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Hydration of guanine: Electronic singlet excited states for complexes with 19 and 27 water molecules
Chemical Physics Letters 478 (2009) 254–259
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Hydration of guanine: Electronic singlet excited states for complexes with 19 and 27 water molecules M.K. Shukla, Jerzy Leszczynski * NSF CREST Interdisplinary Nanotoxicity Center, Department of Chemistry and Biochemistry, Jackson State University, Jackson, MS 39217, USA
a r t i c l e
i n f o
Article history: Received 14 May 2009 In final form 26 July 2009 Available online 29 July 2009
a b s t r a c t Computational investigation on the ground and electronic lowest singlet pp* excited state (S1(pp*)) of guanine hydrated by a large number (19 and 27) water molecules are reported and obtained results are compared with those for isolated guanine and the comparatively smaller hydrated complexes. Ground state geometries were optimized at the HF level and Configuration Interaction-Singles (CIS) method was used for excited state geometry optimization utilizing the 6-311G(d,p) basis set. It was found that excited state geometry of guanine is significantly different with each other in the studied complexes. The possible effect of hydration on the excited state dynamics of guanine is also discussed. Ó 2009 Elsevier B.V. All rights reserved.
1. Introduction Water is an essential part of everybody’s life. Therefore, it is not unexpected that in the quest for search of life on other planets and solar systems, experts look for the water signature. Deoxyribonucleic acid (DNA), another vital life’s component, is the genetic carrier where information is stored in the form of specific patterns of hydrogen bonds formed between complementary purine and pyrimidine bases. Structures and functions of nucleic acids significantly depend upon the hydration [1,2]. In fact, DNA in vivo is significantly hydrated; the degree of hydration depends upon the relative humidity, types of DNA, major and minor grooves and the type of bases [3]. Nuclear Magnetic Resonance (NMR) results have suggested that the relative humidity and temperature control the movement of backbone as well as bases in nucleic acids [4,5]. Relative stability of some minor nucleic acid tautomers have been found to be increased due to hydration [6–8]. Theoretical calculations have suggested that polyhydration can cause ground state geometrical distortion among nucleic acid bases [9–11]. Guanine is one of the important building blocks of nucleic acids. It exhibits the largest number of minor tautomers among all nucleic acid bases [6,12,13]. It is the site for the most efficient oxidative damage, has lowest ionization potential, electron affinity and largest amino group pyramidalization among bases [13]. Although, the ground state geometry of guanine is planar, except the amino group which is pyramidal, the electronic singlet excited state geometry has been predicted to be strongly nonplanar [13]. Significant geometrical distortion in the excited state of guanine has been suggested to be responsible for the efficient nonradiative decays via the conical intersection between the ground and excited * Corresponding author. E-mail address: [email protected] (J. Leszczynski). 0009-2614/$ - see front matter Ó 2009 Elsevier B.V. All rights reserved. doi:10.1016/j.cplett.2009.07.081
state potential energy surfaces [13]. We performed detailed theoretical investigation on ground and excited state structures of hydrated guanine by considering 1, 3, 5–13 water molecules around guanine [14,15]. Hydration dependent electronic singlet pp* excited state structural distortion of guanine was revealed in these studies. The main objective of the current work is to understand the structures and properties of guanine under significantly large and diverse hydration condition by considering 19 and 27 water molecules in the solvation shells. In the first complex all 19 water molecules are on the one side while in the second complex significant number of water molecules are also at the other side of guanine. This creates diverse water environments that might result in distinctive properties of the studied clusters. The current investigation provides information about the influence of large hydration on excited state geometry of guanine and that of the electronic singlet excited state dynamics. 2. Computational details Ground state geometries of hydrated guanine were optimized at the Hartree–Fock (HF) level, while the geometries in the electronic lowest singlet pp* excited state were optimized at the Configuration Interaction-Singles (CIS) level [16]. The harmonic vibrational frequencies were computed for ground state optimized geometries to ascertain the nature of potential energy surfaces (PESs). The absence of imaginary vibrational frequency suggested all computed geometries to be at least local minima at the respective PESs. The inclusion of such a large number of water molecules will generate structures of numerous hydration configuration of guanine–water complex. It will be impossible to investigate all of them at the ab initio or DFT level of theories. Therefore, search for the global minimum structure for each of the complex was not performed.
M.K. Shukla, J. Leszczynski / Chemical Physics Letters 478 (2009) 254–259
The 6-311G(d,p) basis set was used throughout the computation. Calculations were performed using the GAUSSIAN 03 program [17]. Molecular orbitals were visualized using the MOLEKEL program [18]. Although, the CIS method is an HF analog for excited state which does not account for the electron correlation [16], but it offers reasonable compromise between the computational cost and accuracy for the excited state geometry optimization of large system. Nishimura et al. [19] have shown that the CIS level computed excited state structural deformation in tropolone agrees with the experimental results. The CIS level computation also reproduced satisfactorily the intermolecular geometry of phenol–methanol cluster in the excited state [20]. This agreement was based on the comparison of rotational constants of cluster as well as for five intermolecular parameters that describe the orientation of the monomer units.
3. Results and discussion Hydrated forms of guanine studied in the present work were obtained by adding 19 and 27 water molecules and the resulting complexes will be called, hereafter, as G.19H2O and G.27H2O, respectively. The fully optimized geometries of these complexes
W7 W2
255
are shown in the Figs. 1 and 2 respectively along with the atomic numbering schemes and their front and side views. Important geometrical parameters of these complexes are shown in the Table 1. Earlier, we have performed detailed and systematic theoretical investigations of effect of hydration on the ground and electronic lowest singlet pp* excited state of guanine by considering 1, 3, 5–13 water molecules. For comparison, the important parameters for isolated guanine, and hydrated guanine obtained at the same theoretical levels are also shown in the Table 1 [14,15]. Based upon earlier investigations we found that the guanine in the electronic lowest singlet pp* excited state has significantly nonplanar geometry [13–15]. The degree as well as mode of hydration was found to have considerable influence on the structural deformation of guanine in the electronic lowest singlet pp* excited state [14,15]. In other world, the location as well as number of water molecules in the hydration has significant role in determining the excited state geometry of guanine. It was inferred that hydration will significantly influence the excited state dynamics of guanine. These results suggested that experimental data of guanine obtained with selected number of water molecules should not be extrapolated to bulk water solution. The optimized electronic lowest singlet pp* excited state of guanine and hydrated complexes was characterized by the HOMO ? LUMO configuration [14,15]. Further,
W1
W18
2.058 W8
O2 1.905 W10 W3
W14
2.020
C6
W19 W9
N7 C5
W13
N1
C8
W11
N9
N3 W15
N2
H21
W16
C4
C2
2.129
W12 W17 H22
2.092
1.987 W5
W4
W6
G.19H2O-S0
G.19H2O-S0 W1 W7
W2
W18
1.854 2.014
O6
W8
W14
W10
C6 W3
W13 W19
C5
N1
2.037
N7 C8
W11
W9
H21
C2 N2
C4 N9 W15
N3
W12
H22
2.049 W16
2.197
W17
1.934
W5 W6 W4
G.19H2O-S1
G.19H2O-S1
Fig. 1. Ground (S0) and electronic lowest singlet excited state (S1) geometries of the G.19H2O complex. Both front and side views are given. W represents a water molecule.
256
M.K. Shukla, J. Leszczynski / Chemical Physics Letters 478 (2009) 254–259
W24
2.077 W1 W18
2.776
2.046
W7
H21
W17
2.521
C8
W21
W25
N9
N2
N3
W15
H22
2.168
W22
C4
C2
W9
W16
W26
N7
W19 W12
2.101 W11
W10
2.147
C5
N1
W3
W23
2.235 C6
2.074
W8
W14
O6 W13
W2
2.155
W20
2.028 W5 W6
W4
W27
G.27H2O-S0
G.27H2O-S0 2.031
W24 W1
2.027
W18 W14 W13
W7 W2 W8
2.854
2.115
W19
W10 W3
2.046
W11
W17 W9
H21
N2
2.155
O6
W12
C6
W23
2.273 N7
N1
C5
C2 W15
C4
W22
W26
C8 N3
2.360 N9
W25
H22 2.165 W16
2.133
W5
W21
2.068
W20
W4 W6
W27
G.27H2O-S1
G.27H2O-S1
Fig. 2. Ground (S0) and electronic lowest singlet excited state (S1) geometries of the G.27H2O complex. Both front and side views are given. W represents a water molecule.
Table 1 Selected dihedral angles (°) and amino group angles (°) of guanine and different hydrated complexes in the electronic lowest singlet pp* excited state obtained at the CIS/6311G(d,p) level.a Parameters
G
G + 1W
G + 3W
G + 5W
G + 6W
G + 7W1
G + 7W2
G + 7W3
G + 8W
H21N2C2 H22N2C2 H21N2H22 P 360- HNH C6N1C2N3 N1C2N3C4 C2N3C4C5 N3C4C5C6 N1C6C5C4 N2C2N3C4 H21N2C2N1 H22N2C2N1
115.3 112.7 111.4 20.6 64.0 44.2 2.4 18.5 0.6 161.4 42.3 171.8
117.1 114.3 113.8 14.8 64.7 39.2 2.0 18.1 7.3 159.7 31.0 167.9
116.7 114.4 113.3 15.6 64.8 42.4 0.0 18.8 3.3 160.5 34.8 170.4
119.2 120.4 119.8 0.6 38.1 1.7 32.2 32.2 2.6 177.3 10.2 178.7
119.2 120.4 119.9 0.5 43.0 6.5 29.0 29.7 5.4 179.7 10.6 177.4
119.2 120.1 119.9 0.8 37.1 2.3 30.6 31.0 2.2 177.2 14.8 175.8
119.1 120.2 119.9 0.8 43.9 7.3 28.6 29.5 5.8 179.1 11.2 178.5
119.1 120.5 119.8 0.6 46.5 10.2 26.5 28.0 7.1 177.3 10.9 178.2
119.1 120.2 120.0 0.7 34.9 0.9 29.4 27.6 5.0 175.9 1.7 172.6
G + 9W
G + 10W
G + 11W1
G + 11W2
G + 12W
G + 13W
G + 19W
G + 27W
122.8 118.6 116.4 2.2 32.6 0.2 31.4 32.5 1.2 174.9 21.8 175.8
122.4 118.6 116.1 2.9 32.4 0.6 31.8 32.7 1.1 174.6 23.1 177.0
114.5 114.2 114.2 17.1 67.2 51.4 6.9 20.9 5.9 164.0 32.2 166.6
115.7 114.4 112.5 17.4 65.4 35.4 6.5 15.3 15.5 161.8 41.9 175.1
114.7 114.3 114.3 16.7 67.3 51.2 6.8 20.7 5.4 164.1 31.6 166.4
116.9 116.1 113.4 13.6 63.7 31.5 9.7 16.6 15.9 162.9 33.2 171.4
118.3 119.7 115.1 6.7 53.4 17.6 21.7 25.5 10.0 171.8 18.0 167.5
121.8 120.6 117.6 0 29.4 2.3 29.3 26.6 3.9 173.6 2.6 178.1
H21N2C2 H22N2C2 H21N2H22 P 360- HNH C6N1C2N3 N1C2N3C4 C2N3C4C5 N3C4C5C6 N1C6C5C4 N2C2N3C4 H21N2C2N1 H22N2C2N1 a
W represents a water molecule. Data for guanine and G + nW (n = 1, 3, 5–13) were taken from Refs. [14,15].
M.K. Shukla, J. Leszczynski / Chemical Physics Letters 478 (2009) 254–259
although the mode of excited state structural deformation was found to be hydration dependent, but interestingly, the nonplanarity was localized only in the six-membered ring in all considered systems. We also analyzed stretching vibrational frequencies of guanine and found that both degree and mode of hydration significantly influence the energy of these vibrations. The ground state optimized geometry of G.19H2O complex shows that the most of the water molecules are on one side from the approximate guanine plane (Fig. 1). Further, most of the water molecules are oriented towards the six-membered part of the ring and thus away from the C8H site of guanine. Such accumulation of water molecules appears due to the presence of more hydrogen bonding sites (in the form of acceptors and donors) in the sixmembered than the five membered ring of guanine and due to stronger nature of water–water interactions. It is interesting to note that none of the water molecule is involved in interaction with the N7 site of guanine. On the other hand, carbonyl group of guanine acts as bi-hydrogen bond acceptor to W1 and W2 water molecules. The W3, W16 and W6 water molecules are involved in hydrogen bond accepting interaction with N1H, N2H21 and N9H sites, respectively, while the W5 water molecule is acting as hydrogen bond donor with the N3 site of the guanine (Fig. 1). The interaction of the W16 water molecule with N2H21 site causes significant pyramidalization (15.8°) in amino group. In the electronic lowest singlet pp* excited state of the G.19H2O complex, guanine adopts significantly nonplanar geometry. The nonplanarity is mainly localized at the six-membered ring. Subsequently, the hydration structure is significantly modified compared to that in the ground state. The W1 and W2 water molecules are more strongly bonded to the carbonyl group in the excited state than that in the ground state. This fact is evident from the correspondingly reduced hydrogen bond distance in the excited state (Fig. 1). The W3 water molecule, which was hydrogen bonded to the N1H site in the ground state, is not involved in such interaction in the excited state. The amino group hydrogens are hydrogen bonded to water molecules (W3 and W16) and such interaction is responsible for the reduced amount of amino group pyramidalization in the excited state compared to that in the ground state (Table 1). Further, the W6 water molecule forms stronger bond with the N9H site and W5 forms weaker bond with the N3 site of guanine in the excited state. In the isolated guanine, the C2N3 and C4C5 bonds were found to be increased by about 0.107 and 0.064 Å, respectively and the N3C4 bond was decreased by about 0.071 Å in the excited state with respect to the corresponding ground state values. However, for the G.19H2O complex, the C2N3 and N3C4 bonds of guanine were revealed to be increased and decreased, respectively, by about 0.04 Å and C4C5 bond was found to be increased by about 0.08 Å in the excited state compared to that in the ground state. These discussion(s) reflects remarkable difference among bond length of isolated and hydrated guanine in the excited state. The quantitative information about bond lengths and bond angles of guanine and hydrated guanine can be obtained from Table S1 of the ‘Supplementary material’. One notices that in the excited state the selected dihedral angles of isolated and hydrated forms of guanine presented in the Table 1 are significantly different. In the excited state the C2N3C4C5 and N1C6C5C4 are almost planar for the isolated guanine but significantly deformed in the G.19H2O complex. Appreciably large change among other dihedral angles is also revealed in the isolated and hydrated forms in the excited state. The ground state optimized geometry of the G.27H2O complex shows significant number of water molecules that are on one side of the approximate guanine plane and only a few water molecules are on the other side near the N7C8N9 fragment. Obviously, the increased amount of water molecules forms more contacts (interactions) with different sites of guanine. Therefore, it is not surprising
257
that in this complex the N7 site of guanine acts as a dihydrogen bond acceptor while the carbonyl group acts as a tri-hydrogen bond acceptor (one hydrogen bond is very weak with bond distance of 2.776 Å). Other hydrogen bond donating and accepting sites (N1H, NH2, N9H and N3) are also involved in hydrogen bond interaction with water molecules. Consequent to the large number of water molecules in this complex the C8H site is also involved in a comparatively weak hydrogen bond donating interaction with a water molecule (W21); the hydrogen bond distance being 2.521 Å (Fig. 2). Since both amino group hydrogens are engaged in interactions with water molecules, the amino group pyramidalization was found to be smaller than that in the isolated guanine and that in the ground state of G.19H2O complex. The electronic lowest singlet pp* excited state geometry of guanine in the G.27H2O complex is also predicted to be significantly nonplanar. This feature is localized at the six-membered ring. However, major restructuring in the hydration structure of this complex, compared to the ground state, is not revealed. For example, consequent to the structural nonplanarity of guanine in the excited state neither of G H2O hydrogen bond is broken (nor formed) compared to that in the ground state. Although, some change in hydrogen bond distances is revealed. In the excited state, the C8H and NH2 groups interact more strongly with water molecules while N1H, N9H, and N3 sites form comparatively less strong hydrogen bonds with the respective water molecules. Hydrogen bond length reversal consequent to electronic excitation is predicted for those associated with the N7 site. Among three hydrogen bonds formed between the carbonyl group of guanine and water molecules in the ground state, two become stronger while the remaining one becomes weaker, consequent to the electronic excitation to the S1(pp*) excited state of the G.27H2O complex. As the result of electronic excitation of the complex, the C4C5 and C4N9 bonds are increased by about 0.1 and 0.05 Å, respectively, while other bonds are comparatively less affected. The values of dihedral angles shown in the Table 1 suggest that mode of excited state structural deformation of guanine in the G.27H2O complex is quite different than that in the G.19H2O. For example, the N1C2N3C4 and N1C6C5C4 planes of guanine are approximately planar in the former complex while they are about 17° and 10° respectively away from the planarity in the latter complex. The C6N1C2N3 plane of guanine is comparatively less nonplanar (about 20°) in the G.27H2O complex compared to that in the G.19H2O in excited state. Further, amino group of guanine is significantly nonplanar for the G.19H2O while planar in the G.27H2O complex in the excited state. It should be noted that the computed dihedral angles for amino-hydrogens are obtained due to the rotation of the amino group (Table 1). Fig. 3 shows the effect of degree as well as modes of hydration on the structural nonplanarity, in the form of variation of C6N1C2N3, N1C2N3C4, C2N3C4C5, N3C4C5C6 and N1C6C5C4 dihedral angles, of guanine in the electronic lowest singlet pp* excited state. In our earlier investigations, guanine and hydrated guanine (G.nH2O; n = 1, 3, 5–13) were arranged in three groups [14,15]. The first group belongs to complexes with 5–10 water molecules, second groups contains isolated guanine and hydrated guanine with 1, 3, 11 (one configuration) and 12 water molecules while complexes with 11 (other configuration) and 13 water molecules belongs to the third group. The division of these complexes was based upon the mode of nonplanarity (similarity and differences among dihedral angles) in guanine in the excited state. The excited state structural nonplanarity of guanine in the G.27H2O complex is similar to those species belonging to the first group. Though, the G.19H2O complex is closer to the first group than others, but the main difference lies in the C6N1C2N3 and N1C2N3C4 dihedral angles which have larger magnitude than for the other members of the group (Table 1, Fig. 3).
258
M.K. Shukla, J. Leszczynski / Chemical Physics Letters 478 (2009) 254–259 80.0
C6N1C2N3 60.0
0
Dihedral Angle ( )
40.0
N3C4C5C6
20.0
N1C6C5C4 0.0 C2N3C4C5 -20.0
-40.0
G+27W
G+13W
G+19W
G+12W
G+11W1
G+11W2
G+9W
G+10W
G+8W
G+7W3
G+7W1
G+7W2
G+5W
G+6W
G+3W
G
G+1W
N1C2N3C4
-60.0
Fig. 3. The variation of important dihedral angles of guanine with degree of hydration in the electronic lowest singlet excited state. W represents a water molecule.
The optimized electronic lowest singlet pp* excited state of G.19H2O and G.27H2O complexes are characterized by the HOMO ? LUMO configuration. These orbitals are shown in the Fig. 4. We have shown earlier that the corresponding state of the isolated and the other hydrated complexes are also characterized by the similar configuration. It is evident from the Fig. 4 that HOMO of G.19H2O and G.27H2O complexes corresponds to the p-type orbital and has similar nature. The LUMO is localized mainly on the six-membered ring of guanine and is a p*-type. However, the distribution of the LUMO is different for the studied hydrated complexes. Further, orbital contamination from water is not revealed for the electronic excitation configuration of guanine. The difference in the LUMO distribution appears to be responsible for the distinct electronic singlet excited state structural deformation of guanine in the G.19H2O and G.27H2O complexes. Nucleic acid bases absorb the ultraviolet light efficiently, but the quantum efficiency of radiative emission is very poor; the most part of the absorbed energy is released in the form of heat through the ultrafast nonradiative processes [13,21,22]. Consequently, nucleic acid bases have ultrashort excited state life-time. Different experimental and theoretical investigations have been devoted to understand the mechanism of the ultrafast excited state processes in nucleic acids and detailed lucid analysis of which can be found in recent articles [13,21–27]. On the basis of the mass-selected femtosecond time resolved pump–probe resonant ionization study
Fig. 4. HOMO and LUMO of optimized electronic lowest singlet pp* excited state of G.19H2O and G.27H2O complexes.
M.K. Shukla, J. Leszczynski / Chemical Physics Letters 478 (2009) 254–259
Canuel et al. [28] have suggested that the nonplanarity of pyrimidine ring and out-of-plane vibrations of amino group are important in providing the nonradiative decay pathway in adenine and other nucleic acid bases. Although, a detailed analysis about excited state dynamics of guanine is beyond the scope of the current work, however, brief description of such process in relation with guanine hydration is discussed. Based upon the theoretical calculations it was found that large S1 excited state geometrical deformation in 9-methylguanine compared to the 7-methylguanine is responsible for the increased nonadiabatic transition probability and thus shorter life-time in former than the latter species [29]. On the basis of CASPT2/CASSCF level of theoretical calculations, a conical intersection between the lowest singlet pp* excited state and the ground state was suggested to be responsible for the ultrafast nonradiative decay in guanine [30– 32]. The role of NH bond in the nonradiative deactivation is also revealed [31,32]. In another calculation at the DFT/MRCI level [33] the out-of-plane distortion induced ultrafast nonradiative deactivation in stable tautomers of guanine, namely, keto-N9H, ketoN7H and enol-N9H-cis, was suggested to be responsible for the absent of discrete bands of the corresponding tautomers in the UV spectra. Recently, three state model for nonradiative decay in guanine has been suggested by Serrano-Andres et al. [34] at the CASPT2/CASSCF level where importance of two lower lying electronic singlet pp* states and the lowest np* state are revealed. Thus, detailed theoretical and experimental investigations, as briefly discussed above, suggest that excited state geometrical nonplanarity and subsequent intersection of ground and excited state potential energy surfaces along some reaction coordinates are responsible for the ultrafast nonradiative deactivation in guanine and other nucleic acid bases. Our theoretical calculations clearly show that degree as well as mode of hydration has important effect on the excited state structural nonplanarity of guanine. Therefore, it is expected that degree and mode of hydration will significantly influence the excited state dynamics of guanine. We would like to point out that in the present investigation of hydration of guanine we have only considered the static picture. For the larger cluster several configurations of hydration of guanine are possible and it is in fact formidable task to study all of them at the ab initio level of theory. However, in real aqueous solution guanine will undeniably be surrounded by several water molecules probably forming a water cage. Such investigation is currently in the advanced stage in our laboratory and will be published in the near future. 4. Conclusion We found that degree and mode of hydration of guanine has important effect on its ground and excited state properties. The formation of complex with 19 water molecules results in appreciably more nonplanar electronic singlet lowest excited state geometry than hydration with the 27 water molecules. Consequently, under electronic excitation the hydration structure of G.19H2O is significantly more rearranged than that in the G.27H2O complex. This study further supports that excited state dynamics of hydrated guanine will significantly depend upon the degree as well as the mode of hydration.
259
Acknowledgements Authors are thankful to financial supports from NSF CREST Grant No. HRD-0833178. Authors are also thankful to the Mississippi Center for Supercomputing Research (MCSR) for the generous computational facility. Appendix A. Supplementary material Supplementary data associated with this article can be found, in the online version, at doi:10.1016/j.cplett.2009.07.081. References [1] R.E. Franklin, R.G. Gosling, Acta Cryst 6 (1953) 673. [2] V.I. Poltev, A.V. Teplukhin, G.G. Malenkov, Int. J. Quantum Chem. 42 (1992) 1499. [3] B. Schneider, D. Cohen, H.M. Berman, Biopolymers 32 (1992) 725. [4] R. Brandes, A. Rupprecht, D.R. Kearns, J. Biophys. 56 (1989) 683. [5] H. Shindo, Y. Hiyama, S. Roy, J.S. Cohen, D.A. Torchia, Bull. Chem. Soc. Jpn. 60 (1987) 1631. [6] J. Leszczynski, in: M. Hargittai, I. Hargittai (Eds.), Advances in Molecular Structure Research, Vol. 6, JAI Press, Stamford, CT, 2000, p. 209. [7] S.A. Trygubenko et al., Phys. Chem. Chem. Phys. 4 (2002) 4192. [8] M. Hanus, F. Ryjacek, M. Kabelac, T. Kubar, T.V. Bogdan, S.A. Trygubenko, P. Hobza, J. Am. Chem. Soc. 125 (2003) 7678. [9] O.V. Shishkin, L. Gorb, J. Leszczynski, Int. J. Mol. Sci. 1 (2000) 17. [10] O.V. Shishkin, L. Gorb, J. Leszczynski, J. Phys. Chem. B 104 (2000) 5357. [11] O.S. Sukhanov, O.V. Shishkin, L. Gorb, Y. Podolyan, J. Leszczynski, J. Phys. Chem. B 107 (2003) 2846. [12] D. Nachtigallova, P. Hobza, V. Spirko, J. Phys. Chem. A 112 (2008) 1854. [13] M.K. Shukla, Jerzy Leszczynski, J. Biomol. Struct. Dynam. 25 (2007) 93. [14] M.K. Shukla, Jerzy Leszczynski, J. Phys. Chem. B 109 (2005) 17333. [15] M.K. Shukla, Jerzy Leszczynski, J. Phys. Chem. B 112 (2008) 5139. [16] J.B. Foresman, M. Head-Gordon, J.A. Pople, M.J. Frisch, J. Phys. Chem. 96 (1992) 135. [17] M.J. Frisch et al., GAUSSIAN 03, Revision B.03, Gaussian, Inc., Pittsburgh PA, 2003. [18] MOLEKEL 4.3, P. Flükiger, H.P. Lüthi, S. Portmann, J. Weber, Swiss Center for Scientific Computing, Manno (Switzerland), 2000. www.cscs.ch/molekel. [19] Y. Nishimura, T. Tsuji, H. Sekiya, J. Phys. Chem. A 105 (2001) 7273. [20] J. Kupper, A. Westphal, M. Schmitt, Chem. Phys. 263 (2001) 41. [21] C.E. Crespo-Hernandez, B. Cohen, P.M. Hare, B. Kohler, Chem. Rev. 104 (2004) 1977. [22] C.T. Middleton, K. de La Harpe, C. Su, Y.K. Law, C.E. Crespo-Hernandez, B. Kohler, Annu. Rev. Phys. Chem. 60 (2009) 217. [23] M. Barbatti, B. Sellner, A.J.A. Aquino, H. Lischka, in: M.K. Shukla and J. Leszczynski (Eds.), Radiation Induced Molecular Phenomena in Nucleic Acids, in: J. Leszczynski (Ed.), Challenges and Advances in Computational Chemistry and Physics, vol. 5, Springer Science + Business Media B.V., 2008, p. 209. [24] M. Mons, I. Dimicoli, F. Piuzzi, in: M.K. Shukla, J. Leszczynski (Eds.), Radiation Induced Molecular Phenomena in Nucleic Acids, in: J. Leszczynski (Ed.), Challenges and Advances in Computational Chemistry and Physics, vol. 5, Springer Science + Business Media B.V., 2008, p. 343. [25] L. Serrano-Andres, M. Merchan, in: M.K. Shukla, J. Leszczynski (Eds.), Radiation Induced Molecular Phenomena in Nucleic Acids, in: J. Leszczynski (Ed.), Challenges and Advances in Computational Chemistry and Physics, vol. 5, Springer Science + Business Media B.V., 2008, p. 435. [26] L. Blancafort, M.J. Bearpark, M.A. Robb, in: M.K. Shukla, J. Leszczynski (Eds.), Radiation Induced Molecular Phenomena in Nucleic Acids, in: J. Leszczynski (Ed.), Challenges and Advances in Computational Chemistry and Physics, vol. 5, Springer Science + Business Media B.V., 2008, p. 473. [27] S. Perun, A.L. Sobolewski, W. Domcke, J. Am. Chem. Soc. 127 (2005) 6257. [28] C. Canuel, M. Mons, F. Piuzzi, B. Tardivel, I. Dimicoli, M. Elhanine, J. Chem. Phys. 122 (2005) 74316. [29] H. Langer, N.L. Doltsinis, Phys. Chem. Chem. Phys. 6 (2004) 2742. [30] H. Chen, S. Li, J. Chem. Phys. 124 (2006) 154315. [31] S. Yamazaki, W. Domcke, A. Sobolewski, J. Phys. Chem. A 112 (2008) 11965. [32] S. Yamazaki, W. Domcke, J. Phys. Chem. A 112 (2008) 7090. [33] C.M. Marian, J. Phys. Chem. A 111 (2007) 1545. [34] L. Serrano-Andres, M. Merchan, A.C. Borin, J. Am. Chem. Soc. 130 (2008) 2473.
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Chemical Physics Letters journal homepage: www.elsevier.com/locate/cplett
Hydration of guanine: Electronic singlet excited states for complexes with 19 and 27 water molecules M.K. Shukla, Jerzy Leszczynski * NSF CREST Interdisplinary Nanotoxicity Center, Department of Chemistry and Biochemistry, Jackson State University, Jackson, MS 39217, USA
a r t i c l e
i n f o
Article history: Received 14 May 2009 In final form 26 July 2009 Available online 29 July 2009
a b s t r a c t Computational investigation on the ground and electronic lowest singlet pp* excited state (S1(pp*)) of guanine hydrated by a large number (19 and 27) water molecules are reported and obtained results are compared with those for isolated guanine and the comparatively smaller hydrated complexes. Ground state geometries were optimized at the HF level and Configuration Interaction-Singles (CIS) method was used for excited state geometry optimization utilizing the 6-311G(d,p) basis set. It was found that excited state geometry of guanine is significantly different with each other in the studied complexes. The possible effect of hydration on the excited state dynamics of guanine is also discussed. Ó 2009 Elsevier B.V. All rights reserved.
1. Introduction Water is an essential part of everybody’s life. Therefore, it is not unexpected that in the quest for search of life on other planets and solar systems, experts look for the water signature. Deoxyribonucleic acid (DNA), another vital life’s component, is the genetic carrier where information is stored in the form of specific patterns of hydrogen bonds formed between complementary purine and pyrimidine bases. Structures and functions of nucleic acids significantly depend upon the hydration [1,2]. In fact, DNA in vivo is significantly hydrated; the degree of hydration depends upon the relative humidity, types of DNA, major and minor grooves and the type of bases [3]. Nuclear Magnetic Resonance (NMR) results have suggested that the relative humidity and temperature control the movement of backbone as well as bases in nucleic acids [4,5]. Relative stability of some minor nucleic acid tautomers have been found to be increased due to hydration [6–8]. Theoretical calculations have suggested that polyhydration can cause ground state geometrical distortion among nucleic acid bases [9–11]. Guanine is one of the important building blocks of nucleic acids. It exhibits the largest number of minor tautomers among all nucleic acid bases [6,12,13]. It is the site for the most efficient oxidative damage, has lowest ionization potential, electron affinity and largest amino group pyramidalization among bases [13]. Although, the ground state geometry of guanine is planar, except the amino group which is pyramidal, the electronic singlet excited state geometry has been predicted to be strongly nonplanar [13]. Significant geometrical distortion in the excited state of guanine has been suggested to be responsible for the efficient nonradiative decays via the conical intersection between the ground and excited * Corresponding author. E-mail address: [email protected] (J. Leszczynski). 0009-2614/$ - see front matter Ó 2009 Elsevier B.V. All rights reserved. doi:10.1016/j.cplett.2009.07.081
state potential energy surfaces [13]. We performed detailed theoretical investigation on ground and excited state structures of hydrated guanine by considering 1, 3, 5–13 water molecules around guanine [14,15]. Hydration dependent electronic singlet pp* excited state structural distortion of guanine was revealed in these studies. The main objective of the current work is to understand the structures and properties of guanine under significantly large and diverse hydration condition by considering 19 and 27 water molecules in the solvation shells. In the first complex all 19 water molecules are on the one side while in the second complex significant number of water molecules are also at the other side of guanine. This creates diverse water environments that might result in distinctive properties of the studied clusters. The current investigation provides information about the influence of large hydration on excited state geometry of guanine and that of the electronic singlet excited state dynamics. 2. Computational details Ground state geometries of hydrated guanine were optimized at the Hartree–Fock (HF) level, while the geometries in the electronic lowest singlet pp* excited state were optimized at the Configuration Interaction-Singles (CIS) level [16]. The harmonic vibrational frequencies were computed for ground state optimized geometries to ascertain the nature of potential energy surfaces (PESs). The absence of imaginary vibrational frequency suggested all computed geometries to be at least local minima at the respective PESs. The inclusion of such a large number of water molecules will generate structures of numerous hydration configuration of guanine–water complex. It will be impossible to investigate all of them at the ab initio or DFT level of theories. Therefore, search for the global minimum structure for each of the complex was not performed.
M.K. Shukla, J. Leszczynski / Chemical Physics Letters 478 (2009) 254–259
The 6-311G(d,p) basis set was used throughout the computation. Calculations were performed using the GAUSSIAN 03 program [17]. Molecular orbitals were visualized using the MOLEKEL program [18]. Although, the CIS method is an HF analog for excited state which does not account for the electron correlation [16], but it offers reasonable compromise between the computational cost and accuracy for the excited state geometry optimization of large system. Nishimura et al. [19] have shown that the CIS level computed excited state structural deformation in tropolone agrees with the experimental results. The CIS level computation also reproduced satisfactorily the intermolecular geometry of phenol–methanol cluster in the excited state [20]. This agreement was based on the comparison of rotational constants of cluster as well as for five intermolecular parameters that describe the orientation of the monomer units.
3. Results and discussion Hydrated forms of guanine studied in the present work were obtained by adding 19 and 27 water molecules and the resulting complexes will be called, hereafter, as G.19H2O and G.27H2O, respectively. The fully optimized geometries of these complexes
W7 W2
255
are shown in the Figs. 1 and 2 respectively along with the atomic numbering schemes and their front and side views. Important geometrical parameters of these complexes are shown in the Table 1. Earlier, we have performed detailed and systematic theoretical investigations of effect of hydration on the ground and electronic lowest singlet pp* excited state of guanine by considering 1, 3, 5–13 water molecules. For comparison, the important parameters for isolated guanine, and hydrated guanine obtained at the same theoretical levels are also shown in the Table 1 [14,15]. Based upon earlier investigations we found that the guanine in the electronic lowest singlet pp* excited state has significantly nonplanar geometry [13–15]. The degree as well as mode of hydration was found to have considerable influence on the structural deformation of guanine in the electronic lowest singlet pp* excited state [14,15]. In other world, the location as well as number of water molecules in the hydration has significant role in determining the excited state geometry of guanine. It was inferred that hydration will significantly influence the excited state dynamics of guanine. These results suggested that experimental data of guanine obtained with selected number of water molecules should not be extrapolated to bulk water solution. The optimized electronic lowest singlet pp* excited state of guanine and hydrated complexes was characterized by the HOMO ? LUMO configuration [14,15]. Further,
W1
W18
2.058 W8
O2 1.905 W10 W3
W14
2.020
C6
W19 W9
N7 C5
W13
N1
C8
W11
N9
N3 W15
N2
H21
W16
C4
C2
2.129
W12 W17 H22
2.092
1.987 W5
W4
W6
G.19H2O-S0
G.19H2O-S0 W1 W7
W2
W18
1.854 2.014
O6
W8
W14
W10
C6 W3
W13 W19
C5
N1
2.037
N7 C8
W11
W9
H21
C2 N2
C4 N9 W15
N3
W12
H22
2.049 W16
2.197
W17
1.934
W5 W6 W4
G.19H2O-S1
G.19H2O-S1
Fig. 1. Ground (S0) and electronic lowest singlet excited state (S1) geometries of the G.19H2O complex. Both front and side views are given. W represents a water molecule.
256
M.K. Shukla, J. Leszczynski / Chemical Physics Letters 478 (2009) 254–259
W24
2.077 W1 W18
2.776
2.046
W7
H21
W17
2.521
C8
W21
W25
N9
N2
N3
W15
H22
2.168
W22
C4
C2
W9
W16
W26
N7
W19 W12
2.101 W11
W10
2.147
C5
N1
W3
W23
2.235 C6
2.074
W8
W14
O6 W13
W2
2.155
W20
2.028 W5 W6
W4
W27
G.27H2O-S0
G.27H2O-S0 2.031
W24 W1
2.027
W18 W14 W13
W7 W2 W8
2.854
2.115
W19
W10 W3
2.046
W11
W17 W9
H21
N2
2.155
O6
W12
C6
W23
2.273 N7
N1
C5
C2 W15
C4
W22
W26
C8 N3
2.360 N9
W25
H22 2.165 W16
2.133
W5
W21
2.068
W20
W4 W6
W27
G.27H2O-S1
G.27H2O-S1
Fig. 2. Ground (S0) and electronic lowest singlet excited state (S1) geometries of the G.27H2O complex. Both front and side views are given. W represents a water molecule.
Table 1 Selected dihedral angles (°) and amino group angles (°) of guanine and different hydrated complexes in the electronic lowest singlet pp* excited state obtained at the CIS/6311G(d,p) level.a Parameters
G
G + 1W
G + 3W
G + 5W
G + 6W
G + 7W1
G + 7W2
G + 7W3
G + 8W
H21N2C2 H22N2C2 H21N2H22 P 360- HNH C6N1C2N3 N1C2N3C4 C2N3C4C5 N3C4C5C6 N1C6C5C4 N2C2N3C4 H21N2C2N1 H22N2C2N1
115.3 112.7 111.4 20.6 64.0 44.2 2.4 18.5 0.6 161.4 42.3 171.8
117.1 114.3 113.8 14.8 64.7 39.2 2.0 18.1 7.3 159.7 31.0 167.9
116.7 114.4 113.3 15.6 64.8 42.4 0.0 18.8 3.3 160.5 34.8 170.4
119.2 120.4 119.8 0.6 38.1 1.7 32.2 32.2 2.6 177.3 10.2 178.7
119.2 120.4 119.9 0.5 43.0 6.5 29.0 29.7 5.4 179.7 10.6 177.4
119.2 120.1 119.9 0.8 37.1 2.3 30.6 31.0 2.2 177.2 14.8 175.8
119.1 120.2 119.9 0.8 43.9 7.3 28.6 29.5 5.8 179.1 11.2 178.5
119.1 120.5 119.8 0.6 46.5 10.2 26.5 28.0 7.1 177.3 10.9 178.2
119.1 120.2 120.0 0.7 34.9 0.9 29.4 27.6 5.0 175.9 1.7 172.6
G + 9W
G + 10W
G + 11W1
G + 11W2
G + 12W
G + 13W
G + 19W
G + 27W
122.8 118.6 116.4 2.2 32.6 0.2 31.4 32.5 1.2 174.9 21.8 175.8
122.4 118.6 116.1 2.9 32.4 0.6 31.8 32.7 1.1 174.6 23.1 177.0
114.5 114.2 114.2 17.1 67.2 51.4 6.9 20.9 5.9 164.0 32.2 166.6
115.7 114.4 112.5 17.4 65.4 35.4 6.5 15.3 15.5 161.8 41.9 175.1
114.7 114.3 114.3 16.7 67.3 51.2 6.8 20.7 5.4 164.1 31.6 166.4
116.9 116.1 113.4 13.6 63.7 31.5 9.7 16.6 15.9 162.9 33.2 171.4
118.3 119.7 115.1 6.7 53.4 17.6 21.7 25.5 10.0 171.8 18.0 167.5
121.8 120.6 117.6 0 29.4 2.3 29.3 26.6 3.9 173.6 2.6 178.1
H21N2C2 H22N2C2 H21N2H22 P 360- HNH C6N1C2N3 N1C2N3C4 C2N3C4C5 N3C4C5C6 N1C6C5C4 N2C2N3C4 H21N2C2N1 H22N2C2N1 a
W represents a water molecule. Data for guanine and G + nW (n = 1, 3, 5–13) were taken from Refs. [14,15].
M.K. Shukla, J. Leszczynski / Chemical Physics Letters 478 (2009) 254–259
although the mode of excited state structural deformation was found to be hydration dependent, but interestingly, the nonplanarity was localized only in the six-membered ring in all considered systems. We also analyzed stretching vibrational frequencies of guanine and found that both degree and mode of hydration significantly influence the energy of these vibrations. The ground state optimized geometry of G.19H2O complex shows that the most of the water molecules are on one side from the approximate guanine plane (Fig. 1). Further, most of the water molecules are oriented towards the six-membered part of the ring and thus away from the C8H site of guanine. Such accumulation of water molecules appears due to the presence of more hydrogen bonding sites (in the form of acceptors and donors) in the sixmembered than the five membered ring of guanine and due to stronger nature of water–water interactions. It is interesting to note that none of the water molecule is involved in interaction with the N7 site of guanine. On the other hand, carbonyl group of guanine acts as bi-hydrogen bond acceptor to W1 and W2 water molecules. The W3, W16 and W6 water molecules are involved in hydrogen bond accepting interaction with N1H, N2H21 and N9H sites, respectively, while the W5 water molecule is acting as hydrogen bond donor with the N3 site of the guanine (Fig. 1). The interaction of the W16 water molecule with N2H21 site causes significant pyramidalization (15.8°) in amino group. In the electronic lowest singlet pp* excited state of the G.19H2O complex, guanine adopts significantly nonplanar geometry. The nonplanarity is mainly localized at the six-membered ring. Subsequently, the hydration structure is significantly modified compared to that in the ground state. The W1 and W2 water molecules are more strongly bonded to the carbonyl group in the excited state than that in the ground state. This fact is evident from the correspondingly reduced hydrogen bond distance in the excited state (Fig. 1). The W3 water molecule, which was hydrogen bonded to the N1H site in the ground state, is not involved in such interaction in the excited state. The amino group hydrogens are hydrogen bonded to water molecules (W3 and W16) and such interaction is responsible for the reduced amount of amino group pyramidalization in the excited state compared to that in the ground state (Table 1). Further, the W6 water molecule forms stronger bond with the N9H site and W5 forms weaker bond with the N3 site of guanine in the excited state. In the isolated guanine, the C2N3 and C4C5 bonds were found to be increased by about 0.107 and 0.064 Å, respectively and the N3C4 bond was decreased by about 0.071 Å in the excited state with respect to the corresponding ground state values. However, for the G.19H2O complex, the C2N3 and N3C4 bonds of guanine were revealed to be increased and decreased, respectively, by about 0.04 Å and C4C5 bond was found to be increased by about 0.08 Å in the excited state compared to that in the ground state. These discussion(s) reflects remarkable difference among bond length of isolated and hydrated guanine in the excited state. The quantitative information about bond lengths and bond angles of guanine and hydrated guanine can be obtained from Table S1 of the ‘Supplementary material’. One notices that in the excited state the selected dihedral angles of isolated and hydrated forms of guanine presented in the Table 1 are significantly different. In the excited state the C2N3C4C5 and N1C6C5C4 are almost planar for the isolated guanine but significantly deformed in the G.19H2O complex. Appreciably large change among other dihedral angles is also revealed in the isolated and hydrated forms in the excited state. The ground state optimized geometry of the G.27H2O complex shows significant number of water molecules that are on one side of the approximate guanine plane and only a few water molecules are on the other side near the N7C8N9 fragment. Obviously, the increased amount of water molecules forms more contacts (interactions) with different sites of guanine. Therefore, it is not surprising
257
that in this complex the N7 site of guanine acts as a dihydrogen bond acceptor while the carbonyl group acts as a tri-hydrogen bond acceptor (one hydrogen bond is very weak with bond distance of 2.776 Å). Other hydrogen bond donating and accepting sites (N1H, NH2, N9H and N3) are also involved in hydrogen bond interaction with water molecules. Consequent to the large number of water molecules in this complex the C8H site is also involved in a comparatively weak hydrogen bond donating interaction with a water molecule (W21); the hydrogen bond distance being 2.521 Å (Fig. 2). Since both amino group hydrogens are engaged in interactions with water molecules, the amino group pyramidalization was found to be smaller than that in the isolated guanine and that in the ground state of G.19H2O complex. The electronic lowest singlet pp* excited state geometry of guanine in the G.27H2O complex is also predicted to be significantly nonplanar. This feature is localized at the six-membered ring. However, major restructuring in the hydration structure of this complex, compared to the ground state, is not revealed. For example, consequent to the structural nonplanarity of guanine in the excited state neither of G H2O hydrogen bond is broken (nor formed) compared to that in the ground state. Although, some change in hydrogen bond distances is revealed. In the excited state, the C8H and NH2 groups interact more strongly with water molecules while N1H, N9H, and N3 sites form comparatively less strong hydrogen bonds with the respective water molecules. Hydrogen bond length reversal consequent to electronic excitation is predicted for those associated with the N7 site. Among three hydrogen bonds formed between the carbonyl group of guanine and water molecules in the ground state, two become stronger while the remaining one becomes weaker, consequent to the electronic excitation to the S1(pp*) excited state of the G.27H2O complex. As the result of electronic excitation of the complex, the C4C5 and C4N9 bonds are increased by about 0.1 and 0.05 Å, respectively, while other bonds are comparatively less affected. The values of dihedral angles shown in the Table 1 suggest that mode of excited state structural deformation of guanine in the G.27H2O complex is quite different than that in the G.19H2O. For example, the N1C2N3C4 and N1C6C5C4 planes of guanine are approximately planar in the former complex while they are about 17° and 10° respectively away from the planarity in the latter complex. The C6N1C2N3 plane of guanine is comparatively less nonplanar (about 20°) in the G.27H2O complex compared to that in the G.19H2O in excited state. Further, amino group of guanine is significantly nonplanar for the G.19H2O while planar in the G.27H2O complex in the excited state. It should be noted that the computed dihedral angles for amino-hydrogens are obtained due to the rotation of the amino group (Table 1). Fig. 3 shows the effect of degree as well as modes of hydration on the structural nonplanarity, in the form of variation of C6N1C2N3, N1C2N3C4, C2N3C4C5, N3C4C5C6 and N1C6C5C4 dihedral angles, of guanine in the electronic lowest singlet pp* excited state. In our earlier investigations, guanine and hydrated guanine (G.nH2O; n = 1, 3, 5–13) were arranged in three groups [14,15]. The first group belongs to complexes with 5–10 water molecules, second groups contains isolated guanine and hydrated guanine with 1, 3, 11 (one configuration) and 12 water molecules while complexes with 11 (other configuration) and 13 water molecules belongs to the third group. The division of these complexes was based upon the mode of nonplanarity (similarity and differences among dihedral angles) in guanine in the excited state. The excited state structural nonplanarity of guanine in the G.27H2O complex is similar to those species belonging to the first group. Though, the G.19H2O complex is closer to the first group than others, but the main difference lies in the C6N1C2N3 and N1C2N3C4 dihedral angles which have larger magnitude than for the other members of the group (Table 1, Fig. 3).
258
M.K. Shukla, J. Leszczynski / Chemical Physics Letters 478 (2009) 254–259 80.0
C6N1C2N3 60.0
0
Dihedral Angle ( )
40.0
N3C4C5C6
20.0
N1C6C5C4 0.0 C2N3C4C5 -20.0
-40.0
G+27W
G+13W
G+19W
G+12W
G+11W1
G+11W2
G+9W
G+10W
G+8W
G+7W3
G+7W1
G+7W2
G+5W
G+6W
G+3W
G
G+1W
N1C2N3C4
-60.0
Fig. 3. The variation of important dihedral angles of guanine with degree of hydration in the electronic lowest singlet excited state. W represents a water molecule.
The optimized electronic lowest singlet pp* excited state of G.19H2O and G.27H2O complexes are characterized by the HOMO ? LUMO configuration. These orbitals are shown in the Fig. 4. We have shown earlier that the corresponding state of the isolated and the other hydrated complexes are also characterized by the similar configuration. It is evident from the Fig. 4 that HOMO of G.19H2O and G.27H2O complexes corresponds to the p-type orbital and has similar nature. The LUMO is localized mainly on the six-membered ring of guanine and is a p*-type. However, the distribution of the LUMO is different for the studied hydrated complexes. Further, orbital contamination from water is not revealed for the electronic excitation configuration of guanine. The difference in the LUMO distribution appears to be responsible for the distinct electronic singlet excited state structural deformation of guanine in the G.19H2O and G.27H2O complexes. Nucleic acid bases absorb the ultraviolet light efficiently, but the quantum efficiency of radiative emission is very poor; the most part of the absorbed energy is released in the form of heat through the ultrafast nonradiative processes [13,21,22]. Consequently, nucleic acid bases have ultrashort excited state life-time. Different experimental and theoretical investigations have been devoted to understand the mechanism of the ultrafast excited state processes in nucleic acids and detailed lucid analysis of which can be found in recent articles [13,21–27]. On the basis of the mass-selected femtosecond time resolved pump–probe resonant ionization study
Fig. 4. HOMO and LUMO of optimized electronic lowest singlet pp* excited state of G.19H2O and G.27H2O complexes.
M.K. Shukla, J. Leszczynski / Chemical Physics Letters 478 (2009) 254–259
Canuel et al. [28] have suggested that the nonplanarity of pyrimidine ring and out-of-plane vibrations of amino group are important in providing the nonradiative decay pathway in adenine and other nucleic acid bases. Although, a detailed analysis about excited state dynamics of guanine is beyond the scope of the current work, however, brief description of such process in relation with guanine hydration is discussed. Based upon the theoretical calculations it was found that large S1 excited state geometrical deformation in 9-methylguanine compared to the 7-methylguanine is responsible for the increased nonadiabatic transition probability and thus shorter life-time in former than the latter species [29]. On the basis of CASPT2/CASSCF level of theoretical calculations, a conical intersection between the lowest singlet pp* excited state and the ground state was suggested to be responsible for the ultrafast nonradiative decay in guanine [30– 32]. The role of NH bond in the nonradiative deactivation is also revealed [31,32]. In another calculation at the DFT/MRCI level [33] the out-of-plane distortion induced ultrafast nonradiative deactivation in stable tautomers of guanine, namely, keto-N9H, ketoN7H and enol-N9H-cis, was suggested to be responsible for the absent of discrete bands of the corresponding tautomers in the UV spectra. Recently, three state model for nonradiative decay in guanine has been suggested by Serrano-Andres et al. [34] at the CASPT2/CASSCF level where importance of two lower lying electronic singlet pp* states and the lowest np* state are revealed. Thus, detailed theoretical and experimental investigations, as briefly discussed above, suggest that excited state geometrical nonplanarity and subsequent intersection of ground and excited state potential energy surfaces along some reaction coordinates are responsible for the ultrafast nonradiative deactivation in guanine and other nucleic acid bases. Our theoretical calculations clearly show that degree as well as mode of hydration has important effect on the excited state structural nonplanarity of guanine. Therefore, it is expected that degree and mode of hydration will significantly influence the excited state dynamics of guanine. We would like to point out that in the present investigation of hydration of guanine we have only considered the static picture. For the larger cluster several configurations of hydration of guanine are possible and it is in fact formidable task to study all of them at the ab initio level of theory. However, in real aqueous solution guanine will undeniably be surrounded by several water molecules probably forming a water cage. Such investigation is currently in the advanced stage in our laboratory and will be published in the near future. 4. Conclusion We found that degree and mode of hydration of guanine has important effect on its ground and excited state properties. The formation of complex with 19 water molecules results in appreciably more nonplanar electronic singlet lowest excited state geometry than hydration with the 27 water molecules. Consequently, under electronic excitation the hydration structure of G.19H2O is significantly more rearranged than that in the G.27H2O complex. This study further supports that excited state dynamics of hydrated guanine will significantly depend upon the degree as well as the mode of hydration.
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