Ultrafast Nonradiative Relaxation Channels of Tryptophan - The

Letter pubs.acs.org/JPCL

Ultrafast Nonradiative Relaxation Channels of Tryptophan Virginia Ovejas,† Marta Fernández-Fernández,† Raúl Montero, Fernando Castaño, and Asier Longarte* Departamento de Quı ́mica-Fı ́sica, Facultad de Ciencia y Tecnologı ́a, Universidad del Paı ́s Vasco (UPV/EHU). Apart. 644, 48080 Bilbao, Spain S Supporting Information *

ABSTRACT: The nonradiative relaxation channels of gas-phase tryptophan excited along the S1−S4 excited states (287−217 nm) have been tracked by femtosecond time-resolved ionization. In the low-energy region, λ ≥ 240 nm, the measured transient signals reflect nonadiabatic interactions between the two bright La and Lb states of ππ* character and the dark dissociative πσ* state of the indole NH. The observed dynamical behavior is interpreted in terms of the ultrafast conversion of the prepared La state, which simultaneously populates the fluorescent Lb> and the dissociative πσ* states. At higher energies, after excitation of the S4 state, the tryptophan dynamics diverges from that observed in indole, pointing to the opening of a relaxation channel that could involve states of the amino acid part. The work provides a detailed picture of the processes and electronic states involved in the relaxation of the molecule, after photoexcitation in the near part of its UV absorption spectrum. SECTION: Spectroscopy, Photochemistry, and Excited States

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The spectrum was composed of the vibronic transitions of different stable conformers, whose individual contributions have been separated in studies.15,16 However, very limited spectroscopic information of the states lying above Lb is available, and thus, theoretical calculations have been a crucial tool to achieve the actual knowledge of the electronic structure of the molecule. In this sense, a decisive contribution has been the identification of the dark πσ* states.17,18 In the last years, these states have been detected in numerous simple aromatic chromophores, and their crucial role in complex photochemical phenomena as proton/electron transfer processes is starting to be understood.17,19 For indole-containing species, the lowest predicted πσ*-type state results in the promotion of a π electron into the 3s orbital of the pyrrolic nitrogen atom, presenting a repulsive surface along the N−H stretching coordinate that drives the ultrafast nonradiative relaxation of the molecule. Recent frequency and time-resolved works have characterized the πσ* state of indole, which is located immediately above the La state.20−23 In the case of tryptophan, although calculations predict a similar location,8 to the best of our knowledge, no experimental evidence of this πσ* state has been collected for the neutral form. It is worth mentioning that, on the other hand, several works have explored the fragmentation patterns of protonated tryptophan, demonstrating the involvement of πσ* states of the amino group, which in the neutral species appear at much higher energies.24,25 In this study, we have examined the evolution of the system in the 287−217 nm excitation region, which covers the location of the S1(Lb), S2(La), S3(πσ*), and S4(ππ*) states. The

ryptophan, the main light-absorbing amino acid, permits peptides and proteins to be efficiently photoexcited by UV light.1 For long, its fluorescence has been extensively used as a probe of protein structure and dynamics, raising great interest to understand the electronic structure of the molecule and the photopysical behavior derived from it.2−4 However, the collected observations reveal that tryptophan is far from a simple light-emitting molecule, especially when the interaction with the solvent in the condensed phase is considered. The interplay of different electronic excited states, induced by the coupling between electronic and vibrational degrees of freedom, gives rise to intricate photochemical pathways of nonradiative nature.5,6 The detailed description of these mechanisms in small building blocks as tryptophan is the starting point for their understanding in bigger scale systems as polypeptides and proteins, where they are fundamental steps of any light-induced phenomena.7 Tryptophan shares with its aromatic chromophore, the indole ring, the low electronic structure. Two ππ* state transitions named Lb (S1) and La (S2) form the two lowest singlet excited states of the amino acid.3,8 While in the gas phase the Lb state is located below La, the larger dipole moment of the latter (5.86 versus 1.86 D) induces a preferential stabilization that leads to an order reversal in aqueous media, where La is considered to be the emitting state.3 The La and Lb states are strongly coupled, forming a conical intersection (CI) whose dynamical signature has been observed in aqueous solutions.9−11 In contrast with the vast amount of studies in condensed media, just a few number of works have focused on the neutral electronic spectroscopy of the molecule in the gas phase, mainly due to the difficulties to evaporate the intact substance.12−16 The pioneering works by Levy and collaborators12−14 provided the first spectra of tryptophan’s Lb electronic state, whose origin was located at ∼34875 cm−1. © 2013 American Chemical Society

Received: April 17, 2013 Accepted: May 23, 2013 Published: May 23, 2013 1928

dx.doi.org/10.1021/jz400810j | J. Phys. Chem. Lett. 2013, 4, 1928−1932

The Journal of Physical Chemistry Letters

Letter

relaxation dynamics of gas-phase tryptophan, evaporated in an oven placed at the exit of the pulsed valve, was tracked by timeresolved femtosecond ionization26 (see Figure 1). Fundamen-

Figure 1. Schematic representation of the employed pump and probe wavelengths (energies), together with the electronic structure of tryptophan. Figure 2. Transients recorded at the tryptophan+ mass channel with the indicated excitation and the 1365 nm probe. The red trace and circles are the experimental data and the best obtained fit, respectively. (a) Black and blue traces correspond to the individual components. The phenol+ 1 + 5′ nonresonant ionization signal (crosses and gray line) is employed as a reference. (b) Green and blue traces are the individual exponential components of the fitting. The ethene+ 1 + 7′ nonresonant signal (crosses and gray line) is used as a reference.

tally, after preparing the molecule along a chosen resonance of the absorption spectrum, the population transferred to the excited state is probed by multiphoton ionization. In this way, by registering the tryptophan ion intensity as a function of the pump−probe delay, a time-dependent signal that reflects the evolution of the excited states is obtained. For the present work, a pure exponential fit was applied to model the transient signals recorded. The use of mass-resolved methods is a great advantage to track the ultrafast dynamics of molecules that, as occurs with tryptophan, are difficult to evaporate in the intact form. A typical mass spectrum recorded at the conditions of the experiment has been included in the Supporting Information (SI). Figure 2 shows the transients collected in the tryptophan+ mass channel, exciting in the lower-energy portion of the electronic spectrum, at 287 and 280 nm. Two different probe wavelengths were employed in these measurements, 800 and 1365 nm. The decays recorded with the 1365 nm probe wavelength at 287 and 280 nm exhibit in both cases a long-lived background, which reflects the nanoseconds lifetime of the lower Lb state. The 287 nm signal contains also a small τ0 = 0 fs Gaussian contribution that can be attributed to nonresonant ionization or out-of-resonance adiabatic excitation of the molecule,27 in any case, not related to excited-state dynamics. However, the fit of the 280 nm transient (Figure 2b) yields in addition a τ2 = 49 ± 10 fs lifetime. This τ2 time component, present in the transients collected in the 280 ≥ λ ≥ 250 nm range can be firmly attributed to the ultrafast internal conversion (IC) between the La and Lb ππ* states of the indole ring. Consequently, assuming that, as was found for indole, the La/Lb crossing is located near the bottom of the La well,28,29 λ = 280 nm can be taken as the onset of the La state absorption. The La/Lb coupling dynamics in tryptophan, compared to that recently characterized for the indole molecule,22,23 shows a great similarity, denoting, as expected,

the very small influence of the amino acid part on the π orbitals involved. As has been established in indole, the coupling is presumably driven by a CI promoted by out-of-plane vibrational coordinates of the indole ring.28,29 The transients recorded with the 800 nm probe have been included in the SI as Figure 3s. On the contrary to what was observed with the 1365 nm probe, these decays do not show the La → Lb IC lifetime, τ2. A detailed discussion on this effect, attributed to the different sensitivities of both probes, has also been incorporated in the SI. The excitation region from 280 to 250 nm, which covers the absorption of the La state, was explored by using also the 800 and 1365 nm probes. With the exception of the τ2 lifetime, absent from the 800 nm transients (see SI Figure 3s), the same dynamical behavior was observed with both probes. The transients collected (Figure 3) are characterized by the appearance, at wavelengths shorter than ∼272 nm, of a τ3 = 360−210 fs lifetime. According to previous observations in indole22,23 and on the grounds of theoretical predictions,8 this lifetime can be assigned to dynamics involving the dissociative πσ* state of the indole ring. This state, besides driving the dissociation of the molecule forming hydrogen atoms, is also connected to the ground state through a S3 πσ*/S0 CI promoted by out-of-plane vibrations of the ring. Consequently, the relaxation along the πσ* surface simultaneously leads to the ultrafast formation of H atoms and a hot ground state. The transients collected in this excitation region with the 1365 nm 1929



Letter

Figure 3. Decays collected at the tryptophan+ mass channel (circles) with the 1365 nm probe, together with the best multiexponential fit obtained (red line). The green, orange, and blue lines correspond to the individual exponential components. The ethene+ nonresonant ionization signal (crosses and gray line) is used as the zero delay time reference.

probe (Figure 3a and b) show, additionally to the τ3 lifetime, the τ2 fs decay already observed at longer wavelengths, which corresponds to the La/Lb IC. The simultaneous observation of both processes can be explained in terms of the laser excitation of the bright La state, followed by the competing relaxation toward the Lb and πσ* states. The two couplings, La/Lb and La/ πσ*, are very likely mediated by CIs promoted by orthogonal vibrational modes. These two relaxation channels have been characterized for the indole molecule in recent studies.22,23 We would like to highlight that, although the τ3 lifetime is clearly related to the πσ* state, our data do not reveal the exact nature of this process. The measured τ3 decay could reflect the La → πσ* IC or, alternatively, the loss of ionization once the system has reached this surface. The observation of either one or the other process will depend once again on the change of the ionization cross section associated with each mechanism. The fact that our data do not show any temporal constant ascribable to the La → πσ* IC could be due to a negligible change in the ionization cross section along the process. Alternatively, it is also possible that if both relaxation channels, La → πσ* and La → Lb occur at similar rates, the measured τ2 ≈ 30 fs lifetime results from the sum of both. By moving the excitation to shorter wavelengths, the absorption of the La state vanishes, and the tryptophan+ decay collected at 240 nm (Figure 4a) is a Gaussian that matches the ethene+ reference signal. The transient is a consequence of the reduced absorption of the molecule at this wavelength30 because no permanent population is transferred to the excited state by the pump laser.27 As the energy is further

Figure 4. (a) Transient recorded at the tryptophan+ channel (red line and circles) with the 800 nm probe, compared to the ethene+ reference signal (blue line and crosses). The tryptophan signal is slightly broader due to the different order of the ionization process, 1 + 2′ versus 1 + 4′ for ethene. (b) Tryptophan+ decay (red line and circles) registered with the 800 nm probe and fitted with a single exponential, along with the ethene+ reference signal (gray line and crosses). (c) Decay collected for indole+ (circles) with the 800 nm probe, fitted by a multiexponential function (red line). The green, orange, and blue lines correspond to the individual exponential components.

increased, the excitation starts to overlap an intense absorption, and the decays show an ultrafast time of τ4 = 31 ± 5 fs (Figure 4b). In order to rationalize this dynamical behavior, transients were also registered for indole (Figure 4c) in this energy region, which had not been explored in previous works. The comparison of both sets of data reveals that, on the contrary to what has been found at lower energies, the dynamics of tryptophan completely differs from that of indole. Calculations predict that the intense absorption with maximum at around 210 nm observed in indole is caused by a strong S4 ππ* transition. In principle, it may be assumed that the state 1930



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energies, λ ≤ 218 nm, is the opening of relaxation channels that could involve electronic states of the amino acid part detected. The study also demonstrates how ultrafast time-resolved techniques with wavelength tuning, guided by accurate theoretical predictions, are a powerful tool to obtain detailed information on increasingly complex models of real biological systems. As a following step, we aim to investigate the photophysics of larger size peptide models, paying special attention to the nonradiative channels resulting from the peptide chain−chromophore interaction and to the existence of conformer-specific dynamics.

responsible for the absorption in this region has a very similar nature in both cases. The indole decay recorded after exciting the S4 state (Figure 4c) exhibits, in addition to the τ4 = 19 ± 6 fs lifetime of this state, the τ3 = 126 ± 26 fs component corresponding to the S3 πσ*, together with a long-lived background τ1 = 333 ± 126 ps. This transient signal supports the idea of a consecutive relaxation pathway S4 → La, followed by the simultaneous IC toward the πσ* and Lb states. On the other hand, the ionization signal of tryptophan’s S4 state drops to zero with a single τ4 = 31 ± 5 fs lifetime, revealing a different route that does not involve the lower ππ* states. Owing to the almost nonexistent information on the electronic structure of tryptophan above S3, it is a complicated task to rationalize the exact relaxation pathway followed by the system from S4. However, on the basis of the comparison with indole, it is plausible to invoke the intervention of excited states of the amino acid backbone. Spectroscopic measurements on glycine and alanine,31 well supported by theoretical calculations,32 find that the two lowest excitations, no → π*CO and nn → 3s, lie close to this energy region. The coupling of the prepared bright ππ* state to any of these two surfaces along a barrierless pathway could be responsible for the measured τ4 = 19 ± 6 fs lifetime. This kind of interaction has been recently postulated as responsible for driving nonradiative relaxation channels in model dipeptides containing aromatic chromophores.7 In view of the flexible nature of tryptophan, it is important to make a brief comment about the dependence of the observed dynamics on the different conformations available to the molecule.16,33 Because of the pick-up method employed to incorporate the molecules into the beam (see Experimental Section and SI), we cannot estimate the final degree of cooling achieved, but it was presumably very poor. Attempts to record a high-resolution spectrum with a nanosecond laser across the region of the S0 → S1 origin were made, but no vibronic features were observed, only a broad unresolved absorption. In these conditions, where the molecule can explore large portions of the potential energy surface, it is complicated to derive any conclusion regarding the dynamics of specific conformations. However, although it is clear that the measured lifetimes result from a distribution of different conformers,33,34 the fact that the observed photophysics can be interpreted in terms of the indole molecule seems to exclude the existence of a significant number of conformers, with a photophysical behavior divergent of the one presented by the bare chromophore. In this sense, the comparison of the data presented here with those derived from the narrow conformer distribution formed in a supersonic expansion could be highly instructive. In summary, the carried out experiments provide a comprehensive view on the processes and the electronic states involved in the electronic relaxation of the tryptophan amino acid, along a wide portion of its absorption spectrum. The timedependent signals collected at increasing excitation energy contain several ultrashort lifetimes that can be associated with different nonradiative relaxation channels. The analysis of these data permits understanding of the photophysical properties of the molecule after excitation to the bright La state in terms of two main competitive relaxation pathways, the La → Lb IC leading to the well-known fluorescent emission and the La/πσ* coupling that promotes the ultrafast nonradiative channels mediated by the repulsive πσ* state. The work clearly shows a direct correlation between the photochemistry of tryptophan and that of its indole chromophore, revealing the role of the πσ* state in the neutral amino acid. Only at high excitation

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EXPERIMENTAL SECTION The experimental setup, described in detail elsewhere,35,36 is based on a time-of-flight linear spectrometer, where the gaseous samples are introduced in the form of a supersonic expansion. In the case of tryptophan, the solid sample was heated up to 473 K in a small glass oven attached to the front end of the nozzle of a Series Nine General Valve (see SI Figure 1s). The evaporated tryptophan molecules were picked up by the He beam coming out of the nozzle. Femtosecond laser pulses were generated by an oscillatorregenerative amplifier commercial system (Mira-Legend UPS). The pump pulses were tuned in the 287−217 nm wavelength range by different interactions (see ref 36) that involved the signal beam of an OPA (optical parametric amplifier). As probe beams, the 800 nm fundamental or the signal of the OPA at 1365 nm was used. The pump and probe beams were collinearly focused on the interaction region to reach intensities of around 109 and 1012−1013 W/cm2, respectively. In order to measure the cross-correlation and to establish precisely the zero delay time, the ethene nonresonant 1 + n′ ionization signal was collected simultaneously to the tryptophan ion. For the 287 and 280 nm transients, a phenol nonresonant ionization signal was employed instead of ethene. Typically, values between 60 and 80 fs were obtained for the instrument response functions at the different excitation wavelengths.

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ASSOCIATED CONTENT

S Supporting Information *

Extended description of the vaporization method employed. Additional decays collected with the 800 nm probe. Discussion on the influence of the probe wavelength on the observed dynamics. 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]. Phone ++34 946018086. Fax: + + 34 946013500. Author Contributions †

V.O. and M.F.-F. contributed equally to the work.

Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS V.O. and M.F. thank the Basque Government and the Spanish MINECO for their respective fellowships. This work was financed by Spanish MINECO under the CTQ2010-17749 grant and the Consolider Program “Science and Applications of Ultrafast Ultraintense Lasers” CSD2007-00013 and by the Basque Government through the “Ayudas para apoyar las 1931



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actividades de grupos de investigación del sistema universitario vasco”. The experiments were carried out at the SGIker laser facility of the UPV/EHU.

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Ultrafast Nonradiative Relaxation Channels of Tryptophan - The

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