Role of electron-driven proton-transfer processes in the excited-state deactivation of the adenine-thymine base pair

Exploratory electronic structure calculations have been performed with the CC2 (simplified singles and doubles coupled-cluster) method for two conformers of the adenine (A)-thymine (T) base pair, with emphasis on excited-state proton-transfer reactions. The Watson-Crick conformer and the most stable (in the gas-phase) conformer of the A-T base pair have been considered. The equilibrium geometries of the ground state and of the lowest excited electronic states have been determined with the MP2 (second-order M?ller-Plesset) and CC2 methods, respectively. Vertical and adiabatic excitation energies, oscillator strengths, and dipole moments of the excited states are reported. Of particular relevance for the photochemistry of the A-T base pair are optically dark (1)pipi* states of charge-transfer character. Although rather high in energy at the ground-state equilibrium geometry, these states are substantially lowered in energy by the transfer of a proton, which thus neutralizes the charge separation. A remarkable difference of the energetics of the proton-transfer reaction is predicted for the two tautomers of A-T: in the Watson-Crick conformer, but not in the most stable conformer, a sequence of conical intersections connects the UV-absorbing (1)pipi* state in a barrierless manner with the electronic ground state. These conical intersections allow a very fast deactivation of the potentially reactive excited states in the Watson-Crick conformer. The results provide evidence that the specific hydrogen-bonding pattern of the Watson-Crick conformer endows this structure with a greatly enhanced photostability. This property of the Watson-Crick conformer of A-T may have been essential for the selection of this species as carrier of genetic information in early stages of the biological evolution.     

Photostability versus photodegradation in the excited-state intramolecular proton transfer of nitro enamines: competing reaction paths and conical intersections

The phototautomerization mechanism of a model nitro enamine (NEA) chromophore (incorporated in the structure of a highly photolabile pesticide, tetrahydro-2-(nitromethylene)-2H-1,3-thiazine) has been studied using complete active space self-consistent field reaction path computations. The optically accessible 1pipi* excited state of NEA involves separation of charge and correlates diabatically with the ground state of the tautomerized acinitro imine (ANI) form. For optimum photostabilization, the 1pipi* state of NEA should be S1: in this case, the tautomer would be efficiently formed via a diabatic intramolecular proton-transfer pathway passing through an S1/S0 conical intersection, followed by a facile thermal back proton-transfer reaction. However, in NEA itself the lowest excited states correspond to nitro group 1npi* states, and there are additional surface crossings that provide a mechanism for populating the 1npi* manifold. The above results indicate that the high photolability observed for the pesticide [Kleier, D.; Holden, I.; Casida, J. E.; Ruzo, L. O. J. Agric. Food Chem. 1985, 33, 998-1000] has to be ascribed to photochemistry originating on the 1npi* manifold of states, populated indirectly from the 1pipi* state.     

Study of 7-azaindole in its first four singlet states

The molecular structure and properties of 7-azaindole in its first four singlet states were studied with a view to improving current understanding of the photophysical behavior of its C(2h) dimer. This dimer, which exhibits a double proton transfer via its two hydrogen bonds upon electronic excitation, has for 35 years been used as a model for the photophysical behavior of DNA base pairs. Electronic excitation of 7-azaindole simultaneously increases its acidity and basicity; these changes facilitate a concerted mechanism for the double proton transfer in the dimer. In this work, we found the acidity and basicity changes to occur only in its first pi,pi(*) excited singlet state.     

Ultrafast deactivation of an excited cytosine-guanine base pair in DNA

Multiconfigurational ab initio calculations and QM/MM molecular dynamics simulations of a photoexcited cytosine-guanine base pair in both gas phase and embedded in the DNA provide detailed structural and dynamical insights into the ultrafast radiationless deactivation mechanism. Photon absorption promotes transfer of a proton from the guanine to the cytosine. This proton transfer is followed by an efficient radiationless decay of the excited state via an extended conical intersection seam. The optimization of the conical intersection revealed that it has an unusual topology, in that there is only one degeneracy-lifting coordinate. This is the central mechanistic feature for the decay both in vacuo and in the DNA. Radiationless decay occurs along an extended hyperline nearly parallel to the proton-transfer coordinate, indicating the proton transfer itself is not directly responsible for the deactivation. The seam is displaced from the minimum energy proton-transfer path along a skeletal deformation of the bases. Decay can thus occur anywhere along the single proton-transfer coordinate, accounting for the remarkably short excited-state lifetime of the Watson-Crick base pair. In vacuo, decay occurs after a complete proton transfer, whereas in DNA, decay can also occur much earlier. The origin of this effect lies in the temporal electrostatic stabilization of dipole in the charge-transfer state in DNA.     

Time-resolved photoelectron and photoion fragmentation spectroscopy study of 9-methyladenine and its hydrates: a contribution to the understanding of the ultrafast radiationless decay of excited DNA bases

The excited state dynamics of the purine base 9-methyladenine (9Me-Ade) has been investigated by time- and energy-resolved photoelectron imaging spectroscopy and mass-selected ion spectroscopy, in both vacuum and water-cluster environments. The specific probe processes used, namely a careful monitoring of time-resolved photoelectron energy distributions and of photoion fragmentation, together with the excellent temporal resolution achieved, enable us to derive additional information on the nature of the excited states (pipi*, npi*, pisigma*, triplet) involved in the electronic relaxation of adenine. The two-step pathway we propose to account for the double exponential decay observed agrees well with recent theoretical calculations. The near-UV photophysics of 9Me-Ade is dominated by the direct excitation of the pipi* ((1)L(b)) state (lifetime of 100 fs), followed by internal conversion to the npi* state (lifetime in the ps range) via conical intersection. No evidence for the involvement of a pisigma* or a triplet state was found. 9Me-Ade-(H(2)O)(n) clusters have been studied, focusing on the fragmentation of these species after the probe process. A careful analysis of the fragments allowed us to provide evidence for a double exponential decay profile for the hydrates. The very weak second component observed, however, led us to conclude that the photophysics were very different compared with the isolated base, assigned to a competition between (i) a direct one-step decay of the initially excited state (pipi* L(a) and/or L(b), stabilised by hydration) to the ground state and (ii) a modified two-step decay scheme, qualitatively comparable to that occurring in the isolated molecule.     

Conical intersections in thymine

The mechanisms which are responsible for the radiationless deactivation of the npi* and pipi* excited singlet states of thymine have been investigated with multireference ab initio methods (the complete-active-space self-consistent-field (CASSCF) method and second-order perturbation theory with respect to the CASSCF reference (CASPT2)) as well as with the CC2 (approximated singles and doubles coupled-cluster) method. The vertical excitation energies, the equilibrium geometries of the 1npi*and 1pipi* states, as well as their adiabatic excitation energies have been determined. Three conical intersections of the S1 and S0 energy surfaces have been located. The energy profiles of the excited states and the ground state have been calculated with the CASSCF method along straight-line reaction paths leading from the ground-state equilibrium geometry to the conical intersections. All three conical intersections are characterized by strongly out-of-plane distorted geometries. The lowest-energy conical intersection (CI1) arises from a crossing of the lowest 1pipi* state with the electronic ground state. It is found to be accessible in a barrierless manner from the minimum of the 1pipi* state, providing a direct and fast pathway for the quenching of the population of the lowest optically allowed excited states of thymine. This result explains the complete diffuseness of the absorption spectrum of thymine in supersonic jets. The lowest vibronic levels of the optically nearly dark 1npi* state are predicted to lie below CI1, explaining the experimental observation of a long-lived population of dark excited states in gas-phase thymine.     

Ab initio study on deactivation pathways of excited 9H-guanine

The complete active space with second-order perturbation theory/complete active space self-consistent-field method was used to explore the nonradiative decay mechanism for excited 9H-guanine. On the 1pipi* (1L(a)) surface we determined a conical intersection (CI), labeled (S0pipi*)(CI), between the 1pipi* (1L(a)) excited state and the ground state, and a minimum, labeled (pipi*)min. For the 1pipi* (1L(a)) state, its probable deactivation path is to undergo a spontaneous relaxation to (pipi*)min first and then decay to the ground state through (S0pipi*)(CI), during which a small activation energy is required. On the 1n(N)pi* surface a CI between the 1n(N)pi* and 1pipi* (1L(a)) states was located, which suggests that the 1n(N)pi* excited state could transform to the 1pipi* (1L(a)) excited state first and then follow the deactivation path of the 1pipi* (1L(a)) state. This CI was also possibly involved in the nonradiative decay path of the second lowest 1pipi* (1L(b)) state. On the 1n(O)pi* surface a minimum was determined. The deactivation of the 1n(O)pi* state to the ground state was estimated to be energetically unfavorable. On the 1pisigma* surface, the dissociation of the N-H bond of the six-membered ring is difficult to occur due to a significant barrier.     

7—氮吲哚二体激发态双质子转移的量子化学研究

用AMl和INDO/CI方法研究了7-氮吲哚二体激发态双质子转移反应的位能面和机理,异构二体虽存在较强的分子内氢键,但基态时正常二体的能量仍比异构二体低,光照时正常二体可通过激发态质子转移变为异构二体,这是其荧光产生反常Stokes位移的原因。     

Theoretical study on the singlet excited state of pterin and its deactivation pathway

The excited-state properties and related photophysical processes of the acidic and basic forms of pterin have been investigated by the density functional theory and ab initio methodologies. The solvent effects on the low-lying states have been estimated by the polarized continuum model and combined QM/MM calculations. Calculations reveal that the observed two strong absorptions arise from the strong pi --> pi* transitions to 1(pipi*L(a)) and 1(pipi*L(b)) in the acidic and basic forms of pterin. The first 1(pipi*L(a)) excited state is exclusively responsible for the experimental emission band. The vertical 1(n(N)pi*) state with a small oscillator strength, slightly higher in energy than the 1(pipi*L(a)) state, is less accessible by the direct electronic transition. The 1(n(N)pi*) state may be involved in the photophysical process of the excited pterin via the 1(pipi*L(a)/n(N)pi*) conical intersection. The radiationless decay of the excited PT to the ground state experiences a barrier of 13.8 kcal/mol for the acidic form to reach the (S(1)/S(0)) conical intersection. Such internal conversion can be enhanced with the increase in excitation energy, which will reduce the fluorescence intensity as observed experimentally.     

Conical intersections involving the dissociative 1pisigma* state in 9H-adenine: a quantum chemical ab initio study

The conical intersections of the dissociative 1pisigma* excited state with the lowest 1pipi* excited state and the electronic ground state of 9H-adenine have been investigated with multireference electronic structure calculations. Adiabatic and quasidiabatic potential energy surfaces and coupling elements were calculated as a function of the NH stretch coordinate of the azine group and the out-of-plane angle of the hydrogen atom, employing MultiReference Configuration-Interaction (MRCI) as well as Complete-Active-Space Self-Consistent-Field (CASSCF) methods. Characteristic properties of the 1pipi*-1pisigma* and 1pisigma*-S0 conical intersections, such as the diabatic-to-adiabatic mixing angle, the geometric phase of the adiabatic electronic wavefunctions, the derivative coupling, as well as adiabatic and diabatic transition dipole moment surfaces were investigated in detail. These data are a prerequisite for future quantum wavepacket simulations of the photodissociation and internal-conversion dynamics of adenine.     

Double proton transfer and charge-transfer transitions in biological hydrogen-bonded systems guaninecytosine (GC) and GCMg2+ systems

Potential energy curves for intermolecular proton transfer have been calculated within a modified INDO scheme. Analysis of the nature of the excited states, with emphasis on charge-transfer transitions, has been performed. The proton-transfer probability was found to be markedly greater in some excited states than for the ground state. With the metal ions the double proton transfer should be most effective in charge-transfer states.     

A theoretical study on excited state double proton transfer reaction of a 7-azaindole dimer: an ab initio potential energy surface and its empirical valence bond model

Double proton transfer (DPT) reaction of a 7-azaindole dimer in the first ππ* electronically excited state was studied theoretically. We investigated the reaction mechanism through constructing a full dimensional empirical valence bond potential energy function (PEF) based on potential energies evaluated by ab initio molecular orbital methods, and carrying out quantum dynamics calculations with the PEF. Potential energy surfaces of the DPT obtained at the multi-reference perturbation level of theory favors a concerted DPT mechanism, although a stepwise channel is suggested to open for an excited initial vibrational state. Reduced two dimensional quantum dynamics calculations for a reaction surface Hamiltonian of DPT coordinates were performed. Time constants of the reaction were evaluated to be on the order of picoseconds, which is consistent with experiments. On the other hand, the computed kinetic isotope effect deviates from experimental evidence, suggesting the importance of intermolecular stretching motion, which is not explicit in the present calculations for the quantum effect.     

Intramolecular charge-transfer process of jet-cooled (p-cyanophenyl)pentamethyldisilane: roles of the torsional motion and the Si-Si bond change

To investigate the intramolecular charge-transfer (ICT) process of (p-cyanophenyl)pentamethyldisilane (CPDS), laser-induced fluorescence, dispersed fluorescence, and two-color resonance enhanced two-photon ionization spectra were measured in a jet-cooled isolated condition. Dual fluorescence of CPDS was observed from a ground vibrational level in the locally excited pipi state. Similar to an emission from the charge-transfer (CT) state in solution, one of the dual emissions of the isolated molecule in the jet was assigned as the CT emission. A significant vibrational dependence on the ICT process was found as exciting vibronic levels of the molecule. It was identified that the promoting mode of the ICT process is a torsional motion of the disilanyl group with respect to the phenyl ring. It was also revealed that an effective appearance energy of the CPDS cation via the CT state is much lower than that via the locally excited pipi state suggesting that the electronic configuration of the CT state is similar to that of the cation. On the basis of an electronic configuration of the cationic state, that of the CT state was suggested to be of the (sigma(Si)(-)(Si), 2ppi) type.     

The molecular symmetry and electronic spectroscopy of 7-azaindole dimer: its proton-transfer channels

The potential-energy surfaces for the proton transfer in the doubly hydrogen-bonded dimer of 7-azaindole in its lowest excited electronic states were examined. The dimer with C2h symmetry in its lowest excited electronic states, 2Ag and 1Bu, undergoes concerted double-proton transfer via transition states of the same symmetry placed at energies 4.55 and 4.70 kcal/mol higher, respectively. This suggests that the activation barriers for the double-proton transfer, if any, are lower than 1 kcal/mol. Emission from the dimers resulting from the double-proton transfer involves a Stokes shift of 5605 cm(-1), as theoretically estimated from the 0-0 components of the absortion and emission transitions of the dimer. Surprisingly, however, the calculations suggest that the green emission cannot arise from the 2Ag state generated by a double-proton transfer, because this structure possesses an imaginary frequency. In the 7-azaindole dimer of Cs symmetry, the first excited electronic state, a', lies 4.9 kcal/mol below 1Bu. This excited state a' can be the starting point for single-proton transfers giving a zwitterionic form that can dissociate into the protonated and deprotonated forms of 7-azaindole, the former being electronically excited. This situation of lower symmetry is consistent with the mutational scheme proposed by Goodman [Nature (London) 378, 237 (1995)].     

Femtosecond time- and wavelength-resolved fluorescence and absorption spectroscopic study of the excited states of adenosine and an adenine oligomer

By employing broadband femtosecond Kerr-gated time-resolved fluorescence (KTRF) and transient absorption (TA) techniques, we report the first (to our knowledge) femtosecond combined time- and wavelength-resolved study on an ultraviolet-excited nucleoside and a single-stranded oligonucleotide (namely adenosine (Ado) and single-stranded adenine oligomer (dA)(20)) in aqueous solution. With the advantages of the ultrafast time resolution, the broad spectral and temporal probe window, and a high sensitivity, our KTRF and TA results enable the real time monitoring and spectral characterization of the excited-state relaxation processes of the Ado nucleoside and (dA)(20) oligonucleotide investigated. The temporal evolution of the 267 nm excited Ado KTRF spectra indicates there are two emitting components with lifetimes of approximately 0.13 ps and approximately 0.45 ps associated with the L(a) and L(b) pipi* excited states, respectively. These Ado results reveal no obvious evidence for the involvement of the npi* state along the irradiative internal conversion pathway. A distinct mechanism involving only the two pipi* states has been proposed for the ultrafast Ado deactivation dynamics in aqueous solution. The time dependence of the 267 nm excited (dA)(20) KTRF and TA spectra reveals temporal evolution from an ultrafast "A-like" state (with a approximately 0.39 ps decay time) to a relatively long-lived E(1) "excimer" (approximately 4.3 ps decay time) and an E(2) "excimer-like" (approximately 182 ps decay time) state. The "A-like" state has a spectral character closely resembling the excited state of Ado. Comparison of the spectral evolution between the results for Ado and (dA)(20) provides unequivocal evidence for the local excitation character of the initially photoexcited (dA)(20). The rapid transformation of the locally excited (dA)(20) component into the delocalized E(1) "excimer" state which then further evolves into the E(2) "excimer-like" state indicates that base stacking has a high ability to modify the excited-state deactivation pathway. This modification appears to occur by suppressing the internal conversion pathway of an individually excited base component where the stacking interaction mediates efficient interbase energy transfer and promotes formation of the collective excited states. This feature of the local excitation that is subsequently followed by rapid energy delocalization into nearby bases may occur in many base multimer systems. Our results provide an important new contribution to better understanding DNA photophysics.     

Photodissociation of uracil

We investigate the photochemistry and photodissociation dynamics of uracil by two-colour photofragment Doppler spectroscopy and by two-colour slice imaging at excitation wavelengths between 268 and 235 nm. We observe the loss of a hydrogen atom upon excitation into the pipi* state. The angular distribution indicates a statistical process, while the translational energy distribution agrees with a dissociation that takes place on the electronic ground state. The pipi* state most likely deactivates via the lower-lying npi* state. In addition there is evidence for a second pathway: direct decay of the pipi* state to the electronic ground state with subsequent dissociation. Experiments on uracil-1,3-D(2) show that there is no site selectivity in the dissociation process. No evidence was found for the direct dissociation via a pisigma* excited state that seems to be relevant in the photochemistry of adenine and many other heterocyclic molecules. Overall, the photochemistry of uracil is similar to that of thymine.     

Theoretical study toward understanding ultrafast internal conversion of excited 9H-adenine

The CASPT2/CASSCF method with the 6-311G basis set and an active space up to (14, 11) was used to explore the ultrafast internal conversion mechanism for excited 9H-adenine. Three minima, two transition states, and seven conical intersections were obtained to build up the two deactivation pathways for the internal conversion mechanism. Special efforts were made to explore the excited-state potential energy surfaces near the Franck-Condon region and determine the various barriers in the processes of deactivation. The barrier required from the 1pipi (1La) state to deactivate nonradiatively is found to be lower than that required from the 1pipi (1Lb) state. On 250 nm excitation, the 1pipi (1La) state is populated, and the transition from 1pipi (1La) to the lowest 1npi state involves very low barriers, which may account for the observed short (<50 fs) lifetime of the 1pipi excited state. The deactivation of the lowest 1npi state is required to overcome a barrier of 3.15 kcal/mol, which should be responsible for the 750 fs lifetime of the npi excited state. On 267 nm excitation, the vibrationally active 1pipi (1Lb) state is populated. Excitation at 277 nm prepares the 1pipi (1Lb) state without much excessive vibrational energy, which may be responsible for the observed >2 ps lifetime.     

A three-state model for the photophysics of adenine

An ab initio theoretical study at the CASPT2 level is reported on minimum energy reaction paths, state minima, transition states, reaction barriers, and conical intersections on the potential energy hypersurfaces of two tautomers of adenine: 9H- and 7H-adenine. The obtained results led to a complete interpretation of the photophysics of adenine and derivatives, both under jet-cooled conditions and in solution, within a three-state model. The ultrafast subpicosecond fluorescence decay measured in adenine is attributed to the low-lying conical intersection (gs/pipi* La)(CI), reached from the initially populated 1(pipi* La) state along a path which is found to be barrierless only in 9H-adenine, while for the 7H tautomer the presence of an intermediate plateau corresponding to an NH2-twisted conformation may explain the absence of ultrafast decay in 7-substituted compounds. A secondary picosecond decay is assigned to a path involving switches towards two other states, 1(pipi* Lb) and 1(npi*), ultimately leading to another conical intersection with the ground state, (gs/npi*), with a perpendicular disposition of the amino group. The topology of the hypersurfaces and the state properties explain the absence of secondary decay in 9-substituted adenines in water in terms of the higher position of the 1(npi*) state and also that the 1(pipi* Lb) state of 7H-adenine is responsible for the observed fluorescence in water. A detailed discussion comparing recent experimental and theoretical findings is given. As for other nucleobases, the predominant role of a pipi*-type state in the ultrafast deactivation of adenine is confirmed.     

Study of acyl group migration by femtosecond transient absorption spectroscopy and computational chemistry

The primary photophysical and photochemical processes in the photochemistry of 1-acetoxy-2-methoxyanthraquinone (1a) were studied using femtosecond transient absorption spectroscopy. Excitation of 1a at 270 nm results in the population of a set of highly excited singlet states. Internal conversion to the lowest singlet npi* excited state, followed by an intramolecular vibrational energy redistribution (IVR) process, proceeds with a time constant of 150 +/- 90 fs. The 1npi* excited state undergoes very fast intersystem crossing (ISC, 11 +/- 1 ps) to form the lowest triplet pipi* excited state which contains excess vibrational energy. The vibrational cooling occurs somewhat faster (4 +/- 1 ps) than ISC. The primary photochemical process, migration of acetoxy group, proceeds on the triplet potential energy surface with a time constant of 220 +/- 30 ps. The transient absorption spectra of the lowest singlet and triplet excited states of 1a, as well as the triplet excited state of the product, 9-acetoxy-2-methoxy-1,10-anthraquinone (2a), were detected. The assignments of the transient absorption spectra were supported by time-dependent DFT calculations of the UV-vis spectra of the proposed intermediates. All of the stationary points for acyl group migration on the triplet and ground state singlet potential energy surfaces were localized, and the influence of the acyl group substitution on the rate constants of the photochemical and thermal processes was analyzed.