Photochemistry of hydrogen-bonded aromatic pairs:
Quantum dynamical calculations for the
Zhenggang Lan†‡, Luis Manuel Frutos†§, Andrzej L. Sobolewski¶, and Wolfgang Domcke†
†Department of Chemistry, Technical University of Munich, D-85747 Garching, Germany; and¶Institute of Physics, Polish Academy of Sciences,
PL-02668 Warsaw, Poland
Edited by F. Fleming Crim, University of Wisconsin, Madison, WI, and approved April 17, 2008 (received for review February 8, 2008)
The photochemical dynamics of the pyrrole–pyridine hydrogen-
bonded complex has been investigated with computational meth-
ods. In this system, a highly polar charge-transfer state of1??*
character drives the proton transfer from pyrrole to pyridine,
leading to a conical intersection of S1 and S0 energy surfaces. A
two-sheeted potential-energy surface including 39 in-plane nu-
clear degrees of freedom has been constructed on the basis of ab
initio multiconfiguration electronic-structure data. The non-Born–
Oppenheimer nuclear dynamics has been treated with time-de-
pendent quantum wave-packet methods, including the two or
three most relevant nuclear degrees of freedom. The effect of the
numerous weakly coupled vibrational modes has been taken into
account with reduced-density-matrix methods (multilevel Redfield
state deactivation of hydrogen-bonded aromatic systems via the
electron-driven proton-transfer process. This process is believed to
be of relevance for the ultrafast excited-state deactivation of DNA
base pairs and may contribute to the photostability of the molec-
ular encoding of the genetic information.
conical intersection ? excited-state hydrogen transfer ?
the functionality of hydrogen bonds in the electronic ground
state have been investigated with powerful experimental and
computational methods for decades and are thus quite well
understood (1), much less is known about the role of hydrogen-
bond dynamics in excited electronic states of chemical or bio-
chemical systems. Fluorescence quenching of aromatic chro-
mophores by protic solvents and fluorescence quenching in
intermolecularly or intramolecularly hydrogen-bonded aromatic
systems are well known phenomena, but are still poorly under-
stood at the atomistic level (2–4). One reason for our limited
knowledge of excited-state hydrogen-bond dynamics is the ex-
tremely short time scale of some of these processes (presumably
of the order of 10 fs or less). Another reason is the difficulty of
performing accurate ab initio electronic-structure calculations
for excited states of complex polyatomic systems.
It has recently been proposed that electron-driven proton-
transfer processes along hydrogen bonds could play a decisive
role for the ultrafast excited-state deactivation of biological
molecules and supermolecular structures, such as DNA base
pairs, peptides, or UV-protecting pigments (5–7). The compu-
tational studies suggest that proton-transfer processes driven by
charge-transfer (CT) states of1??*,1n?*, or1??* character
provide barrierless access to conical intersections (8) of the
excited-state and ground-state potential-energy surfaces, where
ultrafast internal conversions take place. This particularly effi-
cient mechanism of energy dissipation could be essential for
photostability of the molecular encoding of the genetic infor-
mation of life (9). Recent experimental results for DNA base
in chemistry and biochemistry. Although the structure and
pairs or biomimetic models thereof seem to support this
Although ab initio calculations of electronic excitation ener-
gies, minimum-energy reaction paths, and energy profiles, as
well as minima of conical intersection seams can provide valu-
able insight, a true mechanistic understanding requires the
computational treatment of the nuclear dynamics of the photo-
chemical process. Such calculations are challenging because of
the large number of nuclear degrees of freedom, the large excess
energy provided by UV photons, and extremely strong non-
Born–Oppenheimer effects at conical intersections (8). Very
recently, a few ab initio on-the-fly trajectory simulations have
been performed on hydrogen-detachment and hydrogen-
transfer processes in biomolecular systems (13, 14). Although
such simulations can provide useful mechanistic insight, they
have limitations because of the rather significant de Broglie
wavelength of the proton, the approximate treatment of the
nonadiabatic dynamics at the conical intersections, the inevita-
ble compromises with respect to the accuracy of the ab initio
methods, and the very limited number of trajectories that can be
In this work, we describe the first attempt of a fully quantum
mechanical treatment of nonadiabatic photochemical dynamics
of a hydrogen bond in a biomimetic system. We adopt the
hydrogen-bonded pyrrole–pyridine aromatic pair (15) as a
model of the Watson–Crick base pairs in DNA. Multiconfigu-
ration ab initio methods have been used for the characterization
of the potential energy (PE) surfaces of the relevant electronic
states. An approximately 39-dimensional analytic PE surface of
the reaction-path-Hamiltonian type (16) has been constructed.
We report the results of reduced-dimensional time-dependent
quantum wave-packet calculations and calculations in the frame-
work of multilevel Redfield theory (17, 18). In the latter ap-
proach, the few most important nuclear degrees of freedom are
explicitly taken into account, whereas the many weakly coupled
degrees of freedom are treated approximately in perturbation
theory and the Markovian approximation.
Results and Discussions
One-Dimensional Potential-Energy Surfaces. The equilibrium struc-
ture of the hydrogen-bonded model system, planar pyrrole–
performed research; Z.L., L.M.F., and W.D. contributed new reagents/analytic tools; Z.L.,
L.M.F., and W.D. analyzed data; and Z.L., L.M.F., and W.D. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
‡To whom correspondence should be addressed. E-mail: email@example.com.
§Present address: Departamento de Quı ´mica Fı ´sica, Universidad de Alcala ´, 28871 Alcala ´ de
Henares (Madrid), Spain.
This article contains supporting information online at www.pnas.org/cgi/content/full/
© 2008 by The National Academy of Sciences of the USA
September 2, 2008 ?
vol. 105 ?
no. 35 ?
pyridine, is displayed in Fig. 1. The NH distance R of pyrrole is
defined as the reaction coordinate for the hydrogen transfer.
Fig. 2 gives an overview of the potential-energy surfaces of the
three lowest electronic states of pyrrole–pyridine as functions of
the hydrogen-transfer coordinate R (15). It can be seen that the
hydrogen atom is bonded to pyrrole in the electronic ground
state. The lowest locally excited (LE) singlet state of the complex
is of1??* character and1B2symmetry. The lowest singlet CT
state is of1B2symmetry and1??* character. It is optically dark,
i.e., it cannot be excited directly from the S0 state by a one-
the energies of the LE state and the S0 state at 2.4 a.u. and
3.9 a.u., respectively, see Fig. 2. The structures of pyrrole–
pyridine at the ground-state equilibrium geometry and the
conical intersection can be found in supporting information (SI)
Text and Tables S1 and S2. The CT–S0energy crossing visible in
Fig. 2 becomes a conical intersection when the vibrational modes
of B2symmetry, are taken into account.
Two-Dimensional Quantum Wave-Packet Dynamics. As the simplest
nontrivial model, we consider the two-dimensional model in-
cluding the reaction coordinate R and the effective coupling
tential-energy surfaces of this two-dimensional model are dis-
played in Fig. 3 a and b, respectively, as functions of R and the
effective coupling coordinate Qc
potential-energy surfaces are smooth functions of nuclear ge-
ometry, see Fig. 3a. The double-cone shape of the adiabatic
surfaces of the CT–S0conical intersection can be clearly seen in
In the present system, the diabatic coupling constants ?iof all
coupling modes are found to be rather small. Therefore, ?c
relatively small. This implies that the probability of electronic
population transfer is low. For clarity, we therefore consider in the
following only P1
ground state. The population probability of the CT state remains
near unity on the time scale of a few picoseconds.
When the lowest vibrational level of the electronic ground
state is vertically placed into the CT state, we observe that
oscillatory diabatic population transfer takes place with a period
eff(see Methods). The diabatic and adiabatic po-
eff. As expected, the diabatic
d, the population probability of the electronic
of ?500 fs, see Fig. 4a. The lack of irreversible electronic
population transfer is the result of the restriction to just two
nuclear degrees of freedom, the weak coupling at the CT–S0
conical intersection, and the rather small CT–S0energy gap in
Structure of the pyrrole–pyridine complex in the electronic ground
1 2 3 4
Potential Energy (eV)
lowest electronic states of pyrrole–pyridine: diabatic ground S0 state, CT
(1??*) state and LE (1??*) state.
One-dimensional PE functions for hydrogen transfer of the three
Potential Energy (eV)
Potential Energy (au)
eff. For sake of clarity, the diabatic coupling is exaggerated (? ?
0 1 2 3 4
0 1 2 3 4
the two-dimensional wave-packet calculations (a) and the three-dimensional
wave-packet calculations (b). The Inset of a is the diabatic population of the
S0state within the first oscillation period.
www.pnas.org?cgi?doi?10.1073?pnas.0801062105Lan et al.
the hydrogen-transferred complex, see Fig. 2. The superimposed
weak and rapid oscillations (period of ?19 fs, see Inset in Fig.
4a), reflect the time scale of vibrational motion along the
hydrogen-transfer coordinate. In this two-dimensional model,
the conical intersection clearly represents a major bottleneck for
the radiationless deactivation of the CT state.
Three-Dimensional Quantum Wave-Packet Dynamics. To get an im-
pression of the effect of the so-called tuning modes on the reaction
dynamics, we add the effective tuning mode Qt
three-dimensional conical intersection (see Methods). The addition
of a third mode leads to a qualitative change of the electronic
population dynamics. The population probability of the diabatic S0
state now increases monotonically within the first picosecond. The
fluctuations of the electronic population probability. The time
average of P1
4a to ?0.06 in Fig. 4b. The weak rapid oscillations arising from the
irregular than in Fig. 4a.
eff, resulting in a
d(t) over the first 4 ps has increased from ?0.03 in Fig.
Multilevel Redfield Dynamics. The reduced density matrix of the
system Hamiltonian, which includes the reaction coordinate R
and the effective coupling mode Qc
time, employing a Redfield tensor that has been constructed
from the remaining 19 vibrational modes of A1symmetry (see
eff, has been propagated in
Methods). The coupling of the reaction coordinate with the bath
of the remaining A1vibrational modes has a significant impact
on the electronic population dynamics, see Fig. 5a. After an
initial transient behavior, the population probability of the S0
state increases linearly with time, as expected for an incoherent
rate process. Rapid fluctuations are still visible but die out on a
time scale of ?100 ps. The existence of these transient fluctu-
ations reflects the fact that the data in Fig. 5 have been obtained
from a truly microscopic dynamical theory rather than from an
approximate rate expression.
These features can be understood as follows. The system-
bath-coupling slowly drains the vibrational energy out of the
hydrogen-transfer vibrational motion. The large excess energy
of the system is thus transferred to the A1modes on a time scale
of a few hundred picoseconds. The vibrational damping thus
reduces the recurrence of the vibrational wave packet to the
conical intersection, resulting in the lack of transfer of elec-
tronic population to the CT state.
According to these calculations, the internal-conversion dy-
namics from the CT state to the S0state takes place on a rather
slow radiationless decay of the CT state is the relatively weak
diabatic coupling at the CT–S0 conical intersection. Another
reason is the unfavorable location of the CT–S0conical inter-
section in a shallow secondary well of the S0potential-energy
surface (see Fig. 2), where the density of states of the S0surface
is rather low. As far as we can tell, our computer simulation of
the radiationless decay dynamics should be qualitatively correct,
which implies that the rather slow radiationless decay dynamics
existing calculations of the reaction-path potential-energy pro-
files of related singly or doubly hydrogen-bonded aromatic
systems, e.g., indole–pyridine, the 2-aminopyridine dimer (11),
or the guanine–cytosine Watson–Crick base pair (5) indicate a
topography of the CT–S0 conical intersection that is more
favorable for rapid radiationless decay.
To obtain insight into the role of the interstate coupling strength
at the conical intersection and the strength of the system-bath
coupling, we have performed additional reduced-density-matrix
propagations, varying the parameters of the ab initio-based model.
First, we increase the interstate coupling by multiplying ?c
a factor of 2. In this modified model, the rate of internal
conversion increases by approximately a factor of 2, see Fig. 5b.
The interstate coupling at the CT–S0conical intersection is thus
the rate-limiting factor in this model.
In a further calculation, we have increased the system-bath
coupling strength by a factor of 2. Because the Redfield tensor is of
second order in the system-bath coupling strength, it increases by
a factor of 4. As a result, the internal conversion rate increases
by a factor of ?4 (Fig. 5c), compared with the original model
(Fig. 5a). The ground-state population probability begins to satu-
rate at ?70 ps, see Fig. 5c. The damping of the hydrogen-transfer
dynamics is thus another rate-limiting process in this system.
In the original and the modified model, the interstate coupling
strength and the system-bath-coupling strength are rather low. As
time scale (a few hundreds picoseconds). In this limiting case, the
internal-conversion rate is approximately linearly and quadratically
dependent on the corresponding coupling parameters. This simple
strong interstate coupling at conical intersections. However, the
present results are useful for the understanding of the general
mechanism of the internal-conversion dynamics in biomolecular
We have investigated the nonadiabatic dissipative dynamics of
the pyrrole–pyridine hydrogen-bonded complex, which is trig-
from the reduced-density-matrix propagations within the original model (a),
for increased interstate coupling strength (b), and for increased system–bath
coupling strength (c).
Electronic population probability of the diabatic S0state, obtained
Lan et al.
September 2, 2008 ?
vol. 105 ?
no. 35 ?
gered by the photoinduced electron-driven proton-transfer pro-
cess. The potential-energy surfaces of the relevant electronic
states have been characterized by ab initio electronic-structure
calculations at the CASSCF level. A 39-dimensional model of
potential-energy surfaces has been constructed, which is based
on ab initio energy gradients along the hydrogen-transfer reac-
tion coordinate and ab initio vibronic-coupling constants at the
conical intersection of the CT state with the S0state.
The nonadiabatic quantum dynamics of this multidimensional
model system has been investigated, employing time-dependent
wave-packet and reduced-density-matrix methods. Assuming
vertical electronic excitation of the CT state, we have explored
the time evolution of the population probabilities of the CT state
and the S0state. To gain insight into the microscopic mecha-
nisms of the radiationless decay dynamics of this system, we have
performed time-dependent quantum wave-packet calculations
involving the two or three most relevant nuclear coordinates.
To reveal the effect of the remaining, more weakly coupled,
vibrational degrees of freedom, we have adopted a system-bath
approach (Redfield theory) with ab initio determined Redfield
tensor elements. The results illustrate the evolution from a
quasiperiodic electronic population dynamics (for the case of
two nuclear degrees of freedom), via a stochastically fluctuating
electronic population dynamics (for the case of three vibrational
degrees of freedom), to a nonradiative rate process, when all 39
degrees of freedom of the model are taken into account.
The pyrrole–pyridine hydrogen-bonded complex has been
chosen as a representative model for the investigation of the
ultrafast hydrogen-bond photochemistry of DNA base pairs (10,
12). Pyrrole–pyridine can also serve as a model for fluorescence
quenching through intermolecular hydrogen bonding between
aromatic chromophores in solution (4). The radiationless decay
dynamics of pyrrole–pyridine has been found to be compara-
tively slow (of the order of a few hundred picoseconds). The
rather weak vibronic coupling at the CT–S0conical intersection
and the relatively slow damping rate of the hydrogen-transfer
mode have been identified as the origin of the relatively slow
of the present methodology can be used to treat the radiationless
decay dynamics of the guanine-cytosine and adenine-thymine
Watson–Crick base pairs, for which extremely fast internal
conversion rates are expected (5, 10, 12).
Ab Initio Calculations. The ab initio calculations have been performed at the
complete-active-space self-consistent-field (CASSCF) level with the 6–31(G)d
frequencies, and PE surfaces have been calculated with the Gaussian 03
potential-energy surfaces of the nonadiabatically coupled S0, LE, and CT states,
singular derivative coupling at the conical intersections (8), we construct qua-
approach (16). We focus on the conical intersection of the CT state with the S0
internal conversion process. The LE–CT conical intersection remains to be char-
The planar pyrrole–pyridine complex has C2v symmetry. The symmetry
species of the normal modes are
? ? 20A1? 7A2? 11B1? 19B2.
The 20 A1modes consist of the reaction coordinate R and 19 so-called tuning
potential-energy surfaces are described in the so-called linear-vibronic cou-
pling model (20) and will not be considered in what follows.
Because the proton-transfer reaction implies large-amplitude motion in
the reaction coordinate R, the linear vibronic-coupling parameters of the
tuning and coupling modes and the vibrational frequencies have to be con-
of the intrastate linear coupling constants ?i
represent them as fourth-order polynomials of R. For the interstate vibronic-
Rc, where Rc? 3.9 a.u. is the location of the CT–S0conical intersection. This
simplification of the model is appropriate, because the non-Born–Oppenhei-
mer dynamics at conical intersections depends essentially on the ?iat this
geometry. The dependence of the vibrational frequencies of all nonreactive
modes on the electronic state and the reaction coordinate is neglected in the
present linear-vibronic coupling model.
The intrastate coupling parameters, ?i
gradients of the adiabatic S0 and CT energies with respect to Cartesian
state normal coordinates, by using the L-matrix (21) of the latter. Analytical
nonadiabatic coupling vector (22) [or h vector (23)] on the ground-state
normal coordinates of B2symmetry, see the discussions in refs. 8 and 24. The
resulting diabatic potential model includes the large-amplitude proton-
transfer coordinate R, 19 linearly coupling tuning modes of A1symmetry, and
reaction coordinate R (see SI Text and Fig. S2 for characteristic examples)
results in a significant coupling of the tuning modes with the reaction coor-
a result, all 39 in-plane nuclear degrees of freedom in this model are coupled
to each other. We refer to SI Text for a more detailed description of the
39-dimensional potential-energy surface.
(2)of the tuning modes, we
(k)(k ? 1,2), are obtained as the
(k)(R) are obtained by a least-squares fit of the ab initio data to
Treatment of the Time-Dependent Nuclear Dynamics. In this work, we did not
attempt to perform time-dependent quantum wave-packet dynamics calcu-
lations with the inclusion of all 39 vibrational modes of the potential-energy
concepts that allow the reduction of the computational problem to a smaller
number of effective nuclear coordinates. One concept is the definition of
effective modes or cluster modes (25, 26). For a symmetry-allowed conical
intersection, as is the case here, these effective modes are just the gradient-
difference and nonadiabatic coupling (or g, h) vectors (22, 23). The atomic
displacement vectors associated with the g and h vectors are illustrated in Fig.
S1. Within the linear-vibronic-coupling model, the effective tuning and cou-
pling modes are given by (see refs. 20 and 25)
with the coupling strengths and frequencies
???i?2, ???i? ?1
Within the effective-mode approximation, the 39-dimensional dynamics
problem is reduced to a three-dimensional problem, involving the reaction
www.pnas.org?cgi?doi?10.1073?pnas.0801062105Lan et al.
coordinate R, as well as the effective tuning and coupling modes. In this
approximation, the anharmonic couplings arising from the R dependence of
any contribution in the branching space of the conical intersection. The
effective coupling coordinate Qc
B2modes with frequencies ?1,720 cm?1.
To account for the nonseparability of the reaction coordinate and the
tuning modes Qt,i, we have used multilevel Redfield theory (17, 18). Adopting
a system-bath model, the nuclear coordinates of the system Hamiltonian are
chosen as the reaction coordinate R and the effective coupling coordinate
The remaining A1modes are considered as a bath composed of harmonic
(k)are ignored. The B2modes with frequencies ?1,720 cm?1do not give
effthus can be constructed by considering all
eff, resulting in a two-state two-mode model.
The system-bath coupling is given by
estingly, the ?i
R dependence, that is
(k)(R) are fourth-order polynomial functions of R (see SI Text). Inter-
(k)(R) for different tuning modes have approximately the same
?k??R? ? gi
?k???k??R?; k ? 1,2,
??k??R? ? a?k?R4? b?k?R3? c?k?R2? d?k?R ? e?k?.
With this approximation, the system-bath coupling becomes
the spectral function of the bath. In the above approximation, the spectral
?k??2??? ? ?t,i?; ?k ? 1 or 2?.
functions. The full-width half-maximum of these Lorentz functions is 13 meV
(see Fig. S3 for a characteristic example).
It is straightforward to construct the Redfield tensor for this system-bath
coupling model (27). Note that the elements of the Redfield tensor are not
empirical parameters but are determined from the ab initio calculations.
The preparation of the initial state by the absorption of an UV photon is
the electronic ground state to the CT state. As mentioned above, the actual
by assuming direct electronic excitation to the CT state.
split-operator method, as discussed (28). We have used 64 grid points from
0.83 a.u. to 4.83 a.u. for R. Ten and 6 harmonic-oscillator basis functions are
packets are propagated for 4 ps with a time step of 0.1 fs.
We use the split-operator method for the short-time propagation of the
reduced density operator (29):
?s?t ? dt? ? e?iLsdt?2eDdte?iLsdt/2?s?t?,
respectively. The short-time propagator e?iLsdt/2is evaluated in the eigenstate
The fourth-order Runge–Kutta method is used to evaluate the short-time prop-
agator eDdtfor every time step. In this way, we can disentangle the propagation
of the fast system dynamics and the slow dissipative dynamics. It permits us to
propagate the reduced-density matrix for a very long time duration with high
The numbers of the grid points and harmonic basis functions, which are
used to generate the matrix representation of Hamiltonian, lead to a
system Hilbert space of dimension 768. This space is truncated to 500 basis
functions in the propagation of the reduced density matrix. The reduced
density matrix is propagated for 150 ps with a time step of 50 fs.
The observables of primary interest of the present study are the time-
diabatic electronic population probabilities are defined as the expectation
values of the corresponding projection operators with the time-dependent
wave packet. Although the adiabatic electronic population probabilities, Pi
are the observables that most directly reflect the electronic decay dynamics,
therefore consider the diabatic population probabilities, Pi
tive discussion of the nonadiabatic dynamics of the multimode non-Born–
d, for the qualita-
ACKNOWLEDGMENTS. We thank Michael Thoss and Dassia Egorova for many
useful discussions. This work was supported by the Deutsche Forschungsge-
meinschaft (DFG) through a research grant and the DFG-Cluster of Excellence
‘‘Munich Centre of Advanced Photonics’’ (www.munich-photonics.de). The
Leibniz Rechenzentrum der Bayerischen Akademie der Wissenschaften is
acknowledged for providing an ample amount of computing time. L.F. ac-
and support given by the ‘‘Ramo ´n Cajal’’ Program.
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