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Photo-relaxation induced by water-chromophore electron transfer
Mario Barbatti
J. Am. Chem. Soc., Just Accepted Manuscript • DOI: 10.1021/ja505387c • Publication Date (Web): 10 Jul 2014
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7 Photo-relaxation induced by water-chromophore electron
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transfer
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Mario Barbatti
12 Max-Planck-Institut für Kohlenforschung. Kaiser-Wilhelm-Platz 1, D-45470 Mülheim an der Ruhr, Germany
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16 Supporting Information Placeholder
17
ABSTRACT: Relaxation of photoexcited chromophores is a have unveiled how different types of phenomena – internal con-
18
key factor determining diverse molecular properties, from version,5,14 exciton delocalization,15,16 intersystem crossing17 – are
19 involved in nucleic-acid photo-relaxation. These works have also
20 luminescence to photostability. Radiationless relaxation
usually occurs through state intersections caused by distor- showed how many variables like tautomeric effects, fragment
21 nature (isolated bases, base pairs, stacked bases), and solvation
tions in the nuclear geometry of the chromophore. Using
22 state play different roles to determine the main reaction pathways
excited-state nonadiabatic dynamics simulations based on
23 that are followed after photo-excitation.18 In spite of the im-
algebraic diagrammatic construction, it is shown that this is portance of this bio-molecular framework on itself, the findings of
24 the case of 9H-adenine in water cluster, but not of 7H-
25 the present simulations are more general, with potential implica-
adenine in water cluster. 7H-adenine in water cluster relaxes tions for diverse fields of research.
26 via a state intersection induced by electron transfer from
27 water to the chromophore. This result reveals an unknown
28 reaction pathway, with implications for the assignment of
29 relaxation mechanisms of exciton relaxation in organic elec-
30 tronics. The observation of photo-relaxation of 7H-adenine
31 induced by water-chromophore electron transfer is a proof of
32 principle calling for further computational and experimental
33 investigations to determine how common this effect is.
34
35
36
In the last two decades, it became clear that state crossings play
37 a central role for internal conversion.1,2 When involving the
38 ground and the first excited states, such crossings are usually
39 caused by strong distortions of the molecular geometry, such as
40 bond dissociation,3 bond twist,4 or ring puckering.5 Most of time,
41 the environment is assumed to play an important, but passive role:
42 it helps to tune the specific topography of the reaction pathways,
43 shifting the energies of stationary states and state crossings up and
down; however, the environment is not expected to directly con-
44
tribute to the state crossing itself. During my investigations of the
45 relaxation of two tautomers of photo-excited adenine in water
46 clusters, I found out that 9H-adenine in water cluster exemplary
47 corresponds to such conventional description. Its relaxation pro-
48 cess is very similar to what is observed in the gas phase.6,7 Never-
49 theless, the relaxation of 7H-adenine in water cluster was deeply
50 distinct from that in the gas phase, with the electronic structure of
51 one of the water molecules actively contributing to the formation
of the state crossing where internal conversion to the ground state Figure 1. Ground-state structure of a) 9H-adenine + water
52
took place. This finding comes to join another previously identi- and b) 7H-adenine + water. c) Singly occupied orbitals at the
53 fied solvent-chromophore excited-sate pathway, the proton- electron-transfer state intersection for 7H-adenine + water.
54 coupled electron transfer described in Refs.8,9.
55 The initial motivation to investigate the nonadiabatic dynamics
Time-resolved spectroscopy of adenine in the gas phase shows
56 a single time constant of 1.2 ps after excitation at 267 nm.19,20 In
of UV-excited adenine tautomers is that the understanding of how
57 water, adenine shows two time constants, 0.18 ± 0.03 and 8.8 ±
nucleic acid fragments, from nucleobases to double-strands, react
1.2 ps (263 nm).21 Either in gas or in water, these short excited-
58 to photo-excitations is a key step to comprehend mutagenesis,
state deactivation times are undisputed evidence that UV-excited
59 carcinogenesis,10,11 and the development of life in early biotic
adenine relaxes back to the ground state via internal conversion.
60 era.12,13 During the last years, experimental and theoretical works

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In the case of adenine in water, the two time constants have been In the case of 7H-adenine in water cluster, differently from the
1 assigned to the two main tautomers of adenine, the short to 9H- experimental assignment, the simulations showed that this tauto-
2 adenine and the long to 7H-adenine.21-24 Although it is not clear mer should contribute not only to the long, but also to the short
3 why these tautomers would relax with different time constants time constant. The fitting of the relaxation-time distribution shows
4 (see Refs.25,26 for their reaction paths in the gas phase), the validi- that 69% of 7H-adenine population relaxes with a time-constant
ty of this assignment has been taken for granted, as it leads to of 0.37 ps, while the remaining 31% relaxes with a time constant
5
estimate of tautomeric populations consistent with other meas- that is much longer than 1 ps, the maximum simulation time
6 urements.21 (Table 1).
7
So far, it has been challenging to use dynamics simulation Table 1. Excited-state lifetime τ and fraction of the
8 methods to determine the relaxation mechanism of solvated ade-
9 population f0 not deactivated within the ultrafast
nine due to, on one hand, the large size of quantum-mechanical step for adenine tautomers in the gas phase (GP) and
10 active site consisting of adenine plus the first shell of waters; and,
11 in water (W) clusters.
on the other hand, the failure of the time-dependent density func-
12 tional theory to describe this system.27 Recent developments in
the field, including the possibility of performing nonadiabatic f0 τ (ps)
13
14 dynamics7 with algebraic diagrammatic construction to the second
order [ADC(2)],28,29 has made possible to simulate how different Theor. Expt.
15
solvated tautomers react to UV excitation.
16 7H-Ade GP 0.00 1.47
17 My working hypothesis is that the main impact of the solvation 1.2
a
on the excited-state evolution is due to the few water molecules 9H-Ade GP 0.00 1.12
18 directly hydrogen-bonded to adenine. Thus, I ran excited-state
19 nonadiabatic dynamics simulations of 7H- and 9H-adenine within 7H-Ade W 0.31 0.37, >1 b
0.18, 8.8
20 small water clusters using the surface hopping method, based on 9H-Ade W 0.00 0.22
21 ADC(2) potential energy surfaces and couplings. a 19,20 b 21
22 Pump: 267 nm. ; Pump: 263 nm.
The optimized clusters for both tautomers are shown in Fig. 1-a
23 and b (see Supporting Information, SI, for details on geometries
24 and excitation spectra). For 9H-adenine, the minimal cluster has
25 six waters, while for 7H-adenine, it has five waters. Starting from
26 the ground-state optimized clusters, the absorption spectra were
27 computed. Spectral points in the 4.71 ± 0.05 eV (~263 nm, Fig. 2)
domain were taken to start the dynamics.
28
29 0.6
7H-Ade + 5W
30 9H-Ade + 6W
31
Absorption cross section ( )

Å 7H-Ade
2

32 9H-Ade
33 0.4
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37 0.2

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0.0
41 4.0 4.5 5.0 5.5
42 Figure 3. Energy-gap evolution in a representative trajectory
∆E (eV)
43 of 7H-adenine in water.
44 Even more surprising is that ring-puckered intersections only
45 Figure 2. Simulated absorption spectrum of adenine tauto- accounted to a minor fraction of the relaxation processes in 7H-
46 mers in water clusters and in the gas phase. Initial conditions adenine (12% of trajectories). Most of trajectories (58%) followed
47 for dynamics were sampled from the shaded area. a completely new relaxation pathway ending at a S1/S0 intersec-
48 The results of the simulations show that, in fact, the relaxation tion where 7H-adenine is almost planar. At this planar intersec-
49 of 9H-adenine in water cluster should contribute only to the short tion, the S1 state consists of an electron excitation from lone-pair
50 time constant. The distribution of relaxation times can be fitted orbitals at N3 and at the nearest oxygen into a π* orbital at the
with a single decay function (see SI), giving a time constant of imidazole ring. The main mechanistic feature inducing the inter-
51 section is a rotation of the water near N3 (W3 in Fig. 1-b), which
52 0.22 ps (Table 1). Most of trajectories (90%) followed a pathway
ending at a state intersection caused by a strong out-of-plane goes from an OH———N3 conformation in the ground-state geometry
53 distortion of C2 (C2 puckering), very similar to what is observed to a conformation with oxygen lone pair facing the N3 lone pair
54 in the gas phase.7 Few trajectories relaxed at C6-puckered inter- (Fig. 1-c and Fig. 3; see the movies in the SI, too). A natural
55 sections (4%) or at adenine-water proton-transfer intersections population analysis of the S1 density at this intersection geometry
56 (6%). (See SI for statistical errors.) shows that W3 transfers 0.4 electron to the imidazole group. In
57 fact, the statistical analysis of the S1 charge transfer at the inter-
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section point for all trajectories resulted in a mean value of 0.4 ± internal conversion even in situations where steric interactions
1 0.1 electron transferred from water to 7H-adenine. tend to hinder the chromophore distortion.
2 The geometry of the S1-S0 intersection is shown in Fig. 4 (see The active role of water to create state intersections has eluded
3 SI). It is the lowest-energy intersection occurring during the dy- experimentalists and theorists so far due to a few different rea-
4 namics. The S1-S0 energy gap is 0.11 eV. Conical-intersection sons. First, it may not be a widespread effect. As we have seen,
5 optimization30 starting from this structure does not change it 9H-adenine is not affected by this effect and at this point it is
6 significantly. Although the rings are essentially planar, N7 and C8 admittedly too soon to know how common it is. Second, time
7 are slightly pyramidalized to accommodate the excess of electron constants for internal conversion in different environments are
charge in the imidazole ring. usually similar, which induces us to believe that the same qualita-
8 tive process is taking place. In fact, this expectative has affected
9 previous simulations in the field, which commonly took water
10 into account either as a continuum or as a molecular force
11 field.32,33 (Neither of these approaches can describe changes in the
12 electronic structure of the solvent, only its perturbation to the
13 environment.) Even simulations considering explicit quantum-
14 mechanical solvent also missed the effect either for dealing only
with the 9H tautomer or for focusing on traditional reaction
15
paths.34,35 Thus, the manifestation of this water-chromophore
16 electron transfer intersection had to wait for simulations combin-
17 ing dynamics, different tautomers, and explicit quantum-
18 mechanical solvation. (For a recent discussion of the excited
19 states of water clusters see Ref.36.)
20 These results have also two important consequences. First, it
21 Figure 4. Top and lateral views of the S1-S0 intersection in
reinforces the idea that the solvent-chromophore electron-transfer
7H-adenine in water.
22 pathways need to be considered in the assignment of relaxation
23 Other local minima may be accessible at similar energies for mechanisms chromophores in polar solvents.9 Second, the possi-
24 such clusters and also bulk effects may play a role in the final bility that the environment may create state intersections upon
25 quantitative results. For this work, however, it matters only the photoexcitation may have relevant implications for organic elec-
occurrence of relaxation induced by water-chromophore electron tronics, where internal conversion to the ground state is often a
26 factor reducing the efficiency of photovoltaic devices.37
transfer. It is a proof that in principle this effect may take place
27 after photoexcitation of solvated chromophores. Besides that, the In this work I showed that photo-relaxation induced by water-
28 modeling of clusters, initially aimed at simplifying the problem, chromophore electron transfer is a major internal conversion
29 should be seen under new light. In the future, the search for exper- pathway for one specific tautomer of adenine. This new phenom-
30 imental evidences of this new path may profit of cleaner spectra enon is interesting enough to be already communicated to the
31 measured for small clusters31 as compared to those measured in chemistry community. Nevertheless, there is still al long way to
32 bulky water. go from this proof of principle to a more robust characterization.
33 Proton transfer after the electron transfer was not observed. There are a number of questions to be addressed by computational
34 This implies that either it is classically forbidden or there is not simulations, including the reason why this pathway is not activat-
35 enough time for its occurrence before the internal conversion ed in 9H-adenine, whether it happens with other polar solvents,
takes place. Tunneling is not considered in the modeling, but, and how it is affected by the water bulk. Naturally, it also rests the
36 challenge of characterizing this effect experimentally, which may
again, the time between the population of the electron-transfer
37 possibly be achieved by time-resolved photoelectron spectroscopy
state and the internal conversion (~50 fs) may be too short for its
38 occurrence. of selected tautomers within small water clusters.
39
Dynamics of both tautomers in the gas phase was also simulat-
40 ed. 9H-adenine relaxation splits between C2- and C6-puckered
Computational Methods
41 pathways, as reported before.7 The lifetime is 1.12 ps (Table 1). Ab-initio algebraic diagrammatic construction to the second
42 7H-adenine relaxes preferentially through C6-puckered intersec- order [ADC(2)]28 was used to simulate the nonadiabatic dynamics
43 tions, with 1.47 ps lifetime. Assuming a tautomeric population of of 9H and 7H tautomers of adenine in small water clusters. Clus-
44 20% of 7H and 80% of 9H,21 the lifetime is 1.2 ps, in excellent ters were optimized in the ground state with the Møller-Plesset
45 agreement with the experimental time constant (1.2 ps for 267 nm perturbation theory to the second order (MP2; Cartesian coordi-
46 excitation).19,20 nates are given in the SI). aug-cc-pVDZ and cc-pVDZ basis sets
47 As I mentioned above, state intersections between the ground were assigned to N and C atoms, respectively.38 SVP basis set39
and the first excited states are normally associated to strong dis- was assigned to O and H atoms. The nuclear ensemble method40
48
tortions of the nuclear frame. These distortions are needed be- with 500 points and 5 excited states was used to simulate the
49 absorption spectrum, from where initial conditions for dynamics
cause to have a state crossing, it is necessary to simultaneously
50 stabilize the energy of the excited state and destabilize the ground were selected. 50 trajectories for each tautomer with water and in
51 state. This is what happens, for instance, during ring puckering. In the gas phase were started from the 4.71 ± 0.05 eV (~263 nm)
52 the planar intersection, however, the crossing was produced not spectral window, summing to a total of 200 trajectories. For 7H-
53 by distortion of the excited chromophore geometry, but by rear- adenine in water, this window corresponded to 47 trajectories
54 rangement of the solvation shell followed by population of a starting in S1 and 3 trajectories in S2. For 7H-adenine in the gas
55 electron-transfer state. (State and geometry evolutions are dis- phase, this distribution was 25 and 25. For 9H-adenine in water,
cussed in the SI.) This process opens the possibility of having 41 and 9. For 9H-adenine in the gas phase, 33 and 17. Nonadi-
56
abatic effects between excited states were taken into account via
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fewest-switches surface hopping41 with decoherence corrections.42 (14) Canuel, C.; Mons, M.; Piuzzi, F.; Tardivel, B.; Dimicoli, I.;
1 With ADC(2), only nonadiabatic transitions between excited Elhanine, M. J. Chem. Phys. 2005, 122, 074316-074316.
states can be computed.7 Thus, for each trajectory, the time for (15) Banyasz, A.; Gustavsson, T.; Onidas, D.; Changenet-Barret, P.;
2 Markovitsi, D.; Improta, R. Chem. Eur. J. 2013, 19, 3762-3774.
3 internal conversion to the ground state was estimated by the first
(16) Takaya, T.; Su, C.; de La Harpe, K.; Crespo-Hernández, C. E.;
4 time in which the energy gap between the first excited state and Kohler, B. Proc. Natl. Acad. Sci. USA 2008, 105, 10285-10290.
the ground state dropped below 0.15 eV. Trajectories were inte- (17) Mai, S.; Marquetand, P.; Richter, M.; González-Vázquez, J.;
5
grated until this threshold was reached or for a maximum of 1 ps. González, L. ChemPhysChem 2013, 14, 2920-2931.
6 The time step for integration of classical equations was 0.5 fs and (18) Middleton, C. T.; de La Harpe, K.; Su, C.; Law, Y. K.; Crespo-
7 of quantum equations, 0.025 fs. All calculations were done with Hernández, C. E.; Kohler, B. Annu. Rev. Phys. Chem. 2009, 60, 217-239.
8 Turbomole43 and Newton-X44,45 programs. Detailed information (19) Satzger, H.; Townsend, D.; Zgierski, M. Z.; Patchkovskii, S.;
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10 (20) Satzger, H.; Townsend, D.; Stolow, A. Chem. Phys. Lett. 2006,
11 ASSOCIATED CONTENT 430, 144-148.
12 Supporting Information (21) Cohen, B.; Hare, P. M.; Kohler, B. J. Am. Chem. Soc. 2003,
13 125, 13594-13601.
Movies with trajectory examples. Computational details. (22) Buchner, F.; Ritze, H.-H.; Lahl, J.; Lubcke, A. Phys. Chem.
14 Geometries, vertical excitations, and spectra. Statistical anal- Chem. Phys. 2013, 15, 11402-11408.
15 ysis of simulations. Analysis of a single trajectory. Compari- (23) Pancur, T.; Schwalb, N. K.; Renth, F.; Temps, F. Chem. Phys.
16 2005, 313, 199-212.
son to fully-correlated data. Dipole moments and ionization (24) Gustavsson, T.; Sharonov, A.; Onidas, D.; Markovitsi, D.
17 potentials at the intersections. Cartesian coordinates. This Chem. Phys. Lett. 2002, 356, 49-54.
18 material is available free of charge via the Internet at (25) Marian, C. M.; Kleinschmidt, M.; Tatchen, J. Chem. Phys.
19 http://pubs.acs.org. 2008, 347, 346-359.
20 (26) Serrano-Andrés, L.; Merchán, M.; Borin, A. C. Chem.-Eur. J.
AUTHOR INFORMATION 2006, 12, 6559-6571.
21 (27) Barbatti, M.; Lan, Z.; Crespo-Otero, R.; Szymczak, J. J.;
22 Corresponding Author Lischka, H.; Thiel, W. J. Chem. Phys. 2012, 137, 22A503-514.
23 (28) Hättig, C. Adv. Quantum Chem. 2005, 50, 37-60.
E-mail: barbatti@kofo.mpg.de. (29) Schirmer, J. Phys. Rev. A 1982, 26, 2395-2416.
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(30) Levine, B. G.; Coe, J. D.; Martínez, T. J. J. Phys. Chem. B
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Notes
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29 (33) Lan, Z.; Lu, Y.; Fabiano, E.; Thiel, W. ChemPhysChem 2011,
30 The author acknowledges generous computer time provided
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by the Max-Planck-Institut für Kohlenforschung. (34) Gustavsson, T.; Sarkar, N.; Vaya, I.; Jimenez, M. C.;
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Ground-state structure of a) 9H-adenine + water and b) 7H-adenine + water. c) Singly occupied orbitals at
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ACS Paragon Plus Environment
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Table of Contents Graph
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ACS Paragon Plus Environment