Leszczynski Nucleic Acid Bases UV

Electronic Spectra, Excited State Structures and Interactions of Nucleic Acid Bases and

Base Assemblies: A Review

http://www.jbsdonline.com

Abstract

A comprehensive review of recent theoretical and experimental advances in the singlet

electronic transitions, excited state structures and dynamics of nucleic acid bases (NABs)

and base assemblies are presented. It is well known that NABs absorb ultraviolet radiation,

but the absorbed energy is efficiently dissipated in the form of ultrafast internal conversion processes believed to occur in the subpicosecond time scale and, therefore, enabling NABs

highly photostable. It is not known how much evolutionary role was played in evolving these

molecules and the ultimate selection by nature as genetic materials, but it is well accepted

that survival-of-fittest prevails. Recently, significant efforts have been continuously paid to understand the mechanism of electronic excitation deactivation, but universally acceptable

mechanism is still elusive. However, recent investigations reveal that electronic excited state

geometries of DNA bases are usually nonplanar and this structural nonplanarity may facilitate

nonradiative deactivation. Investigation of excited state structures is challenging and, there-

fore, it is not surprising that despite the impressive theoretical and computational advances,

this research area is still hampered by the methodological and computational limitations.

Further, stacking has significant influence on the emission properties of molecules. The 2-aminopurine, a fluorescent adenine derivative frequently used in studying DNA dynamics, shows significant attenuations in fluorescence quantum yield when incorporated in the DNA. Theoretical and computational bottlenecks limit a thorough theoretical understanding of ef-fect of stacking interactions on the excited state dynamics of NABs. Despite these limitations

the investigations of excited state properties are progressing in the right direction and our

better understanding of excited state structure and dynamics of NABs and nucleic acids may

help to design preventive strategy for radiation induced illness and photostable materials.

Key words: Nucleic acid bases; Base pairs; Electronic transitions; Excited states; and

Nonradiative decay.

Introduction

The genetic code in deoxynucleic acid (DNA) is stored in the form of hydrogen bonded purine and pyrimidine bases, the specific patterns of which is unique for each individual. Alteration in DNA structure may lead to mutation by producing a

permanent change in the genetic code (1). It has long been speculated that proton

transfer may lead to mispairing of bases and thus causing point mutations. Some

theoretical investigations on model systems have suggested that the excited state

proton transfer proceeds through small barrier height and in some cases it is even

barrierless (2, 3). Computational studies on adenine, guanine, and hypoxanthine, on the other hand, have suggested that excited state proton transfer barrier height is

significantly large and, therefore, electronic excitation may not facilitate such pro-

cesses in the excited state for these species (4-6). The exact cause for mutation is not known, but several factors, e.g., environment, irradiation, et cetera, may contribute

towards it. It is well known that nucleic acid bases (NABs) absorb ultraviolet (UV)

Journal of Biomolecular Structure &

Dynamics, ISSN 0739-1102

Volume 25, Issue Number 1, (2007)

©Adenine Press (2007)

M. K. ShuklaJerzy Leszczynski*

Computational Center for Molecular Structure and Interactions

Department of ChemistryJackson State University

Jackson, Mississippi 39217, USA

93

*Phone: 601-979-3723Fax: 601-979-7823Email: [email protected]

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Shukla and Leszczynski

radiation efficiently. The formation of pyrimidine dimers between adjacent thymine bases on the same strand results in the most common UV-induced DNA damage (7, 8). Recent investigations suggest that low energy radiation (even less than 3 eV) may also be fatal for the stability of nucleic acid polymers (9, 10). However, the high photostability of NABs is perhaps the reason for their selection as genetic spe-

cies by nature. The high photostability of NABs is associated with the ultrafast non-

radiative decay of absorbed radiation and, therefore, these species show very poor

fluorescence; the fluorescence quantum yield being in the order of 10-4 (11-14).

Recently, impressive progress has been made investigating the excited state dy-

namics of NABs at the picosecond and femtosecond time domains (12). These studies clearly show that the excited state life-times of genetic molecules are in the

sub-picosecond order and they show very complex excited state dynamics (12). Different possible mechanisms for the ultrafast nonradiative decay in nucleic acid

bases have been suggested and they will be discussed in detail latter. They include the out-of-plane vibronic coupling of closed lying electronic ππ* and nπ* states (15, 16) and conical intersection between excited and ground states through some

reaction coordinates (12, 17-24). It is clear that excited state geometries of NABs are generally nonplanar and this nonplanarity plays pivotal role in assisting the

ultra-fast nonradiative decay (12-14, 17-25). Further, we have also shown that mo-

lecular environments, e.g., base pairing, hydration, et cetera, have significant effect on the characteristics of excited state structural nonplanarity and, thus, excited state

dynamics would have significant dependency on the molecular environment (26-28). It should be noted that excited state geometries of these molecules are yet not known experimentally; only few studies have indicated the possibility of nonplanar

excited state geometry (29-32). Billinghurst and Loppnow (31) have studied the excited state structural dynamics of cytosine using the resonance Raman spectros-

copy and time-dependent wave packet analysis and found excited state structural

changes consequent to electronic excitation. These authors also computed the dis-

tribution of reorganization energy consequent to electronic excitation and found that among pyrimidine bases, the thymine has the largest (66%) and uracil has the

lowest (13%) contribution of the reorganization energy along the photochemical relevant coordinates while the contribution for cytosine was revealed to be 31%. The percent contribution of reorganization energy was predicted in agreement with the photodimeric activities of these bases, according to which the thymine shows

the most and uracil shows the least UV induced photodimerization reaction.

The fluorescence for purine bases (adenine and guanine) are known to originate from the rare tautomer (keto-N7H for guanine and amino-N7H for adenine) (11). However, there is at least one low temperature study which shows that the fluo-

rescence excitation and emission spectra of guanine do not agree with that of the

7-methylguanine; thus, suggesting that the fluorescence in guanine sample does not originate from the minor tautomeric form (33). The positions of substitutions have been found to have profound effect on the photophysical properties of purine bases.

For example, the parent molecule, purine, is well know to exhibit strong phospho-

rescence and insignificant fluorescence. On the other hand 2-aminopurine shows very strong fluorescence and no phosphorescence (11, 34). The photophysical prop-

erties of adenine (6-aminopurine) are in between that of purine and 2-aminopurine. Consequently, adenine shows weak fluorescence and weak phosphorescence.

The last substantial review on excited state properties of nucleic acid systems was done by Callis in 1983 (11). In this review, he performed an excellent analysis of ex-

perimental and theoretical results of electronic transitions of nucleic acid bases and

related analogues. But it should be noted that in the early eighties theoretical results

were limited to semiempirical methods (the ab initio calculation for this class of

molecules were almost impossible at that time). An excellent review article on nu-

cleic acid bases has also appeared recently from Kohler’s group (12) and it is mostly devoted to the ultrafast excited state dynamics of bases and base assemblies. The

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95Electronic Spectra,

Excited State Structures, and Interactions of Nucleic

Acid Bases and Base Assemblies

present review focuses on the recent theoretical and experimental advances in the

excited state structures and interactions of nucleic acid bases and base assemblies.

Ground State Structures and Properties of Nucleic Acid Bases and Base Pairs

The nucleic acid bases are well known to exhibit various tautomeric phenomena in different environments. Although, the presence of sugar in nucleic acid polymers

blocks the prototropic tautomerism (N9 ↔ N7 in adenine and guanine and N1 ↔ N3 in cytosine), it does not stop the possibility of the formation of other tautomeric forms (enol and imino). Different ground state properties (e.g., geometries, tautom-

erism, transition states corresponding to the proton transfer from the canonical form

to the rare tautomeric form, base pair formation, stacking interactions, interactions

with metal ions, and hydration) have been discussed in detail in recent review ar-

ticles (35-37). Therefore, only brief description of ground state properties of NABs and base pairs would be presented here.

Earlier experimental investigations have suggested the existence of only two tau-

tomers (N9H and N7H) of adenine; the N9H tautomer is the major form while the relative population of the N7H tautomer has been found to depend upon the environment (38-40). Recent experimental investigation supplemented with theory suggests the existence of three tautomers [N9H (major), N7H and N3H (both mi-nor)] of adenine in dimethyl sulfoxide solution (41). The theoretical calculations also show that although the N9H tautomer is the global minima, the relative stabil-ity of the N3H tautomer is very close to that of the N7H tautomer (42, 43). High level experimental and theoretical investigations performed recently suggest that

the tautomeric equilibria of guanine are very complex. The existence of up to four tautomers of guanine (keto-N9H, keto-N7H, enol-N9H, and enol-N7H) has initial-ly been suggested using the jet-cooled resonance enhanced two photon ionization

(R2PI) spectroscopic investigations (44, 45). However, Choi and Miller (46), on the basis of the comparison of the experimental IR spectra of guanine trapped in the helium droplet and theoretically computed frequencies at the MP2 level using the 6-311++G(d,p) and aug-cc-pVDZ basis sets, have recently assigned the presence of only keto-N9H, keto-N7H, and cis- and trans forms of the enol-N9H tautomer of guanine. Based on the results of Choi and Miller (46), Mons et al. (47) have reas-

signed their experimental findings and accordingly the enol-N9H-trans, enol-N7H, and two rotamers of the keto-N7H-imino tautomers of guanine are present in the supersonic jet-beam. However, it is surprising, since imino tautomers are much less

stable than the canonical form of guanine and probably they are formed during the

laser desorbtion of guanine in the experiments.

It is generally believed that the pyrimidine bases uracil and thymine exist mainly in

the keto form (35-37). However, the existence of a small amount of the enol tauto-

mer in aqueous solutions of 5-chlorouracil at room temperature has been suggested by Suwaiyan et al. (48). A trace amount of the enol form of thymine in aqueous solutions has also been suggested by Morsy et al. (49) on the basis of extensive UV/Vis absorption and fluorescence measurements. Although, the Hobza group (50) does not support the utility of experiments used by Morsy et al. (49) in tautomer detection, but do not completely ruled out the presence of trace amount of minor

tautomers in the water solution. Cytosine exists as a mixture of the amino-hydroxy and amino-oxo (N1H) tautomeric forms with the equilibrium being shifted slightly towards the former tautomeric form in the argon and nitrogen matrices (51, 52). A matrix isolation study of 1-methylcytosine and 5-methylcytosine indicates the

existence of the imino-oxo tautomeric form (53, 54). Three tautomers (amino-oxo, imino-oxo, and amino-hydroxy) of cytosine have been found in a microwave study

(55). In aqueous solutions both of the amino-oxo forms (N1H and N3H) are present (56). In crystals, mainly the N1H amino-oxo form is found (57). The theoretical re-

sults for cytosine are available up to the CCSD(T) level of theory using a complete basis set approach in which the energies are obtained by applying an extrapolation

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technique (58). It has been found that the coupled-cluster approach with single, double, and triple excitations [CCSD(T)] is necessary to predict the relative stabil-ity of cytosine tautomers (59). In the gas phase the amino-hydroxy tautomer is pre-

dicted to be the most stable; however, under aqueous solvation tautomeric stability is found to be shifted to the canonical amino-oxo form (58, 60).

It is established that the amino groups of NABs are pyramidal due to the partial sp3

pyramidalization of the amino nitrogen (35-37, 61). The amino group pyramidali-zation of guanine is highest among the nucleic acid bases (35-37). Experimental evidence for the nonplanarity of adenine and cystosine has been recently indicated

in the vibrational transition moment direction measurement study by Dong and

Miller (62). Further, it has also been revealed theoretically that the pyrimidine ring in the NABs possesses high conformational flexibility (63, 64).

The electron (proton) affinity of a molecule is measured in terms of the amount of energy released when an electron (proton) is added to the molecule. It is com-

puted as the energy difference between the neutral and anionic (cationic) forms

of the molecule. Ionization potential on the other hand is defined as the amount of energy required to remove an electron from a molecule. It is computed as the energy difference between the cationic and neutral forms of the molecule. In a

recent theoretical study, Li et al. (65) with the help of available experimental data

have estimated the value of adiabatic valence electron affinities to be in the range of 0-0.2 eV for pyrimidines and about -0.35 and -0.75 eV for adenine and guanine, respectively. The purines have lower and pyrimidines have higher ionization po-

tentials and it is clear that guanine has the lowest ionization potential among the

nucleic acid bases and, therefore, is the most susceptible for oxidation under irradi-

ation (66-71). Experimental (72-74) and high level theoretical investigations (75-77) were also performed to determine the protonation and deprotonation (basicity and acidicity) properties of the different sites of nucleic acid bases. Our group (75) has computed proton affinities of all nucleic acid bases up to the MP4(SDTQ) level and found that the computed proton affinities are very close to the experimental data; the computed error was found to be within the 2.1%.

The Watson-Crick (WC) base pair geometries are generally planar including the amino group at the HF and DFT levels (35, 37, 78-80). At the MP2 level with smaller basis sets, the amino groups of the WC GC and AT base pairs are pyra-

midal, but with larger basis sets the corresponding group of the AT base pair was revealed almost planar (80, 81). It has been suggested that the nonplanarity of GC base pair may enhance the stacking of bases on the strand and may increase the sta-

bility of the helix (81). The structural properties of different reverse Watson-Crick (RWC), Hoogsteen (H), and reverse Hoogsteen (RH) base pairs have also been investigated, and the geometries of some of them have been found to be nonplanar

(35, 37, 82). Recently, the energetics of hydrogen bonded and stacked base pairs were studies up to the CCSD(T) level (83-85). Kumar et al. (86, 87) have recently investigated the adiabatic electron affinities of GC, AT, and hypoxanthine-cytosine base pairs at the DFT level and found the significant increase in the electron af-finity of the AT base pair under the polyhydrated environments. A comprehensive investigation of structure and properties of deprotonated GC base pair was recently performed by Schaefer and coworkers (88).

Excited State Properties of Nucleic Acid Bases

Ground state geometries of nucleic acid bases are planar (except the amino group, which is pyramidal) (35-37, 61), while the corresponding excited state geometries are generally nonplanar (4-6, 12-14, 25-28, 89-97). The excited state structural nonpla-

narities may facilitate the ultrafast nonradiative decay in bases and base assemblies

(12-14, 17-25, 96). The modes of interaction of NABs with water molecules are also found to be different in the electronic excited states compared to the ground state (26,

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28, 98-101). The hydrogen bond accepting sites under the nπ* excitations provide repulsive potential for hydrogen bonding interactions (100, 101). Consequently base pairs are destabilized under such excitations (78, 79). In femtosecond spectroscopic investigations of adenine-water clusters, the adenine-water hydrogen bonds were

found to be dissociated on the nπ* potential energy surfaces of adenine (98, 99).

Electronic Transitions

Adenine: In 1954 Mason first suggested that the main absorption band of adenine observed near 260 nm (4.77 eV) consists of two electronic transitions differing with respect to the relative intensity and the transition moment directions measured ac-

cording to the DeVoe-Tinoco convention (Fig. 1) (102). However, in the vapor phase and in a trimethyl phosphate (TMP) solution of adenine, these transitions are not resolved (103, 104). In the water solution, a stronger transition appearing at 261 nm (4.75 eV) is short axis polarized, while another transition appearing as a weak shoulder near 267 nm (4.64 eV) is long axis polarized (105). Similar results were also found in the linear dichroism (LD) spectra of 9-methyladenine partially orient-ed in stretched polymer poly(vinyl alcohol) films (106), in the polarized absorption spectra of 9-methyladenine in crystal environments (105), and in the photoacoustic spectra of the evaporated film of adenine (107). However, the splitting between these two transitions appreciably increases in a crystal environment compared to

solution (105). In the photoacoustic spectra (107), four absorption peaks were re-

vealed in the 300-180 nm region with stronger transition found near 270 nm (4.59 eV) and a weaker transition detected near 290 nm (4.28 eV). It is interesting to note that the splitting of the 260 nm band is observed generally in all experiments, in linear dichroism (LD) (106, 108, 109), in magnetic circular dichroism (MCD) (110, 111), in single crystal absorption (105, 112), in fluorescence polarization (113), and

N1

C2H2

N3

C4

C5

C6

N6H61 H62

N7

C8H8

H9

N9

N1

C2

N3

C4

C5

C6

O6

N7

C8H8

N9

H9

N2

H21

H22

H1

Adenine (A) Guanine (G)

N1

H1

C2

O2

N3

H3

C4

O4

C5

C6

H6

R5

N1

H1

C2

O2

N3

C4

N4

C5

H5

C6

H6

H41H42

Uracil (U) (Thymine (T)) Cytosine (C)

N1’C2’

O2’

N3’H3’

C4’

O4’

C5’

C6’H6’

H1’

N1

C2

H2

N3

C4

C5 C6

N6

H61H62

N7

C8

N9

H8

H9

R5’

N1’

H1’

C2’

O2’

N3’

C4’

N4’H41’ H42’

C5’

H5’

C6’H6’N1

H1C2

N2H21

H22

N3

C4

C5 C6

O6N7C8

N9

H9

H8

AU(T) base pair GC base pair

Figure 1: Structure and atomic numbering schemes of

nucleic acid bases and Watson-Crick base pairs. In ura-

cil, R5/R5’=H and in thymine, R5/R5’=CH3. The Φ

represents the transition moment direction according to

the DeVoe-Tinoco convention (11).

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in substituent effects (114), but it has not been found in the CD spectra (115-117). The transition moment direction (according to the DeVoe-Tinoco convention, Fig. 1) for the stronger component is found to be -3º for 9-methyladenine in single crystals

Table I Summary of experimental transition energies ( E, eV) of adenine, guanine, thymine, uracil, cytosine, and their derivatives. The ‘f’ represents oscillator strength and represents transition moment direction (°) according to the Devoe-Tinoco convention (Figure 1).

secnerefeR snoitisnarT/eluceloMAdenine

artcepS noitprosbA E 4.92 5.99 Adenine, vapor (103) E 4.77 5.96 Adenine, TMP (103) E 4.81 5.85 9MA, MCH (103) E 4.77 5.90 9MA, TMP (103) E 4.77 5.99 Adenine, water (104) E 4.59 4.77 5.90 Adenine, water (130) E 4.63 4.77 6.05 Adenine, water (110) E 4.77 6.02 Adenosine, water (110) E 4.59 5.90 6.81 7.75 Adenine sublimed film (164) E 4.51 4.68 5.82 6.08 6.81 7.75 9MA, crystal (120)

f 0.1 0.2 0.25 0.11 0.30 0.23 83 25 -45 15 72 6

LD spectra E 4.55 4.81 5.38 5.80 5.99 9MA, stretched film (106)

f 0.047 0.24 0.027 0.14 0.12 66 19 -15 -21 -64

artceps DC E 4.63 5.93 6.36 Adenines, water (115) E 4.77 5.74 6.36 6.63 Adenines, water (116) E 4.68 5.51 Adenosine, water (110)

MCD spectra E 4.59 4.92 5.90 Adenine, water (110) E 4.56 4.90 5.77 Adenosine, water (110)

Photo acoustic spectra E 4.28 4.59 6.20 6.89 Adenine, film (107)

gnirettacs nortcelE E 4.53 5.84 6.50 7.71 Adenine, film (116)

Guanine Absorption Spectra

E 4.46 5.08 6.20 6.57 Guanine, model (132) f 0.15 0.24 0.40 0.48

-12 80 70 -10 E 4.51 5.04 6.33 Guanine, water (104) E 4.56 5.04 6.19 6.67 Guanosine, water (132)

f 0.15 0.24 0.40 0.48 a -24 88 86 -8 to 44 E 4.56 4.98 6.02 6.63 9EtG, water (131)

f 0.14 0.21 0.38 0.42 E 4.51 4.84 6.11 6.52 9EtG, TMP (114) E 4.51 4.92 6.05 6.59 9EtG, water (114) E 4.46 4.88 5.46 6.08 6.56 9EtG, crystal (131)

f 0.16 0.25 <0.05 0.41 0.48 -4 -75 -75 -9

E 4.35 5.00 6.23 6.70 Guanine, sublimed film (164) LD Spectra

E 4.43 5.00 Guanine, stretched film (109) 4 -88

CD Spectra E 4.51 4.92 5.51 6.20 6.63 dGMP, water (116) E 5.06 5.77 Guanosine, water (110)

MCD Spectra E 4.46 5.00 Guanosine, water (110)

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(transition being at 275 nm) (105, 112), while it amounts to 9º in the film dichroism study (transition being at the 263 nm) (109). In the case of the protonated adenine, transtion moment of the strong transition near 257 nm (4.82 eV) makes an angle of 100º, while that of the weak transition near 273 nm (4.54 eV) is -28º with respect to the C4C5 direction (118). An extensive and elegant work in this regard was per-formed by Clark (119, 120) to model the electronic spectra of adenine in the UV and vacuum UV region. In this study, he has measured the polarized spectra of crystals

of 9-methyladenine and 6-(methylamino)purine and assigned eight bands of adenine along with their transition moment directions and oscillator strengths. The strong transition (265 nm) of the main UV absorption band was shown to be polarized at 25º and weaker transition (near 275 nm) was found to be polarized close to the long molecular axis. The transition moment directions of several transitions of 9-methyl and 7-methyl adenine samples (9MA and 7MA) oriented in stretched polymer films were also measured (106). The existence of a new ππ* transition near 5.38 eV for 9MA (which had not previously been observed) was also revealed. The measured transition moment directions for the first two transitions are generally in agreement with those suggested by Clark (119, 120). However, the transition moment direc-

tions for higher energy transitions are different from those obtained by Clark (120).

Table I Continued Uracil Absorption Spectra

E 5.08 6.05 6.63 Uracil, vapor (103) E 4.84 6.05 6.63 1,3-dimethyluracil, vapor (103) E 4.68 6.08 6.63 1,3-dimethyluracil, water (103) E 4.81 6.11 Uracil, water (110) E 4.75 6.05 Uridine, water (110) E 4.81 6.11 6.85 Uracil, TMP (114) E 4.79 6.14 6.85 Uracil, water (114) E 4.70 6.02 6.74 1,3-dimethyluracil, TMP (114) E 4.73 6.11 6.81 1,3-dimethyluracil, MCH (114) E 4.51 5.82 1-methyluracil, crystal (151)

-9 59 E 4.66 6.08 6.97 7.90 Uracil, sublimed film (164)

CD spectra E 4.73 5.77 6.36 7.00 Uridine, water (116) E 4.63 5.71 Uridine, water (110) E 4.68 5.82 6.26 Uridine, water (115)

MCD spectra E 4.86 5.85 Uracil, water (110) E 4.77 5.71 Uridine, water (110)

Electron Scattering E 4.70 5.93 6.93 Uracil, film (146)

Thymine Absorption Spectra

E 4.68 6.08 Thymine, water (110) E 4.64 6.05 Thymidine, water (110) E 4.54 5.99 1-methylthymine, water (105)

f 0.19 0.28 E 4.64 5.88 7.04 Thymine, sublimed film (164)

CD spectra E 4.68 5.77 6.36 7.00 Thymidine, water (116) E 4.54 5.69 Thymidine, water (110) E 4.63 5.85 6.42 Thymidine, water (115)

MCD spectra E 4.71 5.77 Thymine, water (110) E 4.73 5.64 Thymidine, water (110)

Photo Acoustic spectra E 4.59 5.90 7.08 Thymine, film (107)

Electron scattering E 4.66 5.94 7.08 8.82 Thymine, film (146)

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The existence of a transition near 230 nm (5.39 eV) was also indicated in the MCD (110) and CD (115, 116) spectra, but on the basis of the semiempirical calculations this transition was assigned as being of the nπ* type (11). The experimental elec-

tronic transitions of NABs and their derivatives are summarized in Table I.

The tentative assignment of the existence of nπ* transitions near 244 and 204 nm (5.08 and 6.08 eV) in the crystal of 2ʹ′-deoxyadenosine was made by Clark (121). The possibility of the existence of such nπ* transitions is also supported from a recent theoretical study (78). There are also some investigations suggesting the existence of an nπ* transition near the first singlet ππ* transition (94, 98, 99, 106, 122). The linear dichroism measurements of adenine derivatives partially oriented in stretched polymer poly(vinyl alcohol) films have yielded the existence of an nπ* transition near the first ππ* absorption transition in 9-methyl adenine (106). Simi-lar results were also found in the molecular beam study of hydrated adenine clusters

(98, 99). The existence of the nπ* transition as the first transition (the energy is very close to the first ππ* transition) in adenine in the gas phase is also predicted at the time dependent density functional theory (TDDFT) and the multi-reference perturbation configuration interaction method (known as CIPSI) (94). Kim et al.

(122) have performed REMPI and fluorescence studies of jet-cooled adenine and have suggested that the first transition of adenine has nπ* character with the 0-0 band located at 35503 cm-1 (~281.7 nm, ~4.40 eV), while the corresponding band of the first ππ* transition is located at 36108 cm-1 (~276.9 nm, ~4.48 eV). Luhrs et al. (123) have performed a similar study of adenine and 9MA, but their results do not support the assignment of the nπ* transition suggested by Kim et al. (122). Luhrs et al. (123) have speculated that the nπ* peak observed by Kim et al. (122) may be due to the formation of other tautomers of adenine since the latter study

involved the use of higher temperatures in heating the sample. Luhrs et al. (123) have observed the 0-0 band of the first ππ* transition of adenine and 9MA at 36105 cm-1 (~277 nm, ~4.48 eV) and 36136 cm-1 (~276.7 nm, ~4.48 eV), respectively,

Table I Continued Cytosine Absorption Spectra

E 4.66 5.39 5.85 6.29 Cytosine, water (165) f 0.14 0.03 0.13 0.36

b 6 -46 76 -27 or 86 E 4.64 6.31 Cytosine, water (104) E 4.57 5.39 6.26 Cytidine, water (104) E 4.48 5.23 6.08 6.63 Cytosine, TMP (114) E 4.59 5.28 5.74 6.26 dCMP, water (116) E 4.64 5.21 5.83 6.46 Cytosine, water (167)

f 0.096 0.100 0.211 0.639 E 4.57 5.34 5.77 6.26 Cytidine, water (166) E 4.57 6.17 Cytosine, sublimed film (164) E 4.54 5.40 6.07 6.67 7.35 Cytosine, sublimed film (168)

f 0.058 0.073 0.115 0.072 0.072 LD spectra

E 4.63 5.17 Cytosine, polymer film (109) 25±3 6±4

or or -46±4 -27±3

artceps DC E 4.59 5.27 5.74 6.14 6.56 7.38 dCMP, water (116) E 4.59 5.02 5.64 6.36 Cytosine nucleosides (169) E 4.59 5.17 5.64 6.36 Cytidinec (169)

TMP, Trimethylphosphate; 9MA, 9-methyladenine; MCH, Methylcyclohexane; Adenines, Adenine derivatives: For details see relevant references. aBased on polarized absorption spectra of crystalline guanosine (132); 9EtG, 9-ethylguanine; TMP, Trimethylphosphate: For details see relevant reference. bBased on polarized spectra of cytosine crystal (165); TMP, Trimethylphosphate: For details see relevant reference. cBased on CD and absorption measurements of cytosine nucleosides in different solvents (water, acetonitrile, dioxane, 1,2-dichloroethane).

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and these results are in accordance with the observation made by Kim et al. (122). Similar results were also found from the REMPI study by Nir et al. (124) who used the laser desorption technique instead of heating the samples.

The first ab initio calculations of the electronic transitions of adenine (and gua-

nine) were performed at the multi-reference configuration interaction (MRCI) and random phase approximation (RPA) levels using the ground state self-consistent field orbitals with double-ζ/polarization/diffuse gaussian basis set utilizing the ex-

perimental molecular geometry and assuming its planarity (125). The computed transition energies were higher by 1.48-1.86 eV compared to the experimental tran-

sition energies, and linear scaling was needed for comparison with experimental

data. Roos and coworkers (126) have used the CASSCF/CASPT2 level of theories applying a large ANO-type basis set to study the electronic transitions of the planar form of adenine. As expected, the CASPT2 correlation correction to the CASSCF energies yielded significant improvements in the CASSCF excitation energies and were found to be in reasonably good agreement with the corresponding experimen-

tal data. The TDDFT (94, 127-129) and configuration interaction singles (CIS) (13, 14, 93, 94, 96) methods were also used to study the excited state properties of adenine with reasonable success. The scaled [scaling factor 0.72 (13, 14, 78, 96)] CIS transition energies were found to be in good agreement with the experimental data and the corresponding CASPT2 transition energies. It should be noted that, unless otherwise stated, the discussed CIS computed transition energies of NABs in comparing with the corresponding experimental data and other theoretical results in

the current manuscript correspond to the scaled values.

Table II shows the vertical singlet ππ* and nπ* transition energies, transition mo-

ment directions and dipole moments of the adenine tautomers (N9H and N7H), their hydrated forms obtained at the CIS/6-311G(d,p)//HF/6-311G(d,p) level (13, 14), along with the CASSCF and CASPT2 excitation energies (126), and some experimental data. The super molecular approach considering three water mole-

cules in the first solvation shell of the adenine tautomers was used to model aque-

ous solvation. The first ππ* transition of the N9H tautomer is stronger, while the second ππ* transition is predicted to be much weaker. After hydration the transi-tion energy of the weaker transition is decreased; therefore, the stronger transition

becomes the second transition (Table II). Experimentally, a weak shoulder near 270 nm (4.59 eV) and a strong peak near 260 nm (4.77 eV) in the water solution are observed (130). Thus, the calculated transitions of the hydrated N9H tauto-

mer are in a qualitative agreement with the experimental data (130), although the computed splitting between the two transitions is too small (Table II). Further, the experimental transition energies shown in Table II can be explained within an accuracy of 0.2 eV in terms of the scaled computed transition energies of the hy-

drated N9H tautomer. The CIS calculation predicts that the two scaled transitions computed at 6.18 and 6.24 eV for the isolated N9H tautomer and at 6.12 and 6.17 eV for its hydrated form (Table II) would contribute to the 6.2 eV experimental region of the molecule (Table I). The calculation predicts that the transition mo-

ment directions of these transitions would be approximately perpendicular to each

other (Table II). The MCD results suggest that the UV-absorption band in the 200 nm (6.2 eV) region is composed of two transitions with non-parallel transition dipole moments (111). Therefore, the theoretical CIS results may correspond to the MCD observation in this regard. Although the predicted weak transition near 5.38 eV in the LD spectra of 9MA (106) is not obtained in the calculations; however, it was calculated for the planar form of adenine (78). The agreement between the CIS computed singlet ππ* transition energies of the N7H tautomer and those obtained by CASPT2 calculations (126) and the LD technique (106) is good for the first two transitions; however, such agreement is not reached for higher energy transitions (Table II). Due to the close proximity of the computed transition energies of the N7H tautomer and its hydrated form to those of the N9H tautomer and its hydrated form, contributions to the observed spectra of adenine

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102


from the N7H form cannot be ruled out. It is known from different experimental and theoretical studies that the N7H tautomer is present along with the N9H form under different environmental conditions (38-43).

Three nπ* transitions near 5.18, 5.52, and 5.74 eV (scaled values) for the N9H tautomer of adenine are predicted at the CIS/6-311G(d,p) level. The correspond-

ing values for the hydrated form are 5.38, 5.75, and 5.97 eV, respectively (Table II). The computed first nπ* transition may be related to that indicated in the MCD (110) and CD (115, 116) spectra in the 230 nm (5.39 eV) region as discussed earlier. Further, it can also be suggested as the possible source of the first nπ* transition located near 244 nm (5.08 eV) as indicated in 2ʹ′-deoxyadenosine (121). Although, it is not possible to relate the second computed nπ* transition with experiment, the third computed transition near 5.97 eV (hydrated form) corresponds to the 204 nm (6.08 eV) transition of 2ʹ′-deoxyadenosine (121).

Guanine: The existence of five electronic transitions in the UV region has been suggested in guanine (11, 126). The first transition lies near 275 nm (4.51 eV) and the second appears near 250 nm (4.96 eV); the intensity of the latter being larger than the former one (11, 110, 114, 126, 131-135). The third transition is located in the 225 nm (5.51 eV) region. It is a weak transition with the oscillator strength in the range of 0.01-0.03 and is not very often observed. Evidence for the existence of such a band is found in the CD spectra (116, 117), in the crystal spectra of gua-

nine and 9-ethylguanine, and in aqueous solutions of protonated guanine (131). However, definite information could not be obtained from the CD spectra and this

Table II Vertical singlet * and n * excitation energies ( E, eV), oscillator strengths (f), transition moment directions ( , ), and dipole moments ( , Debye) of the N9H and N7H tautomers of adenine in the isolated and hydrated forms at the CIS/6-311G(d,p)//HF/6-311G(d,p) level (13, 14).

CIS Experimental Dataa

detardyH detalosICASPT2/CASSCFb

Abs Crystal LD E f c Ed E f Ed E1/ E2/f/ / E E/f/ E/f/

N9H * Transitions

6.61 0.394 60 2.85 4.76 6.61 0.440 50 4.76 5.20/6.48/0.37/37/2.30 4.77 4.68/0.2/25 4.81/0.24/19 6.65 0.024 -6 3.40 4.79 6.59 0.038 -66 4.74 5.13/5.73/0.07/23/2.37 4.59 4.51/0.1/83 4.55/0.047/66 8.20 0.398 -38 0.83 5.90 8.09 0.342 -31 5.82 6.24/7.80/0.851/-57/2.13 5.90 5.82/0.25/-45 5.80/0.14/-21 8.58 0.447 15 2.02 6.18 8.50 0.423 19 6.12

6.21e 6.15f 6.72/8.30/0.159/40/4.60 6.08/0.11/15 5.99/0.12/-64 8.67 0.547 -87 3.14 6.24 8.57 0.589 -77 6.17 9.39 0.232 29 2.65 6.76 9.41 0.375 23 6.78 6.99/8.77/0.565/27/3.42 6.81/0.30/72

n * Transitions 7.19 0.001 - 2.47 5.18 7.47 0.000 - 5.38 6.15/6.43/0.001/-/2.14 7.66 0.002 - 0.93 5.52 7.99 0.001 - 5.75 6.86/7.16/0.001/-/1.93 7.97 0.014 - 1.62 5.74 8.29 0.015 - 5.97

N7H

* Transitions 6.38 0.162 35 6.83 4.59 6.36 0.175 28 4.58 4.61/5.12/0.050/23/5.95 4.54/0.11/45 6.78 0.051 3 6.51 4.88 6.84 0.103 16 4.92 4.97/6.63/0.187/-10/9.64 4.90/0.094/-16 8.06 0.766 81 6.87 5.80 7.99 0.765 77 5.75 6.02/7.81/0.363/3/8.68 5.28/0.052/-28 8.27g 0.163 -44 1.75 5.95 8.44 0.579 -32 6.08 6.15/7.22/0.123/-49/6.70 5.68/0.16/76 8.47 0.377 -12 6.00 6.10 8.55 0.207 69 6.16 6.32/8.12/0.077/52/6.72 5.91/0.19/-29

n * Transitions 6.87 0.012 - 4.73 4.95 7.24 0.004 - 5.21 7.33 0.002 - 6.32 5.28 7.61 0.001 - 5.48 7.78 0.014 - 4.24 5.60 8.11 0.015 - 5.84

aAbs, Absorption in aqueous medium (130); Crystal, based on the polarized spectra of single crystals of 6-(methylamino)purine and 9-methyladenine (120); LD, LD spectra of 9-methyladenine and 7-methyladenine oriented in stretch poly(vinyl alcohol) film (106); b E1 corresponds to CASPT2 and E2

corresponds to CASSCF transition energies (126); cGround state dipole moments of the N9H and N7H tautomers at the HF/6-311G(d,p) level are 2.51 and 6.83 Debye, respectively; dScaled (scaling factor 0.72) excitation energies; eAverage of transitions at 6.18 and 6.24 eV; fAverage of transitions at 6.12 and 6.17eV; gRydberg contamination.

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transition was suggested to be due to a weak ππ* or nπ* transition (116). The fourth and fifth transitions are intense and located near 204 nm (6.08 eV) and 188 nm (6.59 eV), respectively (11, 114, 131, 132). The existence of three nπ* transitions near 238, 196, and 175 nm (5.21, 6.32, and 7.08 eV) in guanine has been suggested by Clark, but the assignment is not certain (132). The precise measurement of transition moment directions in the study of crystal spectra is complicated by the

presence of crystal field (105, 136). Callis and coworkers (137) have estimated the angle between the I and II bands to be about 61 ± 10°, while it was found to be 71º by Clark (131). However, it is now clear that the first band is polarized along the short axis (C4C5), while the second band (near 4.96 eV) is long axis polarized (108, 109, 131, 132). Recently, Clark (132) performed a very extensive and elegant study to determine the transition moment directions in guanine using polarized absorp-

tion spectra of a single crystal of guanosine dihydrate. Based on his investigations

and by comparing with earlier results, he suggested that directions in guanine for

transitions near 4.46, 5.08, 6.20, and 6.57 eV would be -12, 80, 70, and -10 de-

grees, respectively. Some advanced spectroscopic studies have been performed

on guanine and substituted analogs, guanine-guanine, and guanine-cytosine base

pairs (44, 45, 138-142). These investigations included: REMPI studies of guano-

sines (139) and guanine (140); REMPI and spectral hole burning (SHB) studies of guanine, methyl guanine (44), guanine-guanine base pairs, guanine-cytosine base

pairs (138), guanine, and hydrated guanine (142); and REMPI and IR-UV depletion spectroscopic studies of guanine, and methyl guanine (45). In these studies (44,

45, 138-140, 142), the spectral origin (0-0 transition) of the S1 excited state and

some lower vibrational frequencies were determined, and the existence of different tautomers of guanine was investigated (44, 45, 142). The tautomeric distribution in guanine in low temperature was compounded by the recent experimental and

theoretical investigation of Choi and Miller (46) by trapping guanine in the helium droplets and subsequent reassignment of R2PI spectra by Mons et al. (47) which showed the existence of imino tautomeric forms. However, it should be noted that

according to this reassignment, the keto-N9H as well as keto-N7H tautomers have not yet been observed. This reassignment is also supported by other theoretical re-

sults (97, 43). Our recent detailed theoretical investigation on all guanine tautomers have predicted that the spectral origins of the keto-N9H and keto-N7H tautomers will be in between the spectral region covering the spectral origin of the keto-N7H-IMINO-cis and the enol-N9H-trans tautomers (143).

The CASSCF/CASPT2 investigation of the singlet electronic transitions of gua-

nine was performed by Roos and coworkers (126) employing the ANO-type basis set and using the MP2/6-31G(d) optimized planar geometry. The effect of the aqueous solvent on electronic transitions was considered using the self-consistent reaction field (SCRF) model. The computed CASPT2 transition energies were found to be in reasonably good agreement (with an accuracy of 0.3 eV) with the experimental data, while the CASSCF transition energies were much larger. Elec-

tronic transition energies of guanine were also computed at the TDDFT (95, 127-129, 144) and CIS (13, 14, 92) methods and in one of the TDDFT calculation basis sets with several set of diffuse functions were used (127). In the case of CIS method the scaling factor 0.72 (13, 14, 96) was used to compare obtained energies with the experimental data and the corresponding CASPT2 transition energies. Mennucci et al. (95) have studied the photophysical properties of guanine tauto-

mers (keto-N9H and keto-N7H) including the excited state tautomerization theo-

retically at the TDDFT, CIS, and multireference perturbation configuration inter-action (CIPSI) methods both in the gas phase and in water solution modeled using the continuum model. The role of protonation in the excited state proton transfer from the keto-N9H to the keto-N7H form and the occurrence of fluorescence from the latter tautomer in the water solution have also been discussed.

Table III shows the computed vertical singlet ππ* and nπ* transition energies, tran-

sition moment directions and dipole moments of the keto-N9H and keto-N7H tau-

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tomers of guanine, and their hydrated

forms (with three water molecules) ob-

tained at the CIS/6-311G(d,p)//HF/6-311G(d,p) level (13, 14) along with some experimental and CASSCF and CASPT2 results (126). It should be noted that the keto-N9H tautomer in the gas phase is found to be about 0.86 kcal/mol more stable than the keto-N7H form while un-

der hydration with three water molecules

the latter tautomer is found to be about

3.19 kcal/mol more stable than the for-mer tautomer (at the HF/6-311G(d,p) level). Data shown in Table III suggest that the scaled CIS/6-311G(d,p)//HF/6-311G(d,p) and CASPT2/CASSCF re-

sults are in agreement with respect to

the assignment of the first nπ* transition as being due to the excitation of the car-

bonyl group lone pair electron. Further,

the order in transition intensity obtained

at the CIS level agrees with the solution spectra of guanine and its derivatives in

which the first transition (near 275 nm) appears as a weak peak in comparison to

the stronger peak near the 250 nm region (11). Further, there is a good correspon-

dence between the computed transitions

(scaled) of the keto-N9H tautomer (and its hydrated form) and the CASPT2 results (solvation included), in particular when

comparison is made with the transition

of the hydrated tautomer. However, the

agreement is better in the lower than in

the higher energy region. The third ππ* transition computed at 5.95 eV of the hy-

drated keto-N9H tautomer has the lowest oscillator strength among all the ππ* tran-

sitions shown in Table III. This transition can be considered for an explanation of

the 5.5 eV band in the experimental data

(116, 117, 131). Therefore, the calcula-

tions favor this transition as a weak ππ* type. Two almost degenerate transitions near 6.66 and 6.67 eV (scaled values) of the keto-N9H tautomer in the gas phase correspond to a single transition at 6.57 eV for the hydrated form, which explains

the 6.0-6.3 eV experimental region of guanine (Table III). This result may be related to that of the MCD observation of guanosine 5’-diphosphate which shows

that the 200 nm (6.2 eV) band is com-

posed of two transitions (111).

The experimental measurement of 7-methylguanine shows that the first ab-

sorption peak is about 10 nm red-shifted

Table

III

Verti

cal s

inglet

* a

nd n

* exc

itatio

n ene

rgies

(E,

eV),

oscil

lator

stren

gths (

f), tr

ansit

ion m

omen

t dire

ction

s (, )

, and

dipo

le mo

ments

(, D

ebye

) of t

he ke

to-N9

H an

d keto

-N7

H tau

tomers

of gu

anine

in th

e iso

lated

and h

ydrat

ed fo

rms a

t the C

IS/6-3

11G(

d,p)//H

F/6-31

1G(d,

p) lev

el (13

,14).

CIS

Expe

rimen

tal D

ataa

detar dyH det alo sI

CASP

T2/C

ASSC

Fb

Abs1

Abs2

CD

Rang

e E

f c

EdE

f Ed

E1 /E2 /f/

/E3 /f/

EE/

f/E

Eke

to-N9

H

* Tran

sition

s

6.39

0.282

-42

5.9

6 4.6

0 6.4

5 0.2

45

-25

4.64

4.76/6

.08/0.

113/-

15/7.

72

4.73/0

.154/-

4 4.5

1 4.5

6/0.15

/-24

4.51

4.4-4.

6 7.2

5 0.5

16

66

7.74

5.22

7.18

0.567

70

5.1

7 5.0

9/6.99

/0.23

1/73/6

.03

5.11/0

.242/7

5 5.0

4 5.0

4/0.24

/88

4.92

4.8-5.

1 8.3

2 0.1

04

51

6.18

5.99

8.27

0.089

59

5.9

5 5.9

6/7.89

/0.02

3/7/5.

54

5.98/0

.021/6

5.5

1 5.4

-5.5

9.25e

0.113

79

5.5

2 6.6

6

6.6

7f 9.1

3 0.5

12

-89

6.57

6.65/8

.60/0.

161/-

80/10

.17

6.49/0

.287/-

85

6.33

6.19/0

.40/86

6.2

0 6.0

-6.3

9.26

0.356

81

6.1

7 6.6

7

n

* Tran

sition

s

6.97

0.001

-

4.71

5.02

7.28

0.001

-

5.24

5.79/6

.22/10

-4 /-/4.31

7.82

0.010

-

5.84

5.63

8.01

0.010

-

5.77

6.60/8

.05/0.

013/-

/4.63

8.58

0.003

-

7.24

6.18

8.89

0.002

-

6.40

6.63/7

.97/0.

002/-

/2.64

ke

to-N7

H

* Tran

sition

s

6.16

0.222

-3

1.71

4.44

6.11

0.277

11

4.4

0

7.5

2 0.2

32

64

1.60

5.41

7.44

0.095

51

5.3

6

8.0

3 0.6

14

86

1.35

5.78

7.86

0.796

89

5.6

6

n

* Tran

sition

s

7.05

0.001

-

4.66

5.08

7.53

0.001

-

5.42

8.06

0.058

-

3.07

5.80

8.18

0.004

-

5.89

a Abs1 , A

bsorp

tion o

f gua

nine i

n wate

r (10

4); A

bs2 , A

bsorp

tion o

f gua

nosin

e in w

ater a

nd

value

s are

based

on po

larize

d abs

orptio

n spe

ctra o

f crys

tallin

e gua

nosin

e (1 3

2); C

D, C

D sp

ectra

in aq

ueou

s solu

tion o

f deo

xy gu

anos

ine 5’

-phos

phate

(dGM

P) (11

6); b

E1 corre

spon

ds to

CAS

PT2 a

nd

E2 corre

spond

s to C

ASSC

F tran

sition

energ

ies in

the g

as ph

ase;

E3 /f/ co

rresp

onds

to re

sults

in w

ater (

126);

c Grou

nd st

ate di

pole

mome

nts o

f the

keto-

N9H

and k

eto-N

7H ta

utome

rs at

the H

F/6-31

1G(d,

p) lev

el are

6.77

and 1

.78 D

ebye

, res

pecti

vely;

d Scale

d (sca

ling f

actor

0.72

) exc

itatio

n ene

rgies;

e Rydb

erg co

ntami

natio

n; f Av

erage

of tra

nsitio

ns at

6.66

and 6

.67 eV

.

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relative to that of guanosine monophosphate (GMP) (145). The predicted transition energy of the first ππ* transition of the keto-N7H tautomer and its hydrated forms is lower than the corresponding transition energies of the keto-N9H tautomer and its hydrated forms (Table III). Therefore, the calculated result is in agreement with the experimental data. Computed nπ* transitions of the hydrated keto-N9H tautomer are found to be at 5.24, 5.77, and 6.40 eV (Table IV). These results support the find-

ings of Clark (132) with regard to the existence of the nπ* transitions near 5.21 and 6.32 eV in guanine. On the basis of theoretical predictions of a ππ* transition near 5.95 eV and an nπ* transition near 5.77 eV (Table III), it appears that in the 5.5 eV region of guanine, the weak ππ* and nπ* transitions are present and are responsible for the ambiguous assignment of transitions in that region.

Uracil and Thymine: The spectral features of uracil and thymine are generally similar and characterized by absorption bands near 260, 205, and 180 nm (4.77, 6.05, and 6.89 eV). It should be noted that with respect to the uracil, the first and third bands in thymine are generally slightly red- and blue-shifted, respectively

(11, 103, 104, 107, 110, 114, 146, 147). The 205 nm band is found to be mixture of two peaks near 215 and 195 nm (5.77 and 6.36 eV) in the CD spectra while the presence of a band near 240 nm (5.17 eV) was also indicated in the CD measure-

ment, which was assigned as nπ* type (11, 116). The existence of an nπ* transi-tion near 250 nm (4.96 eV) was predicted by Hug and Tinoco (148) and this transi-tion was suggested as the possible source of the 240 nm band observed in the CD spectra (11, 116). Based on the polarized absorption (11, 105, 149) and reflection experiments (11, 150) the transition moment direction for the first band is found to be close to 0º for uracil and -20º for thymine (Fig. 1). Although, Novros and Clark (151) have suggested -53º or +59º for the second absorption band, but latter was selected on the basis of agreement with the LD spectra of uracil (109). How-

ever, Anex et al. (152) have suggested it to be -31º. Eaton and Lewis (149) have estimated that polarization of the I and II bands are approximately perpendicular

to each other. Holmen et al. (153) have found 35º for the second transition in 1,3-dimethyluracil. Several investigations of uracil, thymine, and their analogs have

suggested the existence of an nπ* transition within the 260 nm envelope (11, 107, 147, 154). In the photoacoustic spectra of thymine the existence of another transi-tion within the 270 nm (4.59 eV) envelope was also suggested (107). Backer and coworkers (147, 155-157) have performed a series of experiments on the absorp-

tion and emission properties of uracil, thymine, and their derivatives in polar protic

and aprotic solvents at the low and room temperatures. It has been found that

uracil, thymine, and thymidine exhibit strong phosphorescence in polar aprotic

solvents [2-methyltetrahydrofuran (2-MTHF)], while a relatively stronger fluo-

Table IV Vertical singlet * and n * excitation energies ( E, eV), oscillator strengths (f), transition moment directions ( , ), and dipole moments ( , Debye) of the keto tautomer of uracil in the isolated and hydrated forms at the CIS/6-311G(d,p)//HF/6-311G(d,p) level (101).

CIS Experimental Dataa detardyH detalosI

CASPT2/CASSCFb Abs1 Abs2 CD Crystal Range

E f c Ed E f Ed E1/ E2/f/ / E E E E/ E* Transitions

6.83 0.446 -7 5.07 4.92 6.74 0.447 -6 4.85 5.00/6.88/0.19/-7/6.3 5.08 4.79 4.73 4.51/-9 4.6-5.1 8.89 0.123 36 3.48 6.40 8.73 0.140 46 6.29 5.82/7.03/0.08/-29/2.4 6.05 6.14 5.77 5.82/59 5.8-6.1 9.29 0.386 -66 4.99 6.69 9.12 0.439 -57 6.57 6.46/8.35/0.29/23/6.9 6.63 6.36 6.3-6.6 10.0 0.322 -14 2.43 7.20 9.93 0.251 -15 7.15 7.00/8.47/0.76/-42/3.7 6.85 7.00 6.7-7.0 n * Transitions 6.51 0.000 - 2.82 4.69 6.79 0.001 - 4.89 4.54/4.78/-/-/3.4 7.98 0.000 - 5.10 5.75 8.11 0.000 - 5.84 6.00/6.31/-/-/4.8 9.96e 0.006 - 7.06 7.17 9.97 0.009 - 7.18 6.37/7.80/-/-/8.7

aAbs1, Absorption in the gas phase (103); Abs2, Absorption in aqueous medium (114); CD, CD spectra of uridine in an aqueous medium (116); Crystal, Transition energy/transition moment direction (151); Range, Range of transitions observed in different experiments; b E1 represents CASPT2 and E2

represents CASSCF transition energies, for the f values of n * transitions see original paper (160); cGround state dipole moment at the HF/6-311G(d,p) level is 4.67 Debye; dScaled (scaling factor 0.72) excitation energies; eRydberg contamination.

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rescence was observed in a polar protic solvent (EtoH-MeOH). It has been con-

cluded that in an aprotic solvent the lowest singlet excited state of uracil, thymine,

and thymidine has a predominantly nπ* character. However, in a protic solvent or under 1,3-dimethylation, the lowest singlet excited state character is changed to ππ* (147). The relative positions of the nπ* transition is found to be solvent dependent. In the gas phase and in an aprotic solvent, the nπ* state is the lowest, while in a protic environment it lies higher than the ππ* state. Consequently, the nπ* state becomes the second state in a protic environment (11, 154, 147).

Petke et al. (158) have applied the MRCI and RPA theoretical methods using the X-ray crystallographic geometry (159), while Roos and coworkers (160) have applied the CASSCF/CASPT2 level of theory using the average experimental geometrical data from Taylor and Kennard (161) to compute electronic transition energies of uracil and thymine. The CIS method was also used in the study of the excited state geometries, phototautomerization, and solute-solvent (water) interactions of uracil

and thymine (13, 14, 25, 101). In addition, TDDFT method was used to study electronic transitions of uracil and thymine (127-129) and in our study (127) we have used up to five sets of diffuse basis functions. In the CIS investigation, the three water molecules in the first solvation shell were used to model the aqueous solution (13, 14, 101). Recently, TDDFT method using the BPE0 exchange cor-relation function was used to study the absorption and emission spectra of uracil,

thymine, and their derivatives (162, 163). In this study, the four water molecules were considered in the first solvation shell to model the effect of local hydrogen bonding interactions while the effect of bulk water was modeled at the PCM level. To explain the emission spectra, excited state geometries were optimized at the TD-BPE0 level. Tables IV and V show the computed singlet vertical ππ* and nπ* transition energies of uracil and thymine, respectively, obtained at the CIS/6-311G(d,p)//HF/6-311G(d,p) level (13, 14, 101). The first nπ* transition of uracil and thymine is localized at the C4O4 group. The second nπ* transition is localized at the C2O2 group, while the third nπ* transition is of mixed type with contribu-

tion from both the C4O4 and C2O2 groups. The assignments of these transitions are in agreement with the MRCI, RPA (158), and CASSCF/CASPT2 results (160). The nπ* transition energies are blue-shifted upon hydration. Consequently, in the gas phase, the first singlet vertical excited state of uracil and thymine has nπ* character. After hydration, the ππ* state is lowered. This result is in agreement with experimental observations of uracil and thymine that, in the gas phase or in

an aprotic solvent, the nπ* state is the lowest singlet excited state, while in a protic solvent the ππ* state is the lowest (11, 147). The computed (scaled) first nπ* transition of hydrated uracil and thymine near 4.89 eV (Tables IV, V) can be cor-

Table V Vertical singlet * and n * excitation energies ( E, eV), oscillator strengths (f), transition moment directions ( , ), and dipole moments ( ,Debye) of thymine in the isolated and hydrated forms at the CIS/6-311G(d,p)//HF/6-311G(d,p) level (13).

ataD latnemirepxE SIC a

detardyH detalosICASPT2/CASSCFb

Abs PA CD Range E f c Ed E f Ed E1/ E2/f/ / E E E E* Transitions

6.70 0.455 -10 5.06 4.82 6.61 0.450 -8 4.76 4.88/6.75/0.17/15/6.5 4.68 4.59 4.68 4.5-4.9 8.77 0.162 67 5.14 6.31 8.57 0.188 75 6.17 5.88/7.15/0.17/-19/1.5 6.08 5.90 5.77 5.8-6.1 9.16 0.436 54 3.56 6.59 9.03 0.493 48 6.50 6.10/8.33/0.15/67/7.8 6.36 6.3-6.4 10.1 0.211 -18 2.31 7.27 10.0 0.216 -10 7.20 7.13/8.62/0.85/-35/3.1 7.08 7.00 6.7-7.1 n * Transitions 6.52 0.000 - 3.22 4.69 6.79 0.000 - 4.89 4.39/5.22/-/-/3.2 8.04 0.000 - 4.67 5.79 8.19 0.000 - 5.90 5.91/6.77/-/-/4.6 9.96 0.000 - 4.66 7.17 9.94 0.004 - 7.16 6.15/8.14/-/-/8.6

aAbs, Absorption of thymine in water (110); PA, Photoacoustic spectra of thymine (107); CD, CD spectra of thymidine in water (116); Range, Range of transitions observed in different experiments; b E1 represents CASPT2 and E2 represents CASSCF transition energies, for the f values of n * transitions see original paper (160); cGround state dipole moment at the HF/6-311G(d,p) level is 4.56 Debye; dScaled (scaling factor 0.72) excitation energies.

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related with the corresponding experimental transition near 250 nm (4.96 eV) in the aqueous solution (11, 110, 115, 116) while the computed second nπ* transition near 5.8 eV can also be correlated with the nπ* transition of 1-methyluracil near 217 nm (5.71 eV) (151). The observed CD spectra in an aqueous solution of thy-

midine and uridine, and the aqueous absorption spectra of uracil and thymine, can be easily explained in terms of the computed (scaled) transitions of hydrated uracil

and thymine with an accuracy of about 0.2 eV, except for the second transition for which the error is somewhat higher. Further, the first singlet ππ* transition of thymine is red-shifted compared to the corresponding transition of uracil (Tables IV and V) (11, 103, 104, 107, 110, 114, 146, 147). The composite nature of the 205 nm (6.05 eV) band observed in the CD spectra (116) of these molecules is also revealed in the CIS computations although the splitting is small.

Cytosine: The existence of two broad peaks near 266 and 197 nm (4.66 and 6.29 eV) and weak peaks (or shoulders) near 230 and 212 nm (5.39 and 5.85 eV) have been reported in the absorption spectra of aqueous solution of cytosine (11, 104, 114, 116, 164-168). However, it should be noted that the general features of the cytosine spectrum are found be solvent dependent (11, 114). The first absorption band of cytidine in an aqueous medium is red-shifted to 271 nm (4.57 eV) com-

pared to the corresponding band of cytosine near 266 nm (104, 166). A significant red-shift in this band is also observed in the absorption spectrum of 3-methylcyto-

sine in aqueous media, which shows a peak near 289 nm (4.29 eV) (167). The 197 nm band of cytosine is found to be composite corresponding to the 202 nm (6.14 eV) and 189 nm (6.56 eV) transitions observed in the CD spectra (116, 169, 170). The CD spectra of different cytosine derivatives reveal that, even though the first CD transition agrees well with the corresponding transition in the absorption spec-

tra, the second and third CD bands are significantly red-shifted (116, 169). Clark’s group has performed extensive studies of transition moment directions of cytosine

(165). By performing the polarized reflection spectroscopy of single crystals of cytosine monohydrate, the first three transition moment directions (I = 6º, II = -46º, III = 76º) were assigned explicitly while two values (-27º or 86º) were suggested for the forth transition of cytosine. It should be noted that the value of transition

moment direction for the first transition was suggested to be 6º by Clark’s group (165), 9º by Callis and Simpson (171), and 10º by Lewis and Eaton (172). Clark’s group (165) has suggested the rotation of orientation axis in the earlier LD mea-

surements of cytosine and related compounds in the stretched film (109, 173) in or-der to obtain coherency of results with those obtained in the crystal environments.

The conclusion regarding the transition moment directions for the second and third transitions was based on the study of polarized fluorescence of 5-methylcytosine (150), which resulted in the angle between the transition moments of I and II bands

as 40±15º. Similar results were also found for cytosine monophosphate (174). Further, the stretched film work (108, 109, 173) indicated that the angle between the transition moments of I and III bands is larger than that between I and II bands.

With regard to the nπ* transitions, the experimental (110, 165, 166, 175) and theo-

retical (13, 14, 25, 100, 176) evidences suggest the existence of such a transition in the 5.3 eV (232 nm) region in cytosine. Zaloudek et al. (165) have suggested the

existence of another nπ* transition near 5.6 eV (220 nm).

Electronic transitions of cytosine were studied at the MRCI and RPA levels (158) using the x-ray crystallographic geometry (57), CASSCF/CASPT2 methods using the average experimental geometry (176), TDDFT (127-129), and CIS method (13, 14, 25, 100). In the CIS study (13, 14, 100), three water molecules were considered in the first solvation shell to model aqueous solution. The computed transition ener-gies (scaled, scaling factor 0.72) of cytosine and its hydrated form obtained at the CIS/6-311G(d,p)//HF/6-311G(d,p) level are shown in the Table VI. The computed transition energies (scaled) of the hydrated cytosine are in good agreement (within

an accuracy of 0.2 eV) with the experimental data of cytosine in water, except for the second transition. However, the error becomes smaller if a comparison is made of

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the transitions of the cytosine sublimed film (168). Since the general features of the cytosine spectrum are found to be solvent dependent, differences between the

computed and experimental data is not unexpected. It appears that the absorption

peak of cytosine in water (165, 167) near 212 nm (5.85 eV) is shifted to 6.07 eV in the sublimed film experiment (168). Further, the computed nπ* transitions of the hydrated cytosine near 5.37 and 5.71 eV (Table VI) are also in good agree-

ment with the observed nπ* transition near 5.3 and 5.6 eV (100, 165, 166, 175).

Excited State Geometries of Nucleic Acid Bases

For a comparison of similar computational techniques for the ground and ex-

cited states, the ground state geometries were optimized at the HF/6-311G(d,p) level while the excited state geometries were optimized at the CIS/6-311G(d,p) level for all bases discussed in this section. The nature of corresponding poten-

tial energies surfaces were determined from the harmonic vibrational frequen-

cies calculation and all considered tautomers were found to be minima (13, 14, 100, 101). The ground state geometries of the N9H and N7H tautomers of ad-

enine are generally planar except the amino group, which is pyramidal, and such

nonplanarity is more pronounced for the N7H tautomer. In the S1(ππ*) excited

state the N9H tautomer is almost planar while the N7H tautomer has nonplanar structure; the amino group is pyramidal for both tautomers (13). A nonplanar structure around the N1C2N3 fragment of the N9H tautomer is revealed in the S

1(nπ*) excited state. In the S

1(nπ*) excited state, the N7H tautomer has a struc-

ture reminiscent to twisted intramolecular charge transfer states (96, 177, 178). In this state, the N7H tautomer has C

s symmetry; the amino hydrogens are at

the dihedral angles of ±61º with respect to the ring plane. It should be noted that no significant intramolecular charge transfer was found (13). In the case of hydrated tautomer, where three water molecules were considered in the first sol-vation shell, water molecules were found to induce planarity in the system and

consequently the ground and lowest singlet ππ* excited state geometries were found to be almost planar including the amino group.

The S1(ππ*) excited state geometry of the keto-N9H tautomer of guanine is re-

vealed to be strongly nonplanar around the C6N1C2N3 fragment (13). In the S

1(nπ*) excited state, where excitation is localized at the carbonyl group, it was

found that the C6O6 bond length is increased by about 0.1 Å compared to the ground state value and the O6 and H1 atoms are displaced away from the ring plane lying the opposite side to each other. For the keto-N7H tautomer, geo-

metrical changes in the excited states are similar but usually smaller than those

in the keto-N9H tautomer. It was revealed that hydration generally induces pla-

narity in the system. Therefore, geometrical nonplanarities in the excited states of hydrated tautomers were found comparatively smaller than those in the iso-

lated forms. A similar trend of change in the geometrical parameters of guanine

tautomers was found in another study, where the geometries of the molecules

were also optimized in the ground and excited states in an aqueous medium us-

ing the IEF-PCM model (95). It should be noted that significant change in the geometrical parameters was revealed in the aqueous solution as compared to the gas phase (95). The restricted open-shell Kohn-Sham level of calculation (179) on the first singlet ππ* excited state of guanine tautomers also shows structural deformation similar to that obtained using the CIS method.

Although the ground state geometries of uracil and thymine are planar, the cor-

responding electronic lowest singlet nπ* excited state geometries are slightly nonplanar and characterized by the significant out of plane displacement and elongation of the C6O6 bond by about 0.1 Å compared to that in the ground state (13, 101). Such elongation is consistent with the fact that the state is character-ized by the excitation of lone pair electron belonging to the C4O4 group. In the lowest singlet ππ* excited state a boat type of geometry, where N1, C2, C4, and

Table

VI

Verti

cal s

inglet

* a

nd n

* exc

itatio

n ene

rgies

(E,

eV), o

scilla

tor st

rength

s (f),

trans

ition m

omen

t dire

ction

s (,)

, and

dipo

le mo

ments

(, D

ebye

) of th

e keto

-N1H

tau

tomers

of cy

tosine

in th

e iso

lated

and h

ydrat

ed fo

rms a

t the C

IS/6-3

11G(

d,p)//H

F/6-31

1G(d,

p) lev

el (10

0).

CIS

Expe

rimen

tal D

ataa

de tar dyH d etalosI

CASP

T2/C

ASSC

FbAb

s1 Ab

s2 Ab

s3 Ab

s4

E f

cEd

E f

EdE1 /

E2 /f//

E/f

E/f/

EE/

f * T

ransit

ions

6.32

0.171

24

5.6

0 4.5

5 6.4

6 0.2

21

15

4.65

4.39/5

.18/0.

061/6

0.6/4.

7 4.6

4/0.09

6 4.6

6/0.14

/6 4.5

7 4.5

4/0.05

8 7.8

4 0.3

82

-20

6.73

5.64

7.75

0.365

-19

5.5

8 5.3

6/6.31

/0.10

8/-1.5

/7.0

5.21/0

.100

5.39/0

.03/-4

6 5.3

4 5.4

0/0.07

3 8.4

2 0.6

86

-48

7.06

6.06

8.41

0.649

-49

6.0

6 6.1

6/7.30

/0.86

3/-39

.7/6.2

5.8

3/0.21

1 5.8

5/0.13

/76

5.77

6.07/0

.115

9.49

0.167

17

6.7

4 6.8

3 9.2

3 0.2

93

19

6.65

6.74/7

.82/0.

147/1

4.9/9.

3 6.4

6/0.63

9 6.2

9/0.36

/X

6.26

6.67/0

.072

n* T

ransit

ions

6.97

0.003

-

4.28

5.02

7.46

0.007

-

5.37

5.00/5

.13/0.

005/-

/4.7

7.50

0.001

-

3.73

5.40

7.93

0.000

-

5.71

6.53/7

.14/0.

001/-

/6.4

a Abs1 , A

bsorp

tion o

f cyto

sine i

n wate

r (16

7); A

bs2 , A

bsorp

tion o

f cyto

sine i

n wate

r; va

lues a

re ba

sed on

polar

ized s

pectr

a of c

ytosin

e crys

tal an

d X= -

27 or

86 (1

65);

Abs3 , A

bsorp

tion o

f cyti

dine i

n wate

r (16

6); A

bs4 , A

bsorp

tion o

f sub

limed

cytos

ine (1

68); b

E1 repre

sents

CASP

T2 an

d E2 re

presen

ts CA

SSCF

trans

ition e

nergi

es (17

6); c Gr

ound

state

dipo

le mo

ment

at the

HF/6

-311G

(d,p)

level

is 6.9

8 Deb

ye; d Sc

aled (

scalin

g fac

tor 0.

72) e

xcita

tion e

nergi

es.

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C5 atoms are in approximate plane and N3 and C6 atoms are out of the same plane, is revealed for thymine. For hydrated species, the structural deformations in the

excited state are generally similar to those in isolated species. Detailed discussion

about hydrated species can be found in our earlier papers (13, 101). It should be noted that in jet-cooled studies of these compounds (29, 30), the observed spectral diffuseness were explained due to the possible excited state geometrical distortion.

The ground state geometry of cytosine is planar however, the S1(ππ*) excited state

geometry is nonplanar; the predicted nonplanarity concerns mainly the N1C6C5C4 fragment. The amino group is pyramidal in both states. In the lowest singlet nπ* excited state [S

1(nπ*)], the amino group is considerably rotated and the N3 atom

lies appreciably out-of-plane. Such deformation was explained as being a result of

the excitation of the N3 lone pair. The rotation of the amino group was speculated to be an effect of the partial mixing in excitation due to the amino lone pair electron.

Since the N3 site of cytosine provides a repulsive potential for hydrogen bonding in the S

1(nπ*) excited state, the mode of hydration of cytosine, where three water mol-

ecules were considered in the hydration, is found to be completely modified. The detailed discussion of hydration of different tautomers of cytosine in the ground and

excited states can be found in our recent publications (13, 100).

Excited State Proton Transfer and Hydration of Guanine in the Excited State

The excited state barrier height corresponding to the proton transfer from the N9H site to the N3 site of adenine has been computed at the MCQDPT2/MCSCF level (4) and the corresponding results were compared with the ground state barrier ob-

tained at the same level. Though, the computed barrier in the gas phase was found to be significantly large, the barrier was reduced from 63.0 kcal/mol in the ground state to 43.0 kcal/mol in the excited state. It is expected that the presence of a water molecule in the proton transfer reaction path may reduce the barrier significantly, since in the similar type of reaction in the 7-azaindole the barrier was found to be significantly reduced in the presence of a water molecule (3). The keto-enol tautomerization of guanine in the singlet ππ* excited state was also investigated recently at the TDDFT/CIS level both in the gas phase and in water solution in-

cluding that of hydrated forms in which a water molecule was placed in the pro-

ton transfer reaction path (5). The ground state geometries were optimized at the B3LYP/6-311++G(d,p) level while vertical transitions were computed at the TD-B3LYP/6-311++G(d,p) level using the excited state optimized geometries at the CIS/6-311G(d,p) level. Generally, the excited state barrier heights were revealed slightly larger than the corresponding ground state values. It was concluded that

electronic excitation may not facilitate the excited state keto-enol proton transfer in

the gas phase and in water solution. The geometries of transition states in the ex-

cited states were found significantly nonplanar. Further, transition state structures for hydrated guanine were found to be zwitterionic form in which water molecule

is in the form of hydronium cation (H3O+) and guanine is in the anionic form, ex-

cept for the N9H form in the excited state where water molecule is in the hydroxyl anionic form (OH-) and the guanine is in the cationic form.

Recently hydration of guanine, by considering 1, 3, 5, 6, and 7 water molecules in the first solvation shell, in the electronic lowest singlet ππ* excited state was studied at the CIS/6-311G(d,p) level and the computed excited state structures were compared with the corresponding ground state geometries obtained at the HF/6-

311G(d,p) level (28). It was found that in the ground state the first solvation shell of guanine can accommodate up to six water molecules and water molecules interact-

ing directly with amino group induce planarity in the latter. The hydrogen bond dis-

tances were generally changed in the excited state compared to the corresponding

ground state. Significant change was revealed regarding the excited state structure of guanine, which was found strongly nonplanar in the pyrimidine part of the ring.

But, the mode of the structural distortion was found to be dependent on the number

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of water molecules in the solvation shell of guanine and, thus, indicating the degree

of hydration dependent excited state dynamics of guanine. The excited state geom-

etry of guanine was revealed similar for isolated, mono, and trihydrated guanine but

exhibited significantly different structural distortion for the penta and hexahydrated guanine. The changes in different stretching vibrational frequencies of guanine in the isolated and hydrated complexes were also found to be in accordance with the

change in the hydrogen bond distances in going from the ground state to the excited

state and with increase in the number of water molecules in the solvation shell.

Excited States of Base Pairs

The theoretical evaluation of electronic singlet excited state properties of the AU, AT, and GC base pairs were performed by us as well as other groups (17, 20, 78, 79, 128, 129, 180, 181). The ground state geometries of Watson-Crick (WC) AU, AT, and GC were optimized at the HF level, while the excited state geometries were optimized at the CIS level using the 6-31++G(d,p) basis set and under the constraint of planarity (78, 79). The electronic excitations were generally characterized by the excitation of one or the other monomeric unit. This result is in agreement with the experimental observation of the AT and GC polymers and natural DNA bases where the electronic transitions were assigned to the corresponding monomer bases (182).

Some charge transfer type states, characterized by the excitation from the occupied

orbitals of one base to the virtual orbitals of the complementary base of the base pair,

were also identified lying slightly higher in energy (78, 79). Generally, base pairing does not have a significant effect on the singlet ππ* transitions of the constituent bases, but significant blue-shift has been revealed for the nπ* transitions. It is well known, experimentally, that hydrogen bonding produce blue-shift for nπ* transi-tions compared to the nonhydrogen bonding environments (183, 184). Further, the change in the excited state geometry is restricted to the base where the excitation

energy is localized. The basis set superposition error (BSSE) corrected interac-

tion energies of the base pair formations in the ground state were computed using

the Boys-Bernardi counterpoise correction scheme (185) and the same scheme was utilized to compute BSSE corrected interaction energy in electronic singlet excited

states; the details of which can be found in our work given in Refs. (78) and (79).

The hydrogen bond parameters and interaction energies of base pairs in the ground and electronic singlet excited states suggested that these properties for the AT and AU base pairs are similar. The hydrogen bonds deviate more from linearity in the singlet nπ* states than those in the ground and singlet ππ* states. It follows from the results of calculations that the base pairs are appreciably destabilized due to

nπ* excitations. Noguera et al. (20) have also found the decrease in the base pair-ing energy of the WC GC base pair in the triplet ππ* excited state, the excitation being localized at the guanine moiety, at the B3LYP level. However, the WC AT base pair was found be unaffected under such excitation. The excited state geom-

etries of guanine-guanine base pair in the lowest singlet ππ* excited state were also studied by considering the two configurations of base pairs (GG16 and GG17) at the CIS/6-311G(d,p) level and obtained results were compared with those of geo-

metrical change of guanine and GC base pairs in the excited state (27). It was found that base pairings have significant effect on the excited state geometry of guanine and, therefore, excited state dynamics of guanine may be significantly modified in different hydrogen bonding environments.

Nonradiative Decays in Nucleic Acid Bases and Base Pairs

Although different mechanisms have been suggested for ultrafast nonradiative re-

laxation processes in nucleic acid bases, but universal mechanism is not yet known.

A detailed lucid analysis about nonradiative decays in nucleic acid bases has been

provided by Kohler and coworkers in a recent review article (12) and, therefore,

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we will mainly focus on investigations not covered there. The nonradiative deac-

tivation mechanisms include the out-of-plane vibrational mode coupling of close

lying electronic ππ* and nπ* states due to the nonplanar geometries of the excited states (15, 16, 96). For the large vibrational coupling, the Franck-Condon factor associated with a radiationless transition is large, which will lead to a rapid conver-

sion to the ground state potential energy hypersurface. Recently, another possible mechanism has also been suggested in which the lower lying πσ* Rydberg state in nucleic acid base adenine causes predissociation of the lowest singlet ππ* excited electronic state to the ground state potential energy surface (186-190). This conical intersection takes place along the stretching of the N9H bond. Recently, Ebata et

al. (191) on the basis of jet-cooled spectroscopic studies of aniline have suggested the existence of the πσ* Rydberg state near the S

1(ππ*) state. On the other hand,

experimental study by Kang et al. (192) on adenine does not support the idea of a singlet πσ* state being responsible for the nonradiative process in the molecule; rather it supports that the nπ* state facilitates the internal conversion through the conical intersection to the ground state. This conclusion was based on the fact that methyl and deuterium substitution in adenine do not change the decay time in com-

parison with adenine. In this process, the excited ππ* state is coupled vibronically to the lower lying nπ* excited state. The observation of subpicosecond life-time for adenosine and different methyladenine also do not favor the idea of singlet

πσ* state being responsible for the nonradiative process in adenine (20, 193-195). Pancur et al. (196) have used the femtosecond time-resolved fluorescence up-con-

version spectroscopic technique to measure the electronic excited state lifetimes of the N9H and N7H forms of adenine and that of adenosine in aqueous solution at the room temperature. The temporal fluorescence decay profiles for adenine were found biexponential, while that for the adenosine was revealed to be mono-

exponential. The lifetime measurements were performed over a wide range of excitation wavelength from 245-280 nm. The excited state lifetime of adenine was found to be excitation energy dependent and increase (from 0.3 to 0.7 ps) with the excitation wavelength. This result is found to be in contrast to that of the isolated molecule in the gas phase, where excited state lifetime was found to decrease from

~9 ps to ~1 ps, when excitation energy was increased only about 1500 cm-1 from the

spectral origin (123, 192, 197). The excited state lifetime for adenosine was found to be independent of the excitation wavelength that was varied between 245-280 nm. The lifetime of the N7H tautomer of adenine was revealed significantly large (8.4±0.8 ps) and independent of the excitation wavelength. On the basis of the observed result that the lifetime of the excited state corresponding to the N9H tau-

tomer of adenine was decreased when molecule was excited at lower than 265 nm wavelength, the presence of a πσ* state was speculated and this state was suggested to be situated at energy above the 265 nm. The singlet πσ* state was suggested to be responsible for the decrease in the excited state lifetime at energy above the

265 nm. However, at the wavelength above 265 nm, the conical intersection of the ππ* and ground state is suggested for the ultrafast nonradiative decay. On the basis of the large excited state lifetime of the N7H tautomer, where the presence of nπ* transition is affected due to the substitution of H atom at the N7 site, the possibility of contribution of nπ* state is also suggested. Hunig et al. (198) have also indi-cated the presence of the dissociative πσ* state in adenine at higher energy level by studying the dissociation of the NH bond in adenine and the hydrogen transfer

reaction in adenine dimer in the supersonic jet cooled molecular beam, where the

NH dissociation was obtained with electronic excitation at 243 nm (5.1 eV). The hydrogen transfer in the adenine dimer was also found to takes place under the

electronic excitation. The existence of the πσ* state in decay of adenine was also supported recently by Samoylova et al. (199). The first femtosecond time-resolved photoelectron spectroscopic study of adenine, cytosine, thymine, and uracil in the

molecular beam was performed by Stolow and coworkers (200). They have used 250, 267, and 277 nm wavelengths to excite the molecules. However, these au-

thors have made detailed discussion only for adenine. The main decay pathway in adenine was attributed to the vibronic coupling in between the ππ* and nπ* states.

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In the photoelectron spectra of adenine at the 267 nm, two major bands of different life-times (<50 and 750 fs) were assigned to the ππ* and nπ* states. It was found that close to the band origin (277 nm) the life-time is several pecosecond. At higher vibronic levels, i.e., 250 and 267 nm excitations, rapid internal conversion (< 50 fs) populates the lower lying nπ* state which has a lifetime of 750 fs. At the 267 nm, these authors have found the indication of the presence of another channel

speculated to be πσ* type. Based on the time and frequency resolved detection of H-atoms in adenine and 9-methyladenine, Zierhut et al. (201) have shown that N9H bond dissociation is an important excited state deactivation pathway in adenine at

the excited state wavelength of 266 and 239.5 nm and the observed results sup-

ported the Sobolewski and Domcke model of deactivation of adenine (186-190)

On the basis of the mass-selected femtosecond time resolved pump-probe resonant ionization study on the excited state dynamics of DNA and RNA bases, Canuel et

al. (202) have suggested the importance of nonplanarity of pyrimidine ring and out-of-plane vibrations of amino group in providing the nonradiative decay path-

way in adenine and other nucleic acid bases. These two nuclear motions namely, pyrimidine ring nonplanarity and amino group out-of-plane vibration, play an im-

portant role in facilitating the vibronic coupling between the initially excited ππ* state and the dark nπ* state. The predominant role of the amino group inversion mode in the early dynamics was based on the comparison of the ultrafast compo-

nents of adenine and 9-methyladenine (~100 fs) with dimethylaminoadenine (200 fs). These authors have suggested that this may be a common mechanism for the bases; the vibronic coupling provides the earlier phase of internal conversion path-

way that on the other hand would proceed through conical intersection between the

nπ* state and high vibrational levels of the ground state. Based on the observed similarity in the picosecond decays of adenine and 9-methyladenine, these authors have not supported the role of the πσ* state in the nonradiative decay. The exis-

tence of two-step decay mechanism following a 267 nm excitation of the nucleo-

bases was revealed. Kim et al. (203) have obtained dispersed fluorescence spectra of jet-cooled adenine by exciting the vibronic bands in the fluorescence excitation spectrum. Sufficiently well resolved vibrational bands of the ground electronic state was revealed in the dispersed fluorescence spectra. The existence of strong vibronic coupling between the nπ* and ππ* excited states of adenine is supported. Domcke and coworkers (204, 205) have studied three possible deactivation mecha-

nisms corresponding to the out-of-plane deformation of the six-membered ring,

hydrogen abstraction from the amino and azine groups, opening of the five-mem-

bered in N9H-form of adenine at the CASSCF/CASPT2 level. It was suggested that the out-of-plane deformation of the six-membered ring is the likely mechanism

operating at the lower excitation energies. However, the hydrogen abstraction and

the opening of the five-membered ring may operate at the higher excitation ener-gies for the ultrafast deactivation. Serrano-Andres et al. (21) at the CASPT2 level of theory have shown that the main deactivation route in adenine is through the

conical intersection between the singlet ππ* main (intense) state and the ground state. However, such intersection in 2-aminopurine requires energy to overcome the potential energy barrier and, therefore, blocks the possible nonradiative deacti-

vation in this molecule (22). Blancafort (19) has also shown at the CASPT2 level that the nonradiative decay in adenine proceeds through the conical interaction of

the excited state to the ground state and this process is almost barrierless.

Langer et al. (206) have provided evidence for the singlet πσ* excited state driven hydrogen abstraction mechanism and its role in aqueous photoionization by per-forming an excited state nonadiabatic Car-Parinello dynamic simulation on guanine. Langer and Doltsinis (207) have also studied the nonradiative decay of methylated guanine upon excitation to the first singlet excited state using an “on the fly” sur-face hopping approach based on density functional theory. If was found that the

9-methylguanine undergo large geometrical change in the S1 state giving rise to an

increased nonadiabatic transition probability and, thus, shorter lifetime compared

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to the 7-methylguanine. The global minimum structure of 9-methylguanine shows strong out-of-plane bending in amino group, but the structure of 7-methylguanine is only slightly distorted. Further, for the keto-9H tautomer, the methylation at the N9 site was found to have significant effect on the geometry in the S

1 excited state

while for the keto-N7H tautomer, methylation at the N7 site does not cause signifi-

cant change. Therefore, it was suggested that methylation at the N9 site of guanine induces significant S

1 structural changes leading to a much reduced optical activity

in the Franck-Condon region. This finding is explained as a possible explanation for the absence of a 9-methylguanine (keto form) signal in the R2PI experiment (45).

Ismail et al. (208) have used CASSCF/6-31G(d) level of theory to study the non-

radiative decay in cytosine. They proposed that a state switch from the singlet ππ* to the singlet nπ* state and the conical intersection in between the singlet nπ* and the ground state is responsible for the ultrafast decay in cytosine. On the other hand Merchan and Serrano-Andres (209) on the basis of the CASPT2/6-31G(d,p)/CASSCF/6-31G(d) calculations proposed that the conical intersection in between the ground state and the singlet ππ* excited state is responsible for the decay in cytosine. However, Blancafort and Robb (210) again reexamined their work at the CASPT2/6-31G(d) level and suggested the involvement of three states namely ground, singlet ππ* and singlet nπ* (excitation on the CO group) states in the coni-cal intersection for the ultrafast decay in cytosine. Robb and coworkers (211) have also studied the photophysical properties of 5-fluorocytosine (5FC) and compared with that of cytosine using femtosecond transient absorption measurements and

CASSCF and CASPT2 theoretical methods. The fluorescence quantum yield of the 5FC was found to be about 60 times larger than that of the cytosine (for cytosine it is 8 × 10-5). They have found that 5FC has about 100 time larger excited state life-time than cytosine (720 fs for cytosine and 73±4 for 5FC). The transient absorption signal of 5FC was found to be independent of the polarity of solvent. This suggests that the solvent coordination in the decay is not significant.

He et al. (212) have performed an REMPI investigation of methyluracil in the gas phase and have suggested the existence of a dark state with a large life-time in the

decay path of the molecule. They suggested that this dark state may be of the sin-

glet nπ* type. Matsika (213) has studied the mechanism of radiationless decay in uracil using the ab initio multireference configuration interaction methods. Based on the theoretical calculations, it has been suggested that upon electronic excita-

tion of uracil in the gas phase, the S2(ππ*) state will decay to S1(nO4π*) state via a

conical interaction. This conical interaction will take place at about 0.9 eV below to the vertical S2 state. The dark state [S

1(nO4π*)] will decay to the ground state

via conical interaction, which will take place at about 1.8 eV below the vertical S2

state. However, it should be noted that this mechanism is for the gas phase and

proposed mechanism is expected to modify in the water solution, since a blue shift

is expected for the dark S1 state and generally red-shift is expected for the optically

active ππ* excited state. In the case of the S2 and S1 conical intersection, the geom-

etry changes involve mainly the stretching of the C5C6 bond and the contraction of the C4C5 bond. On the other hand, conical intersection of the S

1 and S

0 involves

the rotation of the C5H5 bond, which is almost perpendicular to the initial (ground state) geometry position. These conical intersections provide pathways for the ul-trafast deactivation to the ground state. It has been speculated that after the initial

S2-S1 decay, the system will be trapped in the dark S

1 state and competition between

different routes will determine the efficiency and overall rate for radiationless decay to the ground state. Perun et al. (18) have also shown that the conical intersection between the lowest singlet ππ* and the ground state which proceeds barrierless is the main route for the ultrafast nonradiative decay in thymine. Zgierski et al. (23, 214) have shown the importance of excited state structural nonplanarity in pyrimi-dine bases in facilitating the ultrafast nonradiative decay where deformed geometry

has biradical character and the excited energy is decayed through the intersection

of biradical state with the ground state explaining the different nonradiative decay

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rates of natural pyrimidine bases and those of 5-fluorinated and 6-fluorinated bases. Merchan et al. (215) have also suggested that in pyrimidines the ethane like excited state geometrical distortion in the singlet ππ* excited state facilitates the ultrafast nonradiative decay through the conical intersection with the ground state. How-

ever, the presence of a planar minimum on the singlet ππ* excited state potential energy surface was proposed to be responsible for the observed longer lifetime

decays and low emission quantum yields in these bases.

Woutersen and Cristalli (216) have studied the dynamics of vibrational relaxation in the AU base pair at the femtosecond time scale. They have found that the vi-brational relaxation of the AU base pair is much faster than that of the uracil and

occurs in the time scale of only few hundred femtoseconds. In the both AU and

uracil systems, the vibrational relaxation does not occur in a single step, but involves

an intermediate state. In the vibrational relaxation of monomeric and base-paired

uracil, different intermediate states are involved; in the base pair, part of the energy

of the NH-stretching mode is transferred to the hydrogen bond between adenine

and uracil. The hydrogen bonding between complementary nucleobases causes a strong enhancement of vibrational relaxation processes in these bases. Schultz et al.

(217) have studied the excited state deactivation mechanism in the aromatic hydro-

gen bonded 2-aminopyridine dimer mimicking WC base pairs. Femtosecond time-resolved mass spectroscopy of 2-aminopyridine clusters revealed an excited state lifetime of 65±10 picosecond for the near planar hydrogen bonded dimer, which is

significantly shorter than the lifetime of either the monomer or the 3- and 4-mem-

bered nonplanar clusters. Ab initio calculations of reaction pathways and potential

energy profiles suggested that the conical intersections connect the locally excited singlet ππ* state (due to the excitation of monomer of the dimer) and the electronic ground state with a singlet ππ* charge transfer state that is strongly stabilized by the transfer of a proton. Sobolewski and Domcke (218) have studied the ultrafast decay reaction in the guanine-cytosine (GC) base pair at the CIS and CASPT2 levels. It was suggested that the barrierless proton transfer from the guanine to cytosine in

the singlet ππ* (third in the vertical transition at the CASPT2 level) guanine to cytosine charge transfer state and the out-of-plane deformation of cytosine in the

form of the twisting of the C5C6 bond may trigger the ultrafast radiationless decay by facilitating a conical intersection in between the lowest singlet ππ* excited state and the ground state. Theoretical results of Sobolewski et al. (181) on GC base pairs support that the photochemistry of hydrogen bonds have significant influence on the photostability of DNA. It was concluded that the WC GC pairing facilitate more ef-ficient nonradiative decay for singlet ππ* excitation than other hydrogen bonded GC base pairs. Recent investigations on single and double stranded AT oligonucleotides show that excited state dynamics of nucleic acids are extremely complicated and

base stacking has main role in decay of excited singlet electronic states (219-221).

Therefore, it is very difficult to arrive at a definite conclusion regarding a univer-sal mechanism for the deactivation process in nucleic acid bases and related com-

pounds, but it is evident that excited state structural distortions may play a role

in assisting the nonradiative decays. Theoretical calculations have generally been performed for the gas phase and with medium quality of basis sets. In polar sol-vents, reordering of excited states are expected and therefore gas phase results may

modify. More extensive research that combines both theoretical and experimental investigations is needed to draw any conclusion for such universal mechanism. It

appears that there are different avenues with various possibilities for the nonradia-

tive decays and such properties may also be dependent on the environment.

Concluding Remarks

A comprehensive review has been presented for the electronic transitions, excited

state structures and interactions, nonradiative deactivation of nucleic acid bases, and

base assemblies. The excited state dynamics of isolated bases are highly complex

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and this complexity is increased multifold in nucleic acid environment where stack-

ing plays prominent role in deciding the faith of excitation energy (219-221). For example, the fluorescence quantum yield of 2-aminopurine, a fluorescent analog of adenine, is significantly attenuated in the nucleic acid environment. The electronic excited state geometries of bases and base pairs are generally nonplanar and this

nonplanarity usually facilitates the nonradiative deactivation in isolated bases and

hydrogen bonded base pairs. Further, theoretical tools in studying excited state

structures and dynamics are not yet as advanced as experimental techniques where researcher can study dynamics at the femtosecond level. However, theory and ex-

periment are complementary to each other. We believe that with the advancement in the computational algorithms and hardware, it would be possible to study rigor-

ously the excited state structures and dynamics of large system containing both the

hydrogen bonding and stacking using highly electron correlated methods and well

suited basis sets for excited states. Nevertheless, our continuous inquisitiveness for better understanding of these genetic molecules is similar to the fabrication of bricks

by which we would be able to construct a solid wall of knowledge of evolution.

Acknowledgement

Authors are also thankful to financial supports from NSF-CREST grant No. HRD-0318519, ONR grant No. N00034-03-1-0116 and NSF-EPSCoR grant No. 02-01-0067-08/MSU. Authors are also thankful to the Mississippi Center for Supercom-

puting Research (MCSR) for the generous computational facility.

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Date Received: March 21, 2007

Communicated by the Editor Jiri Sponer

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Electronic Spectra, Excited State Structures and

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M. K. Shukla a & Jerzy Leszczynski a

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