Electron-Driven Proton Transfer Along H2O Wires Enables

Letter pubs.acs.org/JPCL

Electron-Driven Proton Transfer Along H2O Wires Enables Photorelaxation of πσ* States in Chromophore−Water Clusters Rafał Szabla,*,† Jiří Šponer,†,‡ and Robert W. Góra*,¶ †

Institute of Biophysics, Academy of Sciences of the Czech Republic, Královopolská 135, 61265 Brno, Czech Republic CEITECCentral European Institute of Technology, Masaryk University, Campus Bohunice, Kamenice 5, CZ−62500 Brno, Czech Republic ¶ Theoretical Chemistry Group, Institute of Physical and Theoretical Chemistry, Wrocław University of Technology, Wybrzeże Wyspiańskiego 27, 50-370 Wrocław, Poland ‡

S Supporting Information *

ABSTRACT: The fates of photochemically formed πσ* states are one of the central issues in photobiology due to their significant contribution to the photostability of biological matter, formation of hydrated electrons, and the phenomenon of photoacidity. Nevertheless, our understanding of the underlying molecular mechanisms in aqueous solution is still incomplete. In this paper, we report on the results of nonadiabatic photodynamics simulations of microhydrated 2-aminooxazole molecule employing algebraic diagrammatic construction to the second order. Our results indicate that electron-driven proton transfer along H2O wires induces the formation of πσ*/S0 state crossing and provides an effective deactivation channel. Because we recently have identified a similar channel for 4-aminoimidazole-5-carbonitrile [Szabla, R.; et al. Phys. Chem. Chem. Phys. 2014, 16, 17617−17626], we conclude this mechanism may be quite common to all heterocyclic compounds with low-lying πσ* states.

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possible nonradiative deactivation channels of this molecule in the gas phase, proceeding either via ring puckering motion and direct intersection with the ground state or two consecutive intersections with low-lying πσ* state due to amino N−H bond stretching.11 Similar photorelaxation mechanisms were previously reported for isolated biologically relevant chromophores like imidazole, pyrrole, and phenol and for biomolecules like adenine, histidine, tyrosine, and tryptophan.1,4,16−18 The N−H bond fission mechanism, however, must be significantly altered in aqueous solution. Our recent study of the photochemistry of microhydrated 4-aminoimidazole-5carbonitrile compound (AICN) provides an initial glimpse into the nature of the corresponding solvent-assisted processes.19 The results of our calculations suggested that the electron-driven proton transfer (EDPT)20 along two water molecules might contribute to the deactivation of πσ* states via a conical intersection with the electronic ground state in AICNwater clusters.19 Please note that some authors use the term proton coupled electron transfer (PCET) to describe similar processes.21,22 In this work, we argue that EDPT along water wires might be quite common photorelaxation mechanism for a much larger group of compounds with low lying πσ* states in aqueous environment. We provide a comprehensive description of the

xperimental and theoretical efforts of the past two decades show that πσ* states play a very important role in the photochemistry and photostability of nucleic-acid and protein building blocks.1−4 Although the gas phase photochemistry of these states is now well understood,1−4 complete understanding of πσ*-driven deactivation processes in proper biochemical context requires the incorporation of explicit solvent molecules.1 For instance, it was shown that irradiation of tyrosine and tryptophan chromophores (phenol and indole) in aqueous environment leads to the formation of hydrated electrons.5−7 This phenomenon is also known as charge-transfer-to-solvent (CTTS) and was assigned to the presence of low-lying πσ* states in the spectrum of these molecules.4,6,8 Because CTTS might be followed by a subsequent proton transfer to a nearby water molecule, πσ* states were also proposed as the reason for the distinctive photoacidity of similar chromophores.9 Such direct participation of solvent molecules increases complexity of the studied processes and hinders the interpretation of experimental data.10 Consequently, our understanding of the photochemistry of πσ* states in aqueous solution is still incomplete. 2-Aminooxazole (AMOX) is one of the most noteworthy and yet relatively unexplored chromophores that exhibit πσ* photochemistry.11,12 This small aromatic compound is one of the key intermediates in the prebiotically plausible, UV-assisted synthesis of pyrimidine ribonucleotides proposed by Powner and co-workers.13,14 In this scenario, AMOX is presumed to have accumulated over longer periods of time,15 and for that, it must have been photostable. Recently, we identified two © 2015 American Chemical Society

Received: February 6, 2015 Accepted: March 31, 2015 Published: March 31, 2015 1467

DOI: 10.1021/acs.jpclett.5b00261 J. Phys. Chem. Lett. 2015, 6, 1467−1471

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The Journal of Physical Chemistry Letters underlying mechanism based on the results of surface-hopping nonadiabatic molecular dynamics simulations of microhydrated AMOX. For this purpose, we utilized the Newton-X package,23 where the nuclei were propagated classicaly on the Born− Oppenheimer potential energy surfaces and the nonadiabatic transitions were accounted for by means of the Tully’s fewest switches surface hopping algorithm.24 The energies and forces were calculated using the algebraic diagrammatic construction method to the second order [ADC(2)],25,26 which provides the description of the excited electronic states at a comparable level as MP2 does for the ground state. This computational scheme was carefully tested by the authors and proven to provide highly accurate results in similar studies on the photodynamics of adenine, both in gas phase and in water clusters.27,28 The details of the computational protocol employed here can be found in the Supporting Information. The minimum energy structures of AMOX hydrated by five water molecules are shown in Figure 1. The S1 minimum is of

Figure 2. Simulated UV absorption spectrum of the AMOX-(H2O)5 cluster. Initial conditions for dynamics were sampled from the shaded area.

process has outwardly secondary contribution to the photochemistry of microsolvated AMOX. It should be noted, though, that the EDPT mechanism was activated in 42.2% of the trajectories, but in over a half of such cases, the system eventually followed photorelaxation pathways through either ring-puckered or ring-opened conical intersections. It was also shown that relaxation channels via the πσ* surface become more active at higher excitation energies. 1 Thus, the participation of the EDPT mechanism might be increased when shorter irradiation wavelengths are considered. The importance of this mechanism in our simulations might also be underestimated due to classical propagation of the nuclear trajectories and neglect of proton tunneling.29 The estimated excited-state lifetime of the AMOX-(H2O)5 cluster amounts to ∼125 fs based on the fitting of a biexponential decay function to the relaxation time distribution (see the Supporting Information for more details). The EDPT process has a significant contribution to this value. The trajectories that transiently evolve on the πσ* hypersurface display a longer relaxation time in general. This transient evolution of the system in the πσ* state is connected to the multiple forward−backward proton relays until the EDPT-CI or other state crossing is reached. Because some of the trajectories needed over 500 fs to relax to the electronic ground state, we suspect that also a slow component of about 1 ps might be observed in this system. However, the limited number of trajectories and simulation time makes our estimate of this constant rather tentative. It is interesting to note that similar elongation of excited-state lifetime was observed experimentally in microsolvated tryptophan, which also exhibits πσ* photochemistry.30 Such a delay of photorelaxation should be particularly apparent when the EDPT along water wires has an even larger contribution to the overall photochemistry of the UV-excited chromophore. A representative trajectory that illustrates the main features of the EDPT photorelaxation mechanism is shown in Figure 4. The plot shows that the πσ*−S0 energy gap is significantly reduced during both proton transfers, which occur after about 90 and 130 fs, respectively. Thus, the principal reaction coordinate that leads to the EDPT-CI is associated with

Figure 1. Equilibrium geometries of the studied AMOX-(H2O)5 cluster: (a) ground state minimum; (b) S1 (πσ*) minimum.

πσ* character, and consequently, the network of hydrogen bonds is significantly influenced by the CTTS process. Similarly as in the case of AICN, five water molecules are sufficient to stabilize the formation of the H3O+ cation on the πσ* hypersurface. In contrast to AICN-(H2O)5 cluster, the investigated AMOX-(H2O)5 complex has only one minimum in the πσ* state, which consists of AMOX radical, hydronium cation, and four water molecules solvating an electron. Optimizations of alternative AMOX-(H2O)n cluster geometries, with the water molecules located on both sides of the oxazole ring, always lead to the ejection of the electron in the O-side direction due to character of the πσ* state (see section 4 in the Supporting Information). Therefore, to elucidate the process of solvation of an ejected electron all water molecules are located on the O-side of the oxazole ring. The UV absorption spectra were computed based on the optimized ground-state geometry of this AMOX-(H2O)5 cluster (Figure 2). Initial conditions for the nonadiabatic dynamics were sampled in the 5.60 ± 0.2 eV spectral domain, near the computed absorption maximum. The quantum yields of all the radiationless deactivation channels observed in the simulations are summarized in Figure 3. According to this statistic, ring-puckering and ring-opening processes have dominant contribution to the overall photochemistry of the cluster (37.5% and 35.9% respectively). Both mechanisms were reported previously as possible photorelaxation channels of AMOX in the gas phase.11 As expected, stretching of the N−H bond on the (nonsolvated) N-side of the oxazole ring had a minor contribution to the radiationless deactivation mechanisms of the studied AMOX-(H2O)5 cluster. Interestingly, approximately 20% of the trajectories deactivated through the πσ*/S0 conical intersection after the electrondriven proton transfer (EDPT-CI). It would seem that this 1468

DOI: 10.1021/acs.jpclett.5b00261 J. Phys. Chem. Lett. 2015, 6, 1467−1471

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Figure 3. Quantum yields of the photodeactivation processes calculated for the studied AMOX-(H2O)5 cluster.

Figure 4. Evolution of the energy gap between the πσ* state and the electronic ground state extracted from a representative trajectory. The insets present the initial geometry and structures after the first and second proton transfers.

Figure 5. πσ*/S0 conical intersection geometries. Panels (a) and (b) show the same conical intersection that involves two proton-relaying water molecules and the respective π and σ* molecular orbitals. Panels (c) and (d) show the alternative minimum energy conical intersections involving three and four relaying water molecules, respectively. Arrows indicate the movement of the mobile proton.

subsequent proton transfers in the direction of the hydrated electron. Furthermore, to reach the state crossing, the second proton transfer must be in coherence with a slight elongation of the O−H bond in the newly formed H3O+ cation that points in the direction of the solvated electron. The lack of this coherence extends the trajectory and might lead to backward proton relay to the chromophore. After relaxation to the electronic ground state, the system may either undergo dissociation of the above-mentioned O−H bond, or the hydrated electron and the proton can be subsequently returned to AMOX. These two scenarios are indicated by the energy difference gradient (g) and nonadiabatic coupling (h) vectors, which are responsible for the degeneracy lifting at the intersection point (see also the optimized geometry of the EDPT-CI shown in Figure 5a and b).31 In most of the trajectories connected to the EDPT deactivation mechanism, proton needs to be transferred along two water molecules. However, the number of proton transfers on the πσ* hypersurface is not decisive for the photorelaxation, and the cluster may undergo numerous forward−backward proton transfers along up to four water molecules. In Figure 5, we show examples of optimized conical intersection geometries that required more than two proton-relaying water molecules. This implies that the relative positions of the hydrated electron and the H3O+ cation, as well as the aforementioned coherence

in O−H vibrations are all crucial for the occurrence of a πσ*/S0 state crossing. Naturally, other configurations of AMOX−water clusters and bulk effects may influence the quantum-yields of accessible photorelaxation processes. In this sense, the evaluated contributions of different deactivation mechanisms presented in Figure 3 should be treated as tentative values. However, the main goal of this work was to indicate the plausibility of the EDPT mechanism in a model microhydrated chromophore and to provide its qualitative features. We emphasize that many of the described dynamical features should be transferable to other similar systems regardless of the internal configuration of hydrogen bonds. We extended the above considerations by initial evaluation of a cluster of AMOX with six and seven water molecules. The presence of a larger number of water molecules stabilizes additional minima on the πσ* hypersurface. Consequently, subsequent proton transfers to further H2O molecules are more favorable, and the contribution of the EDPT relaxation pathway might be more significant when larger AMOX−water clusters are considered. To assess the effects of polar environment interacting with the photoexcited cluster, we also performed single point CASPT2/CASSCF calculations along the representative trajectory including the 1469

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(H2O)5 cluster. Thus, we conclude that low-lying πσ* states might have a salient contribution to the overall photochemistry of many aquated biomolecules, even if other photorelaxation channels are dominant.

Kirkwood implicit solvent model of bulk water. The implicit solvation stabilizes the polar πσ* state with respect to the ground state, and we suggest that that the EDPT-CI should be generally more accessible in bulk water (see Supporting Information for more details). This observation is consistent with recent findings of Dargiewicz et al.32 In addition to all the foregoing, the occurrence of multiple proton transfers along H2O wires was also suggested in the case of photochemical water splitting mechanism on GaN/water interfaces33 and photochemical tautomerization in aqueous solution.21 These findings additionally support the transferability of our observations to bulk environments. Even though some features of the photochemistry of fully solvated AMOX cannot be exactly reproduced by the cluster model, such an approach was previously proven to provide reliable results and many valuable insights into the solution phase photochemistry of similar chromophores.6,8,28,34 These insights are often not visible in bulk experiments due to much higher complexity of the acquired spectra.34 In particular, many specific mechanistic features can be obtained by ultrafast pump−probe spectroscopic experiments in conjunction with time-of-flight mass spectrometry, which enables selecting clusters of desired sizes. Such experimental studies on indole and adenine clustered with water or ammonia molecules revealed ultrafast photorelaxation time scales comparable to our observations.35−38 According to these results, at least partial protonation of the surrounding solvent molecules should occur after the UV-irradiation of microsolvated indole.35,37 Furthermore, experimental findings of Ritze et al. suggest that the presence of water molecules solvating adenine remarkably activates photorelaxation through the πσ* state by stabilizing its highly polar character.38 In conclusion, we have shown that the electron-driven proton transfer along H2O wires may be an effective photorelaxation mechanism that enables the occurrence of πσ*/S0 state crossings in microhydrated AMOX. These findings confirm our previous suggestion regarding the existence of a similar photodeactivation channel in microhydrated AICN.19 An analogous relaxation pathway was recently proposed for hydrochinone- and catechol-ammonia clusters.39 The presence of a common mechanism in several distinct molecules indicates that it could be a general feature of πσ* states in microsolvated chromophores. This mechanism could contribute to our understanding of the photochemistry of many other biologically relevant chromophores in bulk water. The latter statement is further supported by experimental evidence for the formation of hydrated electrons and occurrence of comparable ultrafast relaxation time scales in aqueous solutions of compounds like adenine and tryptophan.7,40,41 It should be noted, though, that Roberts et al. attribute the formation of hydrated electrons to photoionization of adenine,41 even though its ionization potential in water is much higher than their laser frequency.42 EDPT photorelaxation is also another mechanism that involves direct participation of solvent molecules in the formation of a state crossing. Therefore, our results supplement the very recent findings of Barbatti,28 which underscores the importance of an opposite process of water-to-chromophore charge transfer. Even though the deactivation through the EDPT-CI has relatively low quantum-yield compared to the ring-puckered and ring-opened conical intersections, the EDPT mechanism was activated in over 40% of the trajectories and significantly extended the exited-state lifetime of the studied AMOX-

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ASSOCIATED CONTENT

S Supporting Information *

Additional information is available that includes: description of the methodology, vertical excitation energies, MS-CASPT2 benchmark calculations, excited-state population fitting, discussion of other possible cluster configurations, and Cartesian coordinates of relevant stationary points. This material is available free of charge via the Internet at http://pubs.acs.org/.

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AUTHOR INFORMATION

Corresponding Authors

*E-mail: [email protected]. *E-mail: [email protected]. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS We thank Prof. Andrzej Sobolewski, Prof. Wolfgang Domcke, and Joanna Jankowska for helpful discussion and suggestions. Financial support from the project “CEITECCentral European Institute of Technology” (CZ.1.05/1.1.00/02.0068) from the European Regional Development Fund and the Grant Agency of the Czech Republic (Grant 14-12010S) is gratefully acknowledged. This work was also supported by a statutory activity subsidy from the Polish Ministry of Science and Higher Education for the Faculty of Chemistry of Wrocław University of Technology. Some of the calculations were performed at the Wroclaw Center for Networking and Supercomputing (WCSS) and Interdisciplinary Centre for Mathematical and Computational Modelling in Warsaw (ICM).

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REFERENCES

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