bondsa VC lifetimes S1 lifetimes

acceptor donor D2O CH3CN H2O CH3CN

AMP

GMP

hypoxanthine

paraxanthine

theophylline

caffeine

3 (15) 2 (3) 2.3 ± 0.8 ps 13.1 ± 0.1 psb 290 ± 40 fsc 0.4 ± 0.1 psb

4 (15) 3 (3) 3.1 ± 0.3 ps

4 2 3 ± 1 ps

460 ± 40 fsc

130 ± 20 fsd

5 1 4 ± 1 ps 10 ± 3 ps 220 ± 20 fsd 0.8 ± 0.1 psd

5 1 5.1 ± 0.8 ps 10 ± 3 ps 540 ± 60 fsd 1.7 ± 0.1 psd

5 0 7.7 ± 0.9 ps 10 ± 3 ps 480 ± 50 fsd 1.3 ± 0.1 psd

a

Total number of solute−solvent hydrogen bond donor and acceptor sites. For AMP and GMP, only the purine chromophore is considered. The numbers in parentheses indicate the additional hydrogen bond counts for the ribose and phosphate groups. bReference 18, 9-methyladenine. c Reference 10, purine nucleoside. dReference 7.

fingerprint region are expected to reside in the vibrational ground state (v = 0) because the thermal energy provided by the environment is insufficient to populate excited states of these moderately high frequency vibrations. The bleach recovery time scale depends in principle on both the excited state lifetime and the rate of vibrational cooling. Vibrational cooling is the process by which the photoexcited molecule dissipates vibrational energy in excess of the thermal average and returns to thermal equilibrium with its surroundings. The initial vibrational energy distribution in the solute is nonthermal because internal conversion is thought to concentrate the excess vibrational energy in a small number of accepting modes. IET is obviously necessary for VC, but intramolecular vibrational redistribution (IVR) can also contribute to the rate of VC. In solvent-assisted IVR,17 solvent molecules accept energy from the solute to enable energyconserving transitions between vibrational states of the solute. IVR can also promote VC by directing energy from the high frequency modes populated by internal conversion to low frequency solute modes that can more efficiently channel excess solute vibrational energy to the solvent due to the increased solvent friction at low frequencies (vide infra). A conventional ansatz for vibrational energy relaxation in large polyatomic molecules like the size of the ones in this study is that IVR occurs more rapidly than energy transfer to the solvent (IET).28,29 Some studies of polyatomic molecules support this separation of time scales,30−33 while others report that IVR and IET occur concurrently.34−36 Exactly how IVR occurs in an associated solvent such as D2O is unclear. In addition, the experiments described here cannot differentiate IVR from IET because we monitor only a small number of modes in the fingerprint region. Thus, we use the term vibrational cooling (VC) to refer to the overall process in which the photoexcited molecule dissipates vibrational energy in excess of the thermal average and returns to thermal equilibrium with the solvent without inferring the relative rates (and importance) of IVR and IET. Considering that the S1 lifetimes of the canonical and alternate bases are subpicosecond in D2O (Table 1), the bleach recovery kinetics at t > 1 ps are determined by the rate of vibrational energy transfer to D2O. A highly vibrationally excited ground state is created as a result of ultrafast IC, which deposits almost all of the photon energy into vibrations. The vibrationally hot molecule subsequently returns to the thermally equilibrated ground state with time constants of 2 to 8 ps in D2O. Although the S1 lifetimes of the alternate bases are up to ∼4× longer in acetonitrile than in aqueous solution (Table 1), the ground state of each recovers with an even longer time constant of 10 ± 3 ps (with negative amplitude),

resembles those of caffeine and theophylline (data not shown). The kinetics of the carbonyl stretch at ∼1665 cm−1 for the acetonitrile solutions of caffeine and theophylline show marked differences from those in D2O solution, and the bleach recovery kinetics can no longer be described by a single exponential function. Figure 4a displays the bleach recovery kinetics for paraxanthine, theophylline, and caffeine in acetonitrile solution. These bleach signals recover with a time constant of 10 ± 3 ps (negative amplitude), but a faster, positive amplitude with a ∼4 ps time constant is also needed to fully describe the recovery at early time (only experimental data points are shown in Figure 4). Interestingly, side-by-side comparison of Figure 4a,b clearly shows that the variation in the bleach recovery time observed in D2O is not observed in acetonitrile. The following discussion will focus on the different kinetics observed in D2O and acetonitrile.

4. DISCUSSION The principal experimental observations are summarized as follows. Negative and positive signals are observed in all the TA spectra of canonical and alternate purine bases following 265 nm excitation. The positive signals exhibit complex spectral and temporal evolution, which can be qualitatively described as “rise, blue-shift, and decay”. Despite this complexity, the decay times of the positive signals are commensurate with the recovery of the negative signals within experimental error. In D2O, the negative signals recover faster, and the kinetics can be fully described by a single exponential function. The methylated xanthines return to thermal equilibrium more slowly than AMP and GMP. Furthermore, 1,3,7-trimethylxanthine (caffeine) has a bleach recovery time of 7.7 ± 0.9 ps in D2O, which is almost twice as long as that of 1,7-dimethylxanthine (paraxanthine). To the best of our knowledge, 7.7 ps is the longest vibrational cooling lifetime observed to date for any monomeric nucleobase in aqueous solution. Note that the excited state lifetime of caffeine is 480 fs,7 which is very similar to GMP, yet the bleach recovery by GMP occurs 2.5 times faster with a time constant of 3.1 ± 0.3 ps (see Table 1). In acetonitrile, on the other hand, the negative signals decay much more slowly, and all three methylated xanthines have similar bleach recovery times (10 ± 3 ps). As mentioned previously, the center frequencies of the negative signals observed in all TA spectra agree well with the positions of steady-state absorption bands in the FT-IR spectra and thus can be unambiguously assigned to ground state bleaching. The initial bleach immediately following photoexcitation and its subsequent recovery signify the removal from and return to the thermally equilibrated ground state, respectively. At room temperature, vibrational modes in the 6775



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hypothesize that the directionality of hydrogen bond interactions with solvent molecules (hydrogen bond acceptor vs donor) is an important factor as discussed below. We first consider whether the range of VC times observed for the canonical and alternate purine bases can be explained by variation in the strength of hydrogen bonds. We only consider the carbonyl group because calculations on the monohydrate of the biologically relevant 9H-guanine have predicted that the C6O···H−O−H hydrogen bond is stronger than other hydrogen bonds including the bond to the amino group (N− H···OH2).43−45 In order to estimate the relative CO···D− O−D hydrogen bond strengths for the methylated xanthines in D2O, we consider the CO stretching frequencies determined from the FT-IR spectra. Analogous to O−H stretch modes,41 the CO stretch is sensitive to the hydrogen bond environment. The CO stretch band red shifts and broadens when the local oscillator is weakened by the solute−solvent hydrogen bond. In D2O, the two bands assigned to CO stretch modes (vide infra) have similar center frequencies for all methylated xanthines investigated, suggesting that hydrogen bonds between CO and water molecules are of similar strength and independent of methylation patterns. It is noteworthy that these two CO stretch modes are observed at higher vibrational frequencies in acetonitrile where hydrogen bonding is minimal, supporting the notion that the CO stretching frequency serves as an indicator of the strength of the CO···D−O−D hydrogen bond. The similar CO stretch frequencies observed for all compounds thus rule out variation in carbonyl−water hydrogen bond strengths as an explanation for the different VC times observed for the methylated xanthines in D2O. Next, we consider whether the VC rate is correlated with the total number of hydrogen bonds. As summarized in Table 1, the total number of hydrogen bonds is nearly constant across the series of molecules studied, excluding hydrogen-bonding sites not located on the base moiety (AMP and GMP). No correlation between VC lifetimes and the total number of hydrogen bonds for each solute is found. For example, caffeine has only one fewer hydrogen bond than hypoxanthine and the other methylated xanthines, but its VC lifetime is almost twice as long. VC by caffeine occurs only slightly faster in D2O than in acetonitrile (7.7 ± 0.9 vs 10 ± 3 ps). This is surprising considering that the total number of hydrogen bonds is substantial in D2O, but near zero in acetonitrile, which is only a weak hydrogen-bond acceptor. The behavior of caffeine in D2O and acetonitrile raises questions about the influence of hydrogen bond directionality on VC dynamics. We first consider the role of hydrogen bond acceptors. Solute hydrogen bond acceptors for the molecules in this study include the oxygen atoms in the carbonyl groups and the nitrogen atoms in the pyrimidine and imidazole rings. Caffeine has five hydrogen bond accepting sites, the same number as the dimethylated xanthines, theophylline, and paraxanthine. Furthermore, the five hydrogen bond acceptor sites are the same for all three molecules: four acceptor sites are provided by the carbonyl O atoms and one by a ring N atom. Despite these similarities in hydrogen bond accepting properties, the VC times for these methylated xanthines differ by a factor of 2 from longest to shortest, suggesting that hydrogen bond acceptors in these molecules do not play a primary role in mediating vibrational energy flow from solute to solvent.

similar to that observed for 9-methyladenine in acetonitrile (13.1 ps).18 This indicates that vibrational energy transfer from the solute to the aprotic solvent is rate determining. The positive component with a ∼4 ps time constant, which causes the deviation from single exponential recovery, may be due to decay of the S1 state (1−2 ps, see Table 1). Another possibility is that the carbonyl stretch acts as an IVR accepting mode that accepts energy from higher frequency modes. This is supported by the ∼4 ps IVR lifetime seen in a similar-sized molecule, pnitroaniline, in DMSO.37 The large uncertainty in the time scale of this positive component coupled with lack of knowledge about relaxation by lower frequency modes precludes a more definitive assignment. Further evidence of the hot ground state lies in the positive features observed in the TA spectra. For all bases investigated, positive features located on the low-frequency side of the bleach signal manifest common rise, blue-shift, and decay kinetics. The rise is due to the initial generation of the hot ground state. In principle, the rise time constants should match the excited state lifetimes summarized in Table 1, but the instrument response time of our experiment precludes accurate determination of these subpicosecond time constants, so they are not reported. Anharmonicity on the ground state potential energy surface is responsible for the dynamic blue shift, which signifies cooling by the hot ground state.38 Lastly, the decay times of positive signals are comparable to the bleach recovery times, further supporting the hot ground state assignment. Assignment of these positive features to vibrational modes in an excited electronic state is ruled out because the subpicosecond rise is far too slow to be excited state absorption by the S1 state population, which would appear instantaneously upon photoexcitation. Additionally, the positive bands decay many times more slowly than excited state deactivation (see Table 1 for S1 lifetimes). We propose that the kinetics of bleach recovery are dictated by the time required to transfer excess vibrational energy to the solvent after the solute molecule has returned to its electronic ground state. In D2O, the canonical purine bases eliminate excess energy with remarkable speed (2−3 ps). What factors influence the rate of VC? Middleton et al.18 observed accelerated cooling of 9-methyladenine in H2O/D2O vs acetonitrile and proposed that hydrogen bonding facilitates the energy flow from the solute to the solvent. Earlier, UVpump/broadband-UV−visible-probe experiments32 and transient grating experiments39 showed that dimethylation of the amino group of p-nitroaniline significantly slows down the VC in various protic solvents, but not in acetonitrile. Furthermore, the lifetime of the vibrationally excited (v = 1) O−H stretch of HOD in D2O increases from 0.7 to 0.9 ps as the temperature increases from 298 to 363 K.40 This observation was ascribed to the weakening of the solute−solvent hydrogen bond at higher temperature, which subsequently decreases the anharmonic coupling between the high frequency O−H stretch and the lowfrequency modes in the O−H···O coordinate.40−42 A major aim of this study is to obtain deeper insight into the role played by hydrogen bonds on VC dynamics. Although VC by relatively large polyatomic molecules is known to occur more rapidly in aqueous solution than in organic solvents,18,32 the observations described here reveal that markedly different cooling rates can be observed in aqueous solution for different members from a family of closely related molecules. These differences are proposed to arise from variation in the number and type of hydrogen bonding interactions. Specifically, we 6776



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energy transfer. The N−D stretch frequency of the nucleobases at approximately 2500 cm−1 (ref 53) is nearly resonant with the O−D stretch of the solvent. The N−D groups are also associated with bending and scissoring modes at ∼1200 cm−1,54 which are approximately resonant with the D2O bend. Furthermore, these frequencies are approximately half as large as the N−D and O−D stretch fundamentals, suggesting that excitation in the latter modes could decay to the first overtone of these bending vibrations. All of these resonant pathways benefit from strong coupling due to hydrogen bonds and can contribute to the overall rate of energy dissipation to the solvent. In contrast to the excellent solute−solvent frequency matching in D2O, N−H stretch and bend modes in the nucleobases are out of resonance with the vibrational frequencies of acetonitrile and thus do not accelerate VC in this aprotic solvent. Moreover, there is no significant overlap between peaks in the FT-IR spectra between the nucleobases and acetonitrile in the fingerprint region. The absence of high and medium frequency solvent modes that are in resonance with solute modes and the lack of strong solute−solvent couplings suggest that VC rates will not be enhanced by the number of N−H groups. Indeed, the bleach recovery times observed for paraxanthine, theophylline, and caffeine in acetonitrile are identical (10 ± 3 ps; Table 1 and Figure 4a). This time constant agrees well with the VC time of 13.1 ps measured for 9-methyladenine in the same solvent in UVpump/UV-probe transient absorption experiments.18 In acetonitrile, which lacks resonant energy transfer pathways, it seems plausible that the high frequency solute modes populated by ultrafast internal conversion undergo slower decay via IVR to lower frequency solute modes that are energy matched to the large number of solvent modes. Hydrogen bonds are expected to strongly couple solute and solvent vibrations. Both the hydrogen bonds themselves and the mid- and high-frequency modes coupled to them have large anharmonicities, and anharmonicity is crucial for rapid vibrational relaxation of high frequency modes.47 Nevertheless, strong coupling is not the whole story as seen by the lack of correlation between VC rates and the presence of nucleobase hydrogen bond acceptors. These groups have characteristic frequencies near 1600 cm−1, which fall between the bend and stretch modes of D2O. This reinforces the hypothesis that hydrogen bond donors of these bases are capable of resonant energy transfer to high frequency solvent modes. In fact, Table 1 shows that the cooling rate is weakly anticorrelated with the number of hydrogen bond acceptors. Hydrogen bond acceptor sites of the solute have lower vibrational frequencies than the N−D stretch and may serve as accepting modes for vibrational energy from the hot solvent. It is possible that these hydrogen bonds could retard VC by allowing the back transfer of vibrational energy from hot water molecules in the first solvation shell of the solute. Resonant transfer of vibrational energy has been observed in neat water.55−57 One quantum of the O−H stretching vibration in H2O is transferred in approximately 80 fs.55,56 The corresponding energy transfer time in D2O is 400 fs.57 Of course, there could be better frequency matching for these identical oscillators than for the N−D and D2O modes mentioned earlier. However, calculations by Lawrence and Skinner illustrate that substantial detuning from resonance can be accommodated.49 These authors showed that the lifetime of the v = 1 state of the O−D stretch of HOD in D2O decreases

N−D bonds in the solutes studied here donate hydrogen bonds to water molecules. These bonds appear to play a major role in facilitating VC as seen from the observed VC times in D2O (Table 1). The canonical purine bases, adenine and guanine, and hypoxanthine each have at least two N−D bonds, and these three compounds exhibit the shortest VC time constants in D2O. Longer VC time constants are observed for the dimethylated xanthines that have only one N−D bond. Caffeine, which possesses no N−D bonds due to methylation at the N1, N3, and N7 positions, has the longest VC time constant of all and the longest value observed for any nucleobase in aqueous solution. The fact that VC by caffeine is only modestly faster in D2O than in acetonitrile (7.7 ± 0.9 vs 10 ± 3 ps) is consistent with enhanced vibrational energy transfer by the other purine derivatives via one or more N−D bonds. The finding that xanthines with a greater number of N−D bonds undergo more rapid vibrational cooling points to important relaxation pathways involving the relatively high frequency modes (ℏω ≫ kBT) that involve these bonds. It is surprising that a small number of high frequency solute modes could exert such a strong influence on IET in these relatively large molecules. In the Landau−Teller or perturbation theory description of vibrational energy relaxation in liquids, the rate of relaxation is proportional to the square of the coupling multiplied by the power spectral density of the time correlation function describing the fluctuating forces exerted by solvent molecules on the solute vibration of interest.17,46,47 The latter quantity is known as the friction, and the relaxation rate depends on its value at the frequency difference between the initial and final vibrational states of the solute. The spectral density for water47−49 decays approximately exponentially with increasing frequency as observed for other molecular liquids. Consequently, the friction exerted by the solvent on solute vibrations is greatest in the low frequency region. These concepts underlie the conventional wisdom that IET proceeds primarily via energy transfer from relatively low frequency solute modes to low frequency modes of the solvent.17,46,50,51 West et al. reported accelerated vibrational cooling by the thymine chromophore when a ribose group is present and attributed this observation to an increase in molecular size and the concomitant increase in low frequency modes.52 In contrast, we see no systematic increase in cooling rates with the number of vibrational degrees of freedom. For example, hypoxanthine has 36 normal modes, caffeine has 66, while AMP has an even greater number when modes of the ribose and phosphate group are counted. If a greater count of low frequency modes is all that is needed for faster energy transfer to the solvent, then the VC lifetimes should increase in the order AMP < caffeine < hypoxanthine. Instead, our observations show that hypoxanthine and AMP have similar VC lifetimes in D2O within experimental uncertainty, even though AMP has many more low frequency modes. Furthermore, caffeine cools more slowly than hypoxanthine despite having a greater number of low frequency modes. The apparent increase of the rate of VC with molecular size in the experiments of West et al.52 could be due to the 85:15 methanol/water solvent used in that study. It is possible that the high methanol content slows IET enough in those experiments to increase the importance of energy dissipation via low frequency modes. We propose that high frequency modes associated with N−D bonds of the nucleobases efficiently dissipate excess vibrational energy to high-frequency solvent vibrations via (near) resonant 6777



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bond fission could occur on the ground state surface if sufficient quanta are excited in the bond-stretching coordinate. The risk of photofragmentation is much higher for an isolated molecule, e.g., in outer space, but fortunately a solvent provides a sink, which can effectively receive the extra energy from the solute. Thus, the UV hardiness of alternate bases is likely to also depend on how fast vibrational energy can be dissipated to the surrounding environment. Water, where every biologically and physiologically important reaction takes place, gives the fastest VC rate for the canonical bases compared to all other solvents.12,18 Adenine and guanine dissipate the vibrational energy with a time constant of 2−3 ps in D2O. Hypoxanthine exhibits comparable VC time scales. However, the methylated xanthines, especially caffeine, have longer hot ground state lifetimes in D2O, which could make them more susceptible to UV-initiated thermal chemistry. Combined with the fact that its excited state lifetime is the shortest ever observed among canonical and alternate purine bases,7 hypoxanthine is suggested to have a high degree of photostability. To the best of our knowledge, damaging photoreactions such as photohydration have not been reported for hypoxanthine. In contrast, both 5-methylcytosine62 and uracil63 undergo photohydration, which can ultimately lead to genome damage. If alternate xanthine bases were available in prebiotic times,64−68 then the selection of today’s canonical purine bases over hypoxanthine as a genetic information carrier must have an explanation beyond UV hardiness.

from 18 ps in simulations with rigid solvent molecules to 390 fs with a flexible solvent model that allows for intermolecular vibrational energy transfer. Inclusion of internal vibrations of the solvent molecules greatly increases the solvent friction in the vicinity of the O−D stretch. Significantly, the friction is enhanced at least 500 cm−1 above and below the O−D stretch frequency, suggesting that this mode can readily deactivate solute vibrations over a broad frequency interval through creation of a quantum of solvent stretch excitation and one or more quanta of low frequency bath modes. The reliability of perturbation theory and even the invocation of normal modes may be suspect at the high internal energies produced by internal conversion, but we expect that calculations like these nonetheless capture much of the basic physics. In order for resonant energy transfer from a small number of high frequency solute modes to high frequency solvent modes to measurably affect VC rates, the former modes must contain a substantial fraction of the total excess vibrational energy. The kinetics of these modes are not monitored in this study, but their initial excitation is reasonable based on Franck−Condon arguments and the large amount of excess vibrational energy (∼38 000 cm−1) present in the molecule following nonradiative decay to the electronic ground state. High frequency modes can accept a large amount of this energy in a small number of vibrational quanta. Of course, the high frequency solute modes that are initially excited upon internal conversion must also maintain their excitation long enough for IET to the solvent to take place. This suggests that IVR in the electronic ground state takes place more slowly than energy transfer to the solvent for these chromophores. Earlier, it was suggested that IVR by formamide following ultrafast internal conversion from an excited electronic state with nearly 6 eV of energy may not be competitive with ultrafast energy transfer to the solvent.36 Vibrational modes with frequencies of 1200 cm−1 and higher have negligible excited state populations in fully thermalized molecules the size of the nucleobases, even with 38 000 cm−1 of excess energy. In other words, if IVR were much faster than IET, VC rates should not depend on high-frequency solute modes as observed in this study. Further work is needed to understand the accepting modes for internal conversion by the nucleobases, but timeresolved Raman experiments have indicated that the initial distribution of vibrational energy can remain nonthermal for many picoseconds following internal conversion by 4-nitroaniline.37 Lastly, we wish to comment on how the VC dynamics could influence the UV hardiness of these alternative purine nucleobases. It was previously determined that the excited states of hypoxanthine7−9 and the methylated xanthines7 deactivate via S1/S0 CIs back to the ground state with near 100% efficiency on a time scale that is comparable to, if not faster than, those of the canonical purine bases. Ultrafast internal conversion provides a basis for UV resistance, which may have been particularly important under conditions of strong UV irradiation in the prebiotic world before the advent of an ozone layer.58−61 The very same mechanism that reduces the risk of photochemistry taking place on the electronically excited state surface, however, converts a large amount of the photon energy to vibrational energy and significantly increases the internal temperature of the molecule to more than 1000 K.13 The thermal chemistry of the alternate bases in vibrationally hot ground states is generally unclear, but X−H (X = N, O, S)

5. CONCLUSIONS Time-resolved vibrational spectra of UV-excited hypoxanthine and three methylated xanthines were studied in D2O and acetonitrile solution by broadband-mid-IR transient absorption spectroscopy. The experiments directly interrogate the VC dynamics of the various bases. Although these closely related molecules contain comparable amounts of excess energy, they exhibit very different VC rates in the same solvent. In D2O, hypoxanthine dissipates excess vibrational energy to the solvent just as efficiently as the canonical purine bases, but the methylated xanthines exhibit slower VC. The VC time of 7.7 ps observed for caffeine is longer than any previously reported value for a vibrationally hot nucleobase in D2O. Furthermore, this time constant approaches the relaxation time observed for this solute in acetonitrile, showing that the ability of water to accelerate VC has been largely frustrated by the type and nature of the intermolecular hydrogen bonds. Hydrogen bond donors accelerate VC, while hydrogen bond acceptor groups do not. This asymmetry is suggested to arise because solute modes associated with the former hydrogen bonds are resonant with several high frequency vibrational modes of the D2O solvent. This study demonstrates that tuning the number of solute N−D bonds directly affects the rate of vibrational cooling. Slower rates are found in solutes with fewer N−D bonds, suggesting that the high frequency vibrations associated with N−D bonds play an important role in transferring excess vibrational energy to water. Near resonances with solvent modes and strong solute−solvent couplings due to hydrogen bonds are two factors that are likely to facilitate ultrafast intermolecular vibrational energy transfer. The importance of resonant energy transfer is underscored by the observation of slower and approximately equal cooling times for these solutes in acetonitrile, where high-frequency acceptor modes are absent. These results suggest that solute-to-solvent energy transfer can relax a significant fraction of excess vibrational 6778



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(13) Kohler, B. Nonradiative Decay Mechanisms in DNA Model Systems. J. Phys. Chem. Lett. 2010, 1, 2047−2053. (14) Nielsen, S. B.; Andersen, J. U.; Forster, J. S.; Hvelplund, P.; Liu, B.; Pedersen, U. V.; Tomita, S. Photodestruction of Adenosine 5 ′-Monophosphate (AMP) Nucleotide Ions in Vacuo: Statistical Versus Nonstatistical Processes. Phys. Rev. Lett. 2003, 91, 048302. (15) Worm, E. S.; Andersen, I. H.; Andersen, J. U.; Holm, A. I. S.; Hvelplund, P.; Kadhane, U.; Nielsen, S. B.; Poully, J. C.; Stochkel, K. Photodissociation of Dinucleotide Ions in a Storage Ring. Phys. Rev. A 2007, 75, 042709. (16) Marcum, J. C.; Halevi, A.; Weber, J. M. Photodamage to Isolated Mononucleotides−Photodissociation Spectra and Fragment Channels. Phys. Chem. Chem. Phys. 2009, 11, 1740−1751. (17) Elles, C. G.; Crim, F. F. Connecting Chemical Dynamics in Gases and Liquids. Annu. Rev. Phys. Chem. 2006, 57, 273−302. (18) Middleton, C. T.; Cohen, B.; Kohler, B. Solvent and Solvent Isotope Effects on the Vibrational Cooling Dynamics of a DNA Base Derivative. J. Phys. Chem. A 2007, 111, 10460−10467. (19) Kuimova, M. K.; Dyer, J.; George, M. W.; Grills, D. C.; Kelly, J. M.; Matousek, P.; Parker, A. W.; Sun, X. Z.; Towrie, M.; Whelan, A. M. Monitoring the Effect of Ultrafast Deactivation of the Electronic Excited States of DNA Bases and Polynucleotides Following 267 nm Laser Excitation Using Picosecond Time-Resolved Infrared Spectroscopy. Chem. Commun. 2005, 1182−1184. (20) Towrie, M.; Doorley, G. W.; George, M. W.; Parker, A. W.; Quinn, S. J.; Kelly, J. M. ps-TRIR Covers All the Bases: Recent Advances in the Use of Transient IR for the Detection of Short-Lived Species in Nucleic Acids. Analyst 2009, 134, 1265−1273. (21) Nielsen, J. B.; Thøgersen, J.; Jensen, S. K.; Nielsen, S. B.; Keiding, S. R. Vibrational Dynamics of Deoxyguanosine 5 ′-Monophosphate Following UV Excitation. Phys. Chem. Chem. Phys. 2011, 13, 13821−13826. (22) Banyay, M.; Sarkar, M.; Gräslund, A. A Library of IR Bands of Nucleic Acids in Solution. Biophys. Chem. 2003, 104, 477−488 and references therein. (23) Peng, C. S.; Jones, K. C.; Tokmakoff, A. Anharmonic Vibrational Modes of Nucleic Acid Bases Revealed by 2D IR Spectroscopy. J. Am. Chem. Soc. 2011, 133, 15650−15660. (24) All bleach recovery kinetics of canonical and alternate purines in deuterated water are fit to biexponential decay functions with a constant offset at longer time. The first component has a positive amplitude and a time constant shorter than 1 ps (not included in this report). The build-up of the bleach signal is due to the time resolution of our instrument. The second component has a negative amplitude and picosecond lifetime, which originates from vibrational cooling. The third component is a constant offset due to the spectral change in the solvent at an elevated temperature. (25) Schreier, W. J.; Schrader, T. E.; Koller, F. O.; Gilch, P.; CrespoHernández, C. E.; Swaminathan, V. N.; Carell, T.; Zinth, W.; Kohler, B. Thymine Dimerization in DNA Is an Ultrafast Photoreaction. Science 2007, 315, 625−629. (26) Shanmugasundaram, M.; Puranik, M. Computational Prediction of Vibrational Spectra of Normal and Modified DNA Nucleobases. J. Raman Spectrosc. 2009, 40, 1726−1748. (27) Gunasekaran, S.; Sankari, G.; Ponnusamy, S. Vibrational Spectral Investigation on Xanthine and Its Derivatives−Theophylline, Caffeine and Theobromine. Spectrochim. Acta, Part A 2005, 61, 117− 127. (28) Nitzan, A.; Mukamel, S.; Jortner, J. Energy Gap Law for Vibrational Relaxation of a Molecule in a Dense Medium. J. Chem. Phys. 1975, 63, 200−207. (29) Elsaesser, T.; Kaiser, W. Vibrational and Vibronic Relaxation of Large Polyatomic Molecules in Liquids. Annu. Rev. Phys. Chem. 1991, 42, 83−107. (30) Laermer, F.; Elsaesser, T.; Kaiser, W. Ultrashort Vibronic and Thermal Relaxation of Dye Molecules after Femtosecond Ultraviolet Excitation. Chem. Phys. Lett. 1989, 156, 381.

energy in relatively large polyatomic molecules via high frequency modes, revealing a distinctly quantum mechanical character to vibrational cooling in aqueous solution. They also hint that high frequency stretch and bend modes associated with solute hydrogen bond donors are a key to the rapid thermalization of excess vibrational energy. Both concepts are worthy of further experimental and theoretical exploration.

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AUTHOR INFORMATION

Corresponding Author

*(B.K.) E-mail: [email protected]. Tel: +1 406994-7931. Fax: +1 406-994-5407. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS This work was made possible by grants from the National Science Foundation ( CHE-11 1256 0) and NASA (NNX12AG77G). We thank Prof. Kimberly de La Harpe (U.S. Air Force Academy) and MSU undergraduates Marie Beitelshees and Benjamin Smith for their help constructing the experimental apparatus.

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REFERENCES

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Hydrogen Bond Donors Accelerate Vibrational Cooling of Hot

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