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Hydrogen bonding of thymine and uracil with surface of dickite: An ab initio study
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Journal of Molecular Structure 844–845 (2007) 48–58 www.elsevier.com/locate/molstruc
Hydrogen bonding of thymine and uracil with surface of dickite: An ab initio study q T.L. Robinson a, A. Michalkova a, L. Gorb b, J. Leszczynski a
a,*
Computational Center for Molecular Structure and Interactions, Department of Chemistry, Jackson State University, 1400 J.R. Lynch Street, P.O. Box 17910, Jackson, MS 39217, USA b US Army Engineer Research and Development Center (ERDC), Vicksburg, MS 39180, USA Received 5 February 2007; received in revised form 28 February 2007; accepted 1 March 2007 Available online 12 March 2007
Abstract The density functional theory (DFT) by means of the B3LYP functional and the 6-31G(d) basis set has been applied to analyze the hydrogen boding of selected nucleic acid bases (thymine and uracil) with the representative cluster models of the clay mineral, dickite. The results obtained from this investigation reveal that the formation of hydrogen bonds accounts for the stabilization of thymine and uracil on the mineral surface. The intermolecular distances and strength of the hydrogen bonds depend on the type of the surface (tetrahedral or octahedral) and on the hydration of the surface. Generally, thymine and uracil are less stable on the tetrahedral surface than on the octahedral surface. The most energetically favorable adsorption is predicted in the case of the system containing hydrated octahedral mineral fragment. The adsorption of thymine on the surface of dickite results in changes in geometry and polarization of thymine. These effects are more significant in the case of the octahedral adsorption than for the tetrahedral adsorption. Ó 2007 Elsevier B.V. All rights reserved. Keywords: Thymine; Uracil; Hydrogen bonding; Adsorption; Clay
1. Introduction Mineral surfaces have been suggested as providing substrates for support of the catalytic assembly of organic and biochemical molecules [1]. Specifically, clay minerals with their charged aluminosilicate layered structure were assumed to have the appropriate characteristics to harbor precursor organic molecules for the synthesis of important biomolecules. Many authors have suggested the involvement of surface chemistry on clays and other minerals in the prebiotic chemical evolution that culminated in the origin of life [2]. It was predicted that clay minerals could have bound the organic molecules from the surrounding water, concentrating them many times and acting as naturally q The authors dedicate this manuscript to Prof. Lucjan Sobczyk in appreciation of his fundamental work on hydrogen bonding. * Corresponding author. Tel.: +1 601 9793482; fax: +1 601 9797823. E-mail address: [email protected] (J. Leszczynski).
0022-2860/$ - see front matter Ó 2007 Elsevier B.V. All rights reserved. doi:10.1016/j.molstruc.2007.03.002
occurring environment for polymerization of large molecules, including self-replicating informational molecules [3–8]. This theory was supported by other studies (for review see Ref. [9]) where it was found that the genetic material retains its integrity and functionality upon interaction with clays while maintaining their biological activity. Moreover, since clays exist everywhere it is highly likely that they were important in protecting materials from degradation by adsorption on active sites [10]. Clays belong to the phyllosilicates group composed of two-dimensional structures. Phyllosilicates are aluminum silicates that form tetrahedral (fourfold coordination) and octahedral (sixfold coordination) sheets according to a cation and anion ratio [11,12]. The cations in a tetrahedral coordination include mostly Si4+. Substitution of Si4+ by Al3+ often occurs in the tetrahedral sheets and substitution of Al3+ by Si4+ or Mg2+ can occur in the octahedral sheets. Clays primarily exist as very small particles (2 lm in diameter) with a high specific surface area and a high
T.L. Robinson et al. / Journal of Molecular Structure 844–845 (2007) 48–58
chemical surface activity [13]. They are found in soil, lending to their importance in agriculture and the environment. Their structural diversities provide the functionality that is expected to give rise to important properties such as adsorption of ions and molecules. Minerals of the kaolinite group have 1:1 dioctahedral structure with the common chemical formula Al2Si2O5(OH)4 [14]. Dickite (a member of this group) differs from kaolinite in the layer stacking. The unit cell of dickite consists of two kaolinite layers and is twice as large as the unit cell of kaolinite. The layers are kept together by the hydrogen bridges between surface hydroxyl groups of the octahedral side and the basal oxygen atoms of the tetrahedral side [15]. Specifically, the nucleic acid adsorption on clay minerals was investigated as early as 1952 by Goring and Bartholomew [16]. Since then in several works DNA/RNA adsorption on clay minerals has been studied [17]. Ferris et al. [18] demonstrated the polymerization of oligonucleotides on clay. Nucleic acids adsorbed and bound on clay minerals are partially protected against degradation by nucleases and other degradative enzymes [19–25]. Two hypotheses have been suggested to describe the adsorption and binding of nucleic acids onto clays. According to Khanna et al. [26] one end of DNA is bound to the edges of the clay with a fraction of the DNA bound on the planar surface. Another model of the DNA–clay complexes has been described by Paget and Simonet [27] where DNA is partially adsorbed on soil having a part (‘‘train’’) interacting with the soil particles and a remaining moiety (‘‘tail’’) not involved in the interaction. Some aspects of this work which relate to the effect of differing molecular masses of DNA and their adsorption to clays still remain controversial [28]. In claynucleic acid complexes, the nucleic acid is adsorbed on the surface of the clay minerals through binding of the substrate by electrostatic and/or hydrogen bonds [29,30]. The importance of the lengths and shape of DNA molecules affects the adsorption on minerals [31]. In the adsorption process, the DNA likely changes its configuration to have a more compact length and shape to allow better adsorption on clay. In practical applications, clays can incorporate the DNA molecules to provide a remedial for the gene therapy of leukemia [32], carriers for the gastrointestinal release of selected cationic drugs [33], and chemotherapeutic treatment of colorectal cancer [34]. In particular, the stability and conformational integrity of nucleic acids are largely controlled by the interactions with surrounding water molecules [35–37]. Previous studies using X-ray diffraction and infrared and ultraviolet spectroscopy have shown that hydration by water is necessary for maintaining the structural integrity of the DNA molecule [38–41]. The interactions of water molecules with thymine and uracil have been studied experimentally and using the computational methods ([42–52] and references therein). Water forms two hydrogen bonds with uracil [48]. Hydration involving the oxygen of uracil was found to be energetically more favorable than hydration involving nitrogen [42,49]. Moreover, all uracil + nwH2O com-
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plexes displayed a planar geometry of uracil [44]. In theoretical study of van Mourik et al. [46] four uracil–water minima were found. Depending on the nature of the tautomers these complexes have cyclic or open structures [45]. The experiment performed using resonantly enhanced multiphoton ionization (REMPI) and laser-induced fluorescence (LIF) spectroscopy revealed that water stabilizes the photochemical behavior of thymine and uracil [52]. Several theoretical works were devoted to study tautomerism of uracil [53] and thymine base pair [54]. To better understand the interactions between DNA and clay minerals the adsorption of thymine and uracil on the surface of dickite has been investigated with an emphasis on the stability of the bases and effect of water. This study can bring more insight into the adsorption and bonding of nucleic acids on the clay mineral systems. 2. Computational details The study of the adsorption of thymine and uracil on the tetrahedral and octahedral surface of dickite was performed using the density functional theory with the Becke’s three parameter exchange functional [55] along with the Lee–Yang–Parr nonlocal correlation functional (B3LYP) [56,57]. The 6-31G(d) basis sets was applied [58].The Gaussian03 program package [59] was used in this study. The representative cluster models of the tetrahedral and octahedral surface of dickite were constructed using its structural data [60]. The model of dickite mimicking the adsorption on the tetrahedral surface consists of one tetrahedral ring of dickite. The model used for the adsorption on the octahedral surface consists of one octahedral ring. The dangling bonds of the mineral fragment of dickite were saturated by the hydrogen atoms. Such a model of the mineral is electroneutral. Since hydration of nucleic acid bases plays important role in structural and biological processes thymine and uracil were adsorbed on both, non-hydrated and hydrated (by one water molecule), surface of dickite. In the hydrated systems water was also optimized. The geometry of the tetrahedral mineral fragment was kept frozen while uracil/ thymine was optimized. The target molecule and six hydrogen atoms of the surface hydroxyl bases were allowed to relax in the case of the adsorption on the octahedral surface. Uracil and thymine were placed above the ring in several different initial positions to investigate the most advantageous orientation. The following notations will be used within the manuscript: D(t)–TH for thymine adsorbed on the non-hydrated tetrahedral surface, D(t)–U for uracil adsorbed on the nonhydrated tetrahedral surface, D(o)–TH for thymine adsorbed on the non-hydrated octahedral surface, and D(o)–U for uracil adsorbed on the non-hydrated octahedral surface. For the hydrated octahedral and tetrahedral surfaces the previously mentioned notations will be used with added ‘‘w’’ letter, i.e. D(t)w–TH, D(t)w–U, D(o)w– TH, and D(o)w–U.
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The interaction energies of studied systems were calculated as the difference between the total energy of a whole system and the energies of subsystems (uracil, thymine and the mineral fragment). According to review concerning the complexes at surface sites [61] the stability of results with respect to the superposition of the orbitals must always be checked by Boys and Bernardi method [62]. Therefore, the interaction energies of the studied systems were corrected by the basis set superposition error (BSSE). The topological characteristics of the electron density distribution were obtained following Bader’s ‘‘Atoms in Molecules’’ approach (AIM) [63]. The geometric parameter of nucleic acid bases, most affected by the adsorption were studied by comparison of the structural characteristics of the isolated and adsorbed target molecule. Applying this technique also changes in the electrostatic potential charges of thymine and uracil caused by the adsorption were analyzed. Electrostatic potential was suggested to be an appropriate indicator of how transferable an atom or functional group is between two or more molecules [64]. The ESP charges were determined using a Grid based method (CHELPG) introduced by Breneman and Wiberg [65] as implemented in Gaussian03 program package [59]. 3. Results and discussion We have found various possible locations and orientations of thymine and uracil on tetrahedral and octahedral surfaces of dickite in the hydrated and non-hydrated environments. These bases are adsorbed on the surfaces of dickite mostly through hydrogen bonds of several different types. This finding is in agreement with the results of experimental studies of clay–nucleic acid complexes [29,30]. The optimized structures of thymine or uracil on the nonhydrated or hydrated tetrahedral and octahedral surface of dickite are presented in Figs. 1–8.
Fig. 2. Two views of the optimized structure of thymine adsorbed on a non-hydrated tetrahedral surface of dickite (D(t)–TH) obtained at the B3LYP/6-31G(d) level of theory.
3.1. Interactions 3.1.1. Tetrahedral mineral fragments The topological characteristics of formed hydrogen bonds between the target molecule and the tetrahedral mineral fragment of dickite are given in Table 1. In the D(t)–TH system (Fig. 2) the AIM analysis reveals the formation of
Fig. 1. Optimized structure of isolated thymine (a) and uracil (b) obtained at the B3LYP/6-31G(d) level of theory.
Fig. 3. Two views of the optimized structure of thymine adsorbed on a hydrated tetrahedral surface of dickite (D(t)w–TH) obtained at the B3LYP/6-31G(d) level of theory.
T.L. Robinson et al. / Journal of Molecular Structure 844–845 (2007) 48–58
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Fig. 5. Two views of the optimized structure of uracil adsorbed on a hydrated tetrahedral surface of dickite (D(t)w–U) obtained at the B3LYP/ 6-31G(d) level of theory. Fig. 4. Two views of the optimized structure of uracil adsorbed on a nonhydrated tetrahedral surface of dickite (D(t)–U) obtained at the B3LYP/631G(d) level of theory.
one hydrogen bond of N–H O type (denoted as HB1 in Table 1 and Fig. 1) between the surface oxygen atoms of the dickite surface and the N1–H amino group of thymine. ˚ . One can see The O H bond length amounts to 2.256 A that this hydrogen bond is weaker than a typical O–H O hydrogen bond. Small values of the electron density (q) and the Laplacian of the electron density ($2q) correspond to the weak bond strength. The intermolecular interactions govern the orientation of the target molecule which is almost perpendicular towards the surface in this system. Upon the addition of one water molecule in the D(t)w–TH (Fig. 3) system , the intermolecular interactions and consequently the orientation of thymine are changed. One hydrogen bond (HB1) is formed between oxygen of the water molecule and thymine’s N3–H group. Second H-bond (HB2) is created between the O4 atom of thymine and the hydroxyl group of water. Since the rest of the molecule adopts the conformation that facilitates the interactions with the surface the orientation of thymine was changed to parallel. The water molecule forms a hydrogen bond with the surface oxygen atom of the tetrahedral mineral fragment. The strongest hydrogen bonds occur in this D(t)w–TH system which are character˚ and the q values of ized by the H O distance of 1.94 A
0.028 and 0.03 e/a.u.3 (the Laplacian values amount to 0.085 and 0.087 e/a.u.5) as shown in Table 1. The D(t)–U and D(t)w–U systems (see Figs. 4 and 5) show the same trend in the intermolecular binding comparing the tetrahedral system containing thymine (two Hbonds are formed in the system with water in which the N3–H and O4 fragments of uracil are involved and one in the system with a non-hydrated mineral fragment (involving the N1–H group)). Moreover, they are characterized by similar distances and topological characteristics as was found for the system with thymine. Thymine and uracil form the same type of H-bonds with water in our studied complexes as was revealed in the theoretical study of the isolated complex of uracil with water [48]. For isolated complex of thymine and uracil with water the hydration on O4 was found to be more favorable [42,49]. However, in our systems the formed H-bonds are similarly strong implying that the tetrahedral mineral surface affects the strength of the interactions between the nucleic acid bases and water. Additional calculations of the D(t)–TH and D(t)–U systems were performed at the B3LYP/6-31++G(d,p) level of theory. The results show the same hydrogen bonding pattern as it was found at the B3LYP/6-31G(d) level of theory. H-bonds are characterized by slightly larger distances ˚ ) and lower values of the electron density (about 0.1 A (about 0.003 and 0.004 e/a.u.3) and the Laplacian of the electron density (about 0.003 e/a.u.5). Since the main aim
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T.L. Robinson et al. / Journal of Molecular Structure 844–845 (2007) 48–58
Fig. 7. Two views of the optimized structure of uracil adsorbed on a nonhydrated octahedral surface of dickite (D(o)–UR) obtained at the B3LYP/ 6-31G(d) level of theory. Fig. 6. Two views of the optimized structure of thymine adsorbed on a non-hydrated octahedral surface of dickite (D(o)–TH) obtained at the B3LYP/6-31G(d) level of theory.
of this work is to study the hydrogen bonding which was found to be the same using both basis sets we conclude that the smaller, 6-31G(d) basis set, is sufficient to study the intermolecular interactions in such adsorption systems. 3.1.2. Octahedral mineral fragments Figs. 6 and 7 illustrate the optimized structure of thymine and uracil adsorbed on the octahedral fragment of dickite. In the case of these complexes the number of the hydrogen bonds is increased comparing to the tetrahedral systems. This is likely due to the presence of the hydroxyl groups on the dickite surface which play a key role in the binding with small organic molecules [66]. The orientation of the target molecule is parallel towards the surface since the compound exerts to maximally overlap with the surface. In the D(o)–TH and D(o)W–TH systems the formation of five hydrogen bonds was revealed. Their H O bond ˚ , respectively. In the lengths range from 1.526 to 2.597 A D(o)–TH system one H-bond is formed between the O4 and O2 atoms of thymine and the hydroxyl groups of the mineral fragment (HB1 and HB2). Moreover, one hydrogen
bond is formed between the N1–H group (HB3) and one between the methyl and C6–H group of thymine and oxygen of the mineral fragment (HB4). In the additional hydrogen bond the hydroxyl group of the surface and the carbon of the methyl group (HB5) also participate. In the D(o)–U system the distance of the N1–H group of uracil from the surface oxygen atoms is too long to create the hydrogen bond as was predicted for the D(o)–TH system. Another difference in the binding between these two systems is the formation of the C5–H O hydrogen bond instead of C(H3) H–O one. Despite of larger number of formed hydrogen bonds in the D(o)–TH system the stronger interactions are mostly predicted in the D(o)–U complex. For the D(o)W–TH complex (see Fig. 8) the same number of the intermolecular interactions was investigated as for the non-hydrated D(o)–TH system. Two O–H O hydrogen bonds are formed between the O2 and O4 atoms of thymine and the hydroxyl group of the mineral fragment (or water). Another H-bond is created between the N1–H group of thymine and the oxygen atom of the mineral fragment. Moreover, one H-bond of the C–H O type is formed between the C6–H group of thymine and the oxygen atom of the mineral fragment. The presence of water leads to the formation of one additional H-bond between the oxygen atom of water and the N3–H group of thymine. The binding situation is the
T.L. Robinson et al. / Journal of Molecular Structure 844–845 (2007) 48–58
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same for the D(o)W–U complex (see Fig. 9) implying that the methyl group does not affect the intermolecular interactions between the target molecule and the surface. In contrary to the tetrahedral systems the octahedral surface does not affect the intermolecular interactions between thymine, uracil and water since the character, number and strength of created H-bonds are the same as was found in theoretical studies of isolated uracil and thymine interacting with water [48,42,49]. Interestingly, thymine and uracil are bounded to the octahedral mineral fragments and hydrated tetrahedral mineral fragments by their highly effective sites (N3–H groups, and O2, and O4 atoms) similarly as they are bounded in A:T and A:U base pairs [67]. These centers play a key role in the stabilization of the nucleic acid bases on the clay mineral surface. The presence of proton-donors (OH groups of the octahedral fragment or water) and proton-acceptors (oxygen atoms of the octahedral fragment or water) accounts for such an adsorption. The presence of only proton-acceptors in the case of tetrahedral systems causes that the N1–H group (proton-donor) surrounded by other proton-donors (the C–H groups) governs the intermolecular binding (the orientation of the target molecule by the N3–H group is unfavorable since this group is surrounded only by proton-acceptors which behave repulsively towards the tetrahedral surface). Experimental evidence of stronger hydrogen bonds in RNA A:U than in DNA A:T base pairs has been reported [68,69]. 3.2. Changes in geometric parameters Fig. 8. Two views of the optimized structure of thymine adsorbed on a hydrated octahedral surface of dickite (D(o)w–TH) obtained at the B3LYP/6-31G(d) level of theory.
The main geometrical features of all studied systems are presented in Tables 2 and 3. Generally, the bond lengths of
Table 1 ˚ ) and X—H...Y angles (°) and electron density characteristics q (e/au3) and Calculated B3LYP/6-31G(d) H Y and X Y (in parentheses) distances (A 2 5 $ q (e/au ) H Y (X Y)
X–H Y
q
$2q
H Y (X Y)
174.0 –
0.013623 –
0.044342 –
1.943 (2.826) 1.944 (2.836)
D(t)–TH HB1 HB2
2.256 (3.266) –
2.315 (3.324) –
1.717 1.942 2.308 2.597 2.238
(2.671) (2.814) (3.201) (3.089) (3.188)
173.5 –
0.012022 –
0.040263 –
1.676 2.193 – 2.973 2.179
(2.612) (3.145) (3.157) (3.055)
148.5 143.2
0.028468 0.030139
0.085066 0.086666
1.948 (2.828) 1.936 (2.829)
148.1 143.3
0.028166 0.030674
0.084055 0.088160
159.3 159.2 156.2 131.2 113.9
0.039510 0.038997 0.0664101 0.013103 0.016074
0.115736 0.114656 0.189244 0.043656 0.064250
157.4 162.1 158.4 129.7 113.9
0.033303 0.069656 0.041854 0.011535 0.015864
0.097080 0.195016 0.123007 0.046139 0.062716
D(o)w–TH 158.1 148.8 145.1 106.8 172.9
0.042008 0.025348 0.013117 0.009190 0.014693
0.124199 0.086811 0.040986 0.035118 0.063514
D(o)–U HB1 HB2 HB3 HB4 HB5
$2q
D(t)w–U
D(o)–TH HB1 HB2 HB3 HB4 HB5
q
D(t)w–TH
D(t)–U HB1 HB2
X–H Y
1.776 1.526 1.797 2.354 2.226
(2.732) (2.487) (2.781) (3.175) (2.797)
D(o)w–U 154.1 167.8 – 91.7 150.6
0.046337 0.014265 – 0.070223 0.019331
0.139734 0.048726 – 0.024906 0.060563
1.852 1.505 1.764 2.421 2.237
(2.795) (2.476) (2.764) (3.223) (2.808)
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T.L. Robinson et al. / Journal of Molecular Structure 844–845 (2007) 48–58
Fig. 9. Two views of the optimized structure of uracil adsorbed on a hydrated octahedral surface of dickite (D(o)w–U) obtained at the B3LYP/ 6-31G(d) level of theory.
thymine and uracil were not modified by the adsorption on the tetrahedral surface but the adsorption on the octahedral surface leads to more significant changes. The largest
changes were found for the D(o)w–TH and D(o)w–U complexes in which the strongest intermolecular interactions are revealed. The N1–C2 bond length is decreased about ˚ and the N1–H bond length is increased about 0.03 A ˚ comparing the isolated thymine and uracil. The dif0.03 A ference in these bond lengths for the D(o)w–U system is ˚ , respectively. Changes of bond lengths in the 0.035 A non-hydrated octahedral systems are less significant than previously discussed modification. However, they still remain larger than the changes in bond distances of the tetrahedral systems. The formation of weak intermolecular interactions between thymine, uracil and the mineral surface results in small changes in angles of adsorbed thymine and uracil comparing to the isolated target molecule. The changes in the octahedral systems are not significant but they are larger than in the systems with the tetrahedral fragment. For example, the N1–C2–O2, N1–C2–N3, and C2–N3–C4 angles in the D(o)w–U system are changed about 3° in comparison with the isolated uracil. On the other hand, a significant change of the C2–N3–C4–O4 dihedral angle (about 30°) was revealed in the D(o)–TH, D(o)w–TH, D(o)–U, and D(o)w–U systems. It means that the interactions of thymine and uracil with the non-hydrated and hydrated octahedral mineral fragment largely affect planarity of the target molecule. Uracil–water complexes were found to be also non-planar [48] but the change of dihedral angles is much less than in our systems. 3.3. Changes in atomic charges Tables 4 and 5 present the ESP charges of the adsorbed and isolated thymine and uracil. The results obtained from comparison of these atomic charges allow us to estimate
Table 2 Geometric parameters of isolated thymine (TH) and thymine adsorbed on the tetrahedral and octahedral surface of dickite obtained at the B3LYP/631G(d) level of theory System/parametersa
D(t)–TH
D(t)w–TH
D(N1–C2) D(N1–H) D(C2@O) D(C2–N3) D(N3–C4) D(C4@O4) D(C4–C5) D(C5–C(–H3))b a(N1–C2–O2) a(N1–C2–N3) a(C2–N3–C4) a(N3–C4–O4) a(N3–C4–C5) a(C4–C5–C(–H3))b c(N1–C2–O2–N3) c(C2–N3–C4–O4) c(N3–C4–O4–C5)
1.386 1.013 1.219 1.388 1.408 1.224 1.464 1.502 123.8 112.4 128.4 120.2 114.3 118.1 179.9 179.6 179.9
1.393 1.012 1.218 1.386 1.396 1.236 1.461 1.502 122.9 112.8 127.3 120.5 115.7 118.4 179.5 174.9 179.4
a b
˚ and angles (a) and dihedral angles (c) are in degrees. Bond lengths (D) are in A Average value.
D(o)–TH 1.378 1.024 1.223 1.391 1.393 1.249 1.449 1.513 125.9 112.6 126.3 118.3 114.3 121.1 178.8 151.3 178.04
D(o)W–TH 1.357 1.040 1.253 1.369 1.405 1.239 1.446 1.502 125.3 114.7 125.7 118.2 114.9 118.8 179.5 157.8 176.1
TH 1.390 1.010 1.217 1.386 1.408 1.222 1.468 1.501 123.2 112.4 128.3 120.4 114.5 117.8 179.9 179.9 179.9
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Table 3 Geometric parameters of isolated uracil (u) and uracil adsorbed on the tetrahedral and octahedral surface of dickite obtained at the B3LYP/6-31G(d) level of theory System/parametersa
D(t)–U
D(N1–C2) D(N1–H) D(C2@O) D(C2–N3) D(N3–C4) D(C4@O4) D(C4–C5) D(C5–C6) a(N1–C2–O2) a(N1–C2–N3) a(C2–N3–C4) a(N3–C4–O4) a(N3–C4–C5) a(C4-C5-C6) c(N1–C2–O2–N3) c(C2–N3–C4–O4) c(N3–C4–O4–C5) a
1.391 1.013 1.218 1.387 1.413 1.222 1.456 1.353 123.3 112.8 128.4 120.1 113.2 120.0 179.7 179.6 180.0
D(t)w–U
D(o)–U
D(o)W–U
1.398 1.011 1.217 1.384 1.400 1.234 1.453 1.352 122.4 113.2 127.3 120.5 114.6 119.4 179.6 174.6 179.3
1.388 1.018 1.214 1.401 1.388 1.250 1.441 1.362 124.9 113.0 125.9 119.3 113.6 118.4 179.7 154.0 179.5
1.361 1.044 1.250 1.368 1.410 1.234 1.441 1.357 124.9 115.2 125.5 118.4 113.4 118.6 179.8 155.6 176.1
U 1.396 1.010 1.216 1.385 1.414 1.219 1.460 1.350 122.7 112.7 128.4 120.4 113.3 119.9 179.9 179.9 179.9
˚ and angles (a) and dihedral angles (c) are in degrees. Bond lengths (D) are in A
Table 4 ESP atomic charges (e) of isolated uracil (U) and uracil adsorbed on the tetrahedral and octahedral surface of dickite obtained at the B3LYP/631G(d) level of theory System N1 C2 O2 N3 C4 O4 C5 C6
D(t)–U 0.459 0.813 0.564 0.656 0.743 0.561 0.408 0.139
D(t)w–U
D(o)–U
D(o)w–U
0.658 0.825 0.548 0.613 0.809 0.606 0.401 0.139
0.549 0.831 0.534 0.663 0.833 0.625 0.504 0.319
0.520 0.881 0.660 0.637 0.786 0.569 0.469 0.279
U 0.473 0.735 0.548 0.602 0.750 0.542 0.436 0.146
the polarization of the target molecule caused by the binding with the mineral surface. One can see that for both molecules the adsorption leads to the same trend in changes of charges. The largest changes were found for the D(o)–TH and D(o)–U systems for the N3, C4, O4, C5, and C6 atoms. The modification is more significant in the system containing thymine than uracil. For example, the charge of the C4 atom in the D(o)–TH complex Table 5 ESP atomic charges (e) of isolated thymine (TH) and thymine adsorbed on the tetrahedral and octahedral surface of dickite obtained at the B3LYP/631G(d) level of theory System N1 C2 O2 N3 C4 O4 C5 C6
D(t)–TH 0.535 0.814 0.579 0.681 0.651 0.524 0.077 0.115
D(t)W–TH 0.627 0.785 0.543 0.581 0.679 0.568 0.041 0.020
D(o)–TH 0.483 0.815 0.577 0.659 0.745 0.604 0.269 0.158
D(o)W–TH 0.525 0.898 0.670 0.679 0.725 0.547 0.190 0.155
TH 0.453 0.707 0.546 0.578 0.629 0.513 0.079 0.014
decreased about 0.116e and for the O4 atom the charge 0.09e. increased due to the adsorption. In the D(o)w–TH and D(o)–U systems the changes were found to be the largest for the C2 and N3 atoms which are the most significant among all changes (the charge of the C2 atom increased about 0.190e in the D(o)W–TH system and about 0.15e in the D(o)w–U system). In the D(t)w–TH and D(t)w–U complexes only the charge of the N1 atom was changed significantly since only the N1–H group of the target molecule is involved in the hydrogen binding with the surface. One can see that the adsorption on the octahedral fragment causes larger changes in charges than the adsorption on the tetrahedral surface. The presence of water on the mineral surfaces increases the variations of the atomic charges. 3.4. Energetics One can see that for very weak interacting systems the BSSE values are quite large. The same situation occurs in several other theoretical studies of adsorption systems containing clay mineral or metal oxide fragments [70–72]. It can be caused by using of relatively small basis se in the calculations of such systems. It was confirmed by calculations of the interaction energy and the BSSE energy at the B3LYP/6-31++G(d,p) level. The BSSE value decreased about two times for the D(t)–TH system and about three times for the D(t)–U complex. However, such a decrease did not affect the trend in the stability of the studied systems and did not change the fact that these two systems remain the least stable among all studied complexes. Therefore, we have selected a level of theory that provides a compromise between the time of calculation and the used basis set with respect to characteristics applied for studies of large systems. As it
56
T.L. Robinson et al. / Journal of Molecular Structure 844–845 (2007) 48–58
Table 6 BSSE corrected interaction energies (kcal/mol) of thymine systems calculated at the B3LYP/6-31G(d) and B3LYP/6-31++G(d,p) levels of theory System/E
D(t)–TH 6-31G(d)
Eint EBSSE Ecorr
7.7 6.3 1.4
6-31++G(d,p) 6.1 2.0 4.1
D(t)w–TH
D(o)–TH
D(o)w–TH
6-31G(d)
6-31G(d)
6-31G(d)
17.4 9.2 8.2
39.5 18.4 21.1
55.2 9.5 45.7
Table 7 BSSE corrected interaction energies (kcal/mol) of uracil systems calculated at the B3LYP/6-31G(d) and B3LYP/6-31++G(d,p) levels of theory System/E
D(t)–U 6-31G(d)
Eint EBSSE Ecorr
7.4 3.8 3.6
6-31++G(d,p) 5.8 1.6 4.2
was discussed above the results of the AIM analysis obtained using larger basis set did not show any significant differences in intermolecular interactions comparing the results obtained using the 6-31G(d) basis set. Based on this conclusion and our results the 6-31G(d) basis set was chosen as sufficient to study the interaction energies of the thymine and uracil adsorption systems despite large values of BSSE for weakly interacting systems. The calculated interaction energies of the studied systems with thymine and uracil are presented in Tables 6 and 7. BSSE was taken into account by applying the counterpoise correction [62]. The interaction energy values of the systems with the tetrahedral fragment are very small because of the formation of only one weak hydrogen bond. The interaction energies amount to 1.4 and 3.5 kcal/ mol for the D(t)–TH and D(t)–U complexes and to 8.2 and 8.5 kcal/mol for the D(t)w–H and D(t)w–U systems. Generally, uracil is better stabilized on the clay mineral surface than thymine. The interaction energy is larger about 9 and 2 kcal/mol for the D(o)–U and D(o)w–U systems than for the D(o)–TH and D(o)w–TH systems. In experimental work Vakonakis and LiWang [68] have concluded that the RNA A:U base pair is about 0.08 kcal/mol more strongly bound than the DNA A:T base pair (the interaction energy of adenine:thymine base pair obtained at the DFT and MP2 level amounts to 12.6 and 11.7 kcal/mol [67]). Similar results concerning stronger interactions for the complexes formed by uracil than thymine were reported by Fonesca et al. [69] and by Swart et al. [73]. Our work shows that the interactions of these two nucleic acid bases with mineral fragments lead to much larger differences in the binding energies. It implies a significant impact of the clay mineral surface on the energetics of nucleic acid bases. Moreover, comparison of the interaction energy values reveals that the target molecule is better stabilized on the mineral surfaces than in the isolated base pairs. The presence of water almost double the interaction energy of the systems with thymine adsorbed on the clay mineral surface. Increase in the interaction energy upon the hydration is shown also for the systems containing ura-
D(t)w–U
D(o)–U
D(o)w–U
6-31G(d)
6-31G(d)
6-31G(d)
17.4 8.8 8.6
36.2 5.9 30.3
52.1 4.3 47.8
cil adsorbed on octahedral mineral fragment. Such an influence suggests a significant role of water in the intermolecular interactions of the nucleic acids with the clay mineral fragments. Thymine and uracil were found to be the most favorable adsorbed on the hydrated octahedral surface. The interaction energies of these two D(o)w–TH and D(o)w–U systems amount to 45.7 and 47.8 kcal/mol. 4. Conclusions The adsorption of thymine and uracil on hydrated and non-hydrated tetrahedral and octahedral surface of dickite was calculated using the B3LYP/6-31G(d) level of theory. Thymine and uracil are adsorbed in a very similar way on the surface of dickite implying that the methyl group does not influence the intermolecular interactions between the nucleic base and the mineral fragment. The most important component of the interactions is due to the formation of hydrogen bond of O–H O, N–H O, and C– H O type with the mineral fragment. In most cases thymine and uracil are oriented in the same way towards the mineral surface (an exception is the D(t)w–U system where uracil is parallel towards the surface while thymine is oriented almost perpendicularly). The tetrahedral systems are characterized by the same number of the intermolecular interactions. The octahedral complex with thymine forms larger number of the hydrogen bonds than the octahedral systems with uracil. The adsorption leads to the changes of the geometrical parameters and the atomic charges of thymine and uracil. The largest geometrical changes were found for the D(o)w–TH and D(o)w–U systems and they are more significant for the systems with uracil. The changes of charges were found to be the largest for the D(o)–TH and D(o)w–TH and D(o)–U and D(o)w–U systems. The changes are more significant for the systems containing thymine. The adsorption on the octahedral mineral surface leads to the non-planarity of thymine and uracil. Thymine and uracil are the most preferably adsorbed on the hydrated octahedral surface of clay minerals. The pres-
T.L. Robinson et al. / Journal of Molecular Structure 844–845 (2007) 48–58
ence of water plays an important role in the stabilization of the target molecule on the surface. The D(o)w–TH and D(o)w–U systems characterized by 45.7 and 47.8 kcal/ mol interaction energies were found the most stable.
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Acknowledgments [30]
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Journal of Molecular Structure 844–845 (2007) 48–58 www.elsevier.com/locate/molstruc
Hydrogen bonding of thymine and uracil with surface of dickite: An ab initio study q T.L. Robinson a, A. Michalkova a, L. Gorb b, J. Leszczynski a
a,*
Computational Center for Molecular Structure and Interactions, Department of Chemistry, Jackson State University, 1400 J.R. Lynch Street, P.O. Box 17910, Jackson, MS 39217, USA b US Army Engineer Research and Development Center (ERDC), Vicksburg, MS 39180, USA Received 5 February 2007; received in revised form 28 February 2007; accepted 1 March 2007 Available online 12 March 2007
Abstract The density functional theory (DFT) by means of the B3LYP functional and the 6-31G(d) basis set has been applied to analyze the hydrogen boding of selected nucleic acid bases (thymine and uracil) with the representative cluster models of the clay mineral, dickite. The results obtained from this investigation reveal that the formation of hydrogen bonds accounts for the stabilization of thymine and uracil on the mineral surface. The intermolecular distances and strength of the hydrogen bonds depend on the type of the surface (tetrahedral or octahedral) and on the hydration of the surface. Generally, thymine and uracil are less stable on the tetrahedral surface than on the octahedral surface. The most energetically favorable adsorption is predicted in the case of the system containing hydrated octahedral mineral fragment. The adsorption of thymine on the surface of dickite results in changes in geometry and polarization of thymine. These effects are more significant in the case of the octahedral adsorption than for the tetrahedral adsorption. Ó 2007 Elsevier B.V. All rights reserved. Keywords: Thymine; Uracil; Hydrogen bonding; Adsorption; Clay
1. Introduction Mineral surfaces have been suggested as providing substrates for support of the catalytic assembly of organic and biochemical molecules [1]. Specifically, clay minerals with their charged aluminosilicate layered structure were assumed to have the appropriate characteristics to harbor precursor organic molecules for the synthesis of important biomolecules. Many authors have suggested the involvement of surface chemistry on clays and other minerals in the prebiotic chemical evolution that culminated in the origin of life [2]. It was predicted that clay minerals could have bound the organic molecules from the surrounding water, concentrating them many times and acting as naturally q The authors dedicate this manuscript to Prof. Lucjan Sobczyk in appreciation of his fundamental work on hydrogen bonding. * Corresponding author. Tel.: +1 601 9793482; fax: +1 601 9797823. E-mail address: [email protected] (J. Leszczynski).
0022-2860/$ - see front matter Ó 2007 Elsevier B.V. All rights reserved. doi:10.1016/j.molstruc.2007.03.002
occurring environment for polymerization of large molecules, including self-replicating informational molecules [3–8]. This theory was supported by other studies (for review see Ref. [9]) where it was found that the genetic material retains its integrity and functionality upon interaction with clays while maintaining their biological activity. Moreover, since clays exist everywhere it is highly likely that they were important in protecting materials from degradation by adsorption on active sites [10]. Clays belong to the phyllosilicates group composed of two-dimensional structures. Phyllosilicates are aluminum silicates that form tetrahedral (fourfold coordination) and octahedral (sixfold coordination) sheets according to a cation and anion ratio [11,12]. The cations in a tetrahedral coordination include mostly Si4+. Substitution of Si4+ by Al3+ often occurs in the tetrahedral sheets and substitution of Al3+ by Si4+ or Mg2+ can occur in the octahedral sheets. Clays primarily exist as very small particles (2 lm in diameter) with a high specific surface area and a high
T.L. Robinson et al. / Journal of Molecular Structure 844–845 (2007) 48–58
chemical surface activity [13]. They are found in soil, lending to their importance in agriculture and the environment. Their structural diversities provide the functionality that is expected to give rise to important properties such as adsorption of ions and molecules. Minerals of the kaolinite group have 1:1 dioctahedral structure with the common chemical formula Al2Si2O5(OH)4 [14]. Dickite (a member of this group) differs from kaolinite in the layer stacking. The unit cell of dickite consists of two kaolinite layers and is twice as large as the unit cell of kaolinite. The layers are kept together by the hydrogen bridges between surface hydroxyl groups of the octahedral side and the basal oxygen atoms of the tetrahedral side [15]. Specifically, the nucleic acid adsorption on clay minerals was investigated as early as 1952 by Goring and Bartholomew [16]. Since then in several works DNA/RNA adsorption on clay minerals has been studied [17]. Ferris et al. [18] demonstrated the polymerization of oligonucleotides on clay. Nucleic acids adsorbed and bound on clay minerals are partially protected against degradation by nucleases and other degradative enzymes [19–25]. Two hypotheses have been suggested to describe the adsorption and binding of nucleic acids onto clays. According to Khanna et al. [26] one end of DNA is bound to the edges of the clay with a fraction of the DNA bound on the planar surface. Another model of the DNA–clay complexes has been described by Paget and Simonet [27] where DNA is partially adsorbed on soil having a part (‘‘train’’) interacting with the soil particles and a remaining moiety (‘‘tail’’) not involved in the interaction. Some aspects of this work which relate to the effect of differing molecular masses of DNA and their adsorption to clays still remain controversial [28]. In claynucleic acid complexes, the nucleic acid is adsorbed on the surface of the clay minerals through binding of the substrate by electrostatic and/or hydrogen bonds [29,30]. The importance of the lengths and shape of DNA molecules affects the adsorption on minerals [31]. In the adsorption process, the DNA likely changes its configuration to have a more compact length and shape to allow better adsorption on clay. In practical applications, clays can incorporate the DNA molecules to provide a remedial for the gene therapy of leukemia [32], carriers for the gastrointestinal release of selected cationic drugs [33], and chemotherapeutic treatment of colorectal cancer [34]. In particular, the stability and conformational integrity of nucleic acids are largely controlled by the interactions with surrounding water molecules [35–37]. Previous studies using X-ray diffraction and infrared and ultraviolet spectroscopy have shown that hydration by water is necessary for maintaining the structural integrity of the DNA molecule [38–41]. The interactions of water molecules with thymine and uracil have been studied experimentally and using the computational methods ([42–52] and references therein). Water forms two hydrogen bonds with uracil [48]. Hydration involving the oxygen of uracil was found to be energetically more favorable than hydration involving nitrogen [42,49]. Moreover, all uracil + nwH2O com-
49
plexes displayed a planar geometry of uracil [44]. In theoretical study of van Mourik et al. [46] four uracil–water minima were found. Depending on the nature of the tautomers these complexes have cyclic or open structures [45]. The experiment performed using resonantly enhanced multiphoton ionization (REMPI) and laser-induced fluorescence (LIF) spectroscopy revealed that water stabilizes the photochemical behavior of thymine and uracil [52]. Several theoretical works were devoted to study tautomerism of uracil [53] and thymine base pair [54]. To better understand the interactions between DNA and clay minerals the adsorption of thymine and uracil on the surface of dickite has been investigated with an emphasis on the stability of the bases and effect of water. This study can bring more insight into the adsorption and bonding of nucleic acids on the clay mineral systems. 2. Computational details The study of the adsorption of thymine and uracil on the tetrahedral and octahedral surface of dickite was performed using the density functional theory with the Becke’s three parameter exchange functional [55] along with the Lee–Yang–Parr nonlocal correlation functional (B3LYP) [56,57]. The 6-31G(d) basis sets was applied [58].The Gaussian03 program package [59] was used in this study. The representative cluster models of the tetrahedral and octahedral surface of dickite were constructed using its structural data [60]. The model of dickite mimicking the adsorption on the tetrahedral surface consists of one tetrahedral ring of dickite. The model used for the adsorption on the octahedral surface consists of one octahedral ring. The dangling bonds of the mineral fragment of dickite were saturated by the hydrogen atoms. Such a model of the mineral is electroneutral. Since hydration of nucleic acid bases plays important role in structural and biological processes thymine and uracil were adsorbed on both, non-hydrated and hydrated (by one water molecule), surface of dickite. In the hydrated systems water was also optimized. The geometry of the tetrahedral mineral fragment was kept frozen while uracil/ thymine was optimized. The target molecule and six hydrogen atoms of the surface hydroxyl bases were allowed to relax in the case of the adsorption on the octahedral surface. Uracil and thymine were placed above the ring in several different initial positions to investigate the most advantageous orientation. The following notations will be used within the manuscript: D(t)–TH for thymine adsorbed on the non-hydrated tetrahedral surface, D(t)–U for uracil adsorbed on the nonhydrated tetrahedral surface, D(o)–TH for thymine adsorbed on the non-hydrated octahedral surface, and D(o)–U for uracil adsorbed on the non-hydrated octahedral surface. For the hydrated octahedral and tetrahedral surfaces the previously mentioned notations will be used with added ‘‘w’’ letter, i.e. D(t)w–TH, D(t)w–U, D(o)w– TH, and D(o)w–U.
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T.L. Robinson et al. / Journal of Molecular Structure 844–845 (2007) 48–58
The interaction energies of studied systems were calculated as the difference between the total energy of a whole system and the energies of subsystems (uracil, thymine and the mineral fragment). According to review concerning the complexes at surface sites [61] the stability of results with respect to the superposition of the orbitals must always be checked by Boys and Bernardi method [62]. Therefore, the interaction energies of the studied systems were corrected by the basis set superposition error (BSSE). The topological characteristics of the electron density distribution were obtained following Bader’s ‘‘Atoms in Molecules’’ approach (AIM) [63]. The geometric parameter of nucleic acid bases, most affected by the adsorption were studied by comparison of the structural characteristics of the isolated and adsorbed target molecule. Applying this technique also changes in the electrostatic potential charges of thymine and uracil caused by the adsorption were analyzed. Electrostatic potential was suggested to be an appropriate indicator of how transferable an atom or functional group is between two or more molecules [64]. The ESP charges were determined using a Grid based method (CHELPG) introduced by Breneman and Wiberg [65] as implemented in Gaussian03 program package [59]. 3. Results and discussion We have found various possible locations and orientations of thymine and uracil on tetrahedral and octahedral surfaces of dickite in the hydrated and non-hydrated environments. These bases are adsorbed on the surfaces of dickite mostly through hydrogen bonds of several different types. This finding is in agreement with the results of experimental studies of clay–nucleic acid complexes [29,30]. The optimized structures of thymine or uracil on the nonhydrated or hydrated tetrahedral and octahedral surface of dickite are presented in Figs. 1–8.
Fig. 2. Two views of the optimized structure of thymine adsorbed on a non-hydrated tetrahedral surface of dickite (D(t)–TH) obtained at the B3LYP/6-31G(d) level of theory.
3.1. Interactions 3.1.1. Tetrahedral mineral fragments The topological characteristics of formed hydrogen bonds between the target molecule and the tetrahedral mineral fragment of dickite are given in Table 1. In the D(t)–TH system (Fig. 2) the AIM analysis reveals the formation of
Fig. 1. Optimized structure of isolated thymine (a) and uracil (b) obtained at the B3LYP/6-31G(d) level of theory.
Fig. 3. Two views of the optimized structure of thymine adsorbed on a hydrated tetrahedral surface of dickite (D(t)w–TH) obtained at the B3LYP/6-31G(d) level of theory.
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Fig. 5. Two views of the optimized structure of uracil adsorbed on a hydrated tetrahedral surface of dickite (D(t)w–U) obtained at the B3LYP/ 6-31G(d) level of theory. Fig. 4. Two views of the optimized structure of uracil adsorbed on a nonhydrated tetrahedral surface of dickite (D(t)–U) obtained at the B3LYP/631G(d) level of theory.
one hydrogen bond of N–H O type (denoted as HB1 in Table 1 and Fig. 1) between the surface oxygen atoms of the dickite surface and the N1–H amino group of thymine. ˚ . One can see The O H bond length amounts to 2.256 A that this hydrogen bond is weaker than a typical O–H O hydrogen bond. Small values of the electron density (q) and the Laplacian of the electron density ($2q) correspond to the weak bond strength. The intermolecular interactions govern the orientation of the target molecule which is almost perpendicular towards the surface in this system. Upon the addition of one water molecule in the D(t)w–TH (Fig. 3) system , the intermolecular interactions and consequently the orientation of thymine are changed. One hydrogen bond (HB1) is formed between oxygen of the water molecule and thymine’s N3–H group. Second H-bond (HB2) is created between the O4 atom of thymine and the hydroxyl group of water. Since the rest of the molecule adopts the conformation that facilitates the interactions with the surface the orientation of thymine was changed to parallel. The water molecule forms a hydrogen bond with the surface oxygen atom of the tetrahedral mineral fragment. The strongest hydrogen bonds occur in this D(t)w–TH system which are character˚ and the q values of ized by the H O distance of 1.94 A
0.028 and 0.03 e/a.u.3 (the Laplacian values amount to 0.085 and 0.087 e/a.u.5) as shown in Table 1. The D(t)–U and D(t)w–U systems (see Figs. 4 and 5) show the same trend in the intermolecular binding comparing the tetrahedral system containing thymine (two Hbonds are formed in the system with water in which the N3–H and O4 fragments of uracil are involved and one in the system with a non-hydrated mineral fragment (involving the N1–H group)). Moreover, they are characterized by similar distances and topological characteristics as was found for the system with thymine. Thymine and uracil form the same type of H-bonds with water in our studied complexes as was revealed in the theoretical study of the isolated complex of uracil with water [48]. For isolated complex of thymine and uracil with water the hydration on O4 was found to be more favorable [42,49]. However, in our systems the formed H-bonds are similarly strong implying that the tetrahedral mineral surface affects the strength of the interactions between the nucleic acid bases and water. Additional calculations of the D(t)–TH and D(t)–U systems were performed at the B3LYP/6-31++G(d,p) level of theory. The results show the same hydrogen bonding pattern as it was found at the B3LYP/6-31G(d) level of theory. H-bonds are characterized by slightly larger distances ˚ ) and lower values of the electron density (about 0.1 A (about 0.003 and 0.004 e/a.u.3) and the Laplacian of the electron density (about 0.003 e/a.u.5). Since the main aim
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T.L. Robinson et al. / Journal of Molecular Structure 844–845 (2007) 48–58
Fig. 7. Two views of the optimized structure of uracil adsorbed on a nonhydrated octahedral surface of dickite (D(o)–UR) obtained at the B3LYP/ 6-31G(d) level of theory. Fig. 6. Two views of the optimized structure of thymine adsorbed on a non-hydrated octahedral surface of dickite (D(o)–TH) obtained at the B3LYP/6-31G(d) level of theory.
of this work is to study the hydrogen bonding which was found to be the same using both basis sets we conclude that the smaller, 6-31G(d) basis set, is sufficient to study the intermolecular interactions in such adsorption systems. 3.1.2. Octahedral mineral fragments Figs. 6 and 7 illustrate the optimized structure of thymine and uracil adsorbed on the octahedral fragment of dickite. In the case of these complexes the number of the hydrogen bonds is increased comparing to the tetrahedral systems. This is likely due to the presence of the hydroxyl groups on the dickite surface which play a key role in the binding with small organic molecules [66]. The orientation of the target molecule is parallel towards the surface since the compound exerts to maximally overlap with the surface. In the D(o)–TH and D(o)W–TH systems the formation of five hydrogen bonds was revealed. Their H O bond ˚ , respectively. In the lengths range from 1.526 to 2.597 A D(o)–TH system one H-bond is formed between the O4 and O2 atoms of thymine and the hydroxyl groups of the mineral fragment (HB1 and HB2). Moreover, one hydrogen
bond is formed between the N1–H group (HB3) and one between the methyl and C6–H group of thymine and oxygen of the mineral fragment (HB4). In the additional hydrogen bond the hydroxyl group of the surface and the carbon of the methyl group (HB5) also participate. In the D(o)–U system the distance of the N1–H group of uracil from the surface oxygen atoms is too long to create the hydrogen bond as was predicted for the D(o)–TH system. Another difference in the binding between these two systems is the formation of the C5–H O hydrogen bond instead of C(H3) H–O one. Despite of larger number of formed hydrogen bonds in the D(o)–TH system the stronger interactions are mostly predicted in the D(o)–U complex. For the D(o)W–TH complex (see Fig. 8) the same number of the intermolecular interactions was investigated as for the non-hydrated D(o)–TH system. Two O–H O hydrogen bonds are formed between the O2 and O4 atoms of thymine and the hydroxyl group of the mineral fragment (or water). Another H-bond is created between the N1–H group of thymine and the oxygen atom of the mineral fragment. Moreover, one H-bond of the C–H O type is formed between the C6–H group of thymine and the oxygen atom of the mineral fragment. The presence of water leads to the formation of one additional H-bond between the oxygen atom of water and the N3–H group of thymine. The binding situation is the
T.L. Robinson et al. / Journal of Molecular Structure 844–845 (2007) 48–58
53
same for the D(o)W–U complex (see Fig. 9) implying that the methyl group does not affect the intermolecular interactions between the target molecule and the surface. In contrary to the tetrahedral systems the octahedral surface does not affect the intermolecular interactions between thymine, uracil and water since the character, number and strength of created H-bonds are the same as was found in theoretical studies of isolated uracil and thymine interacting with water [48,42,49]. Interestingly, thymine and uracil are bounded to the octahedral mineral fragments and hydrated tetrahedral mineral fragments by their highly effective sites (N3–H groups, and O2, and O4 atoms) similarly as they are bounded in A:T and A:U base pairs [67]. These centers play a key role in the stabilization of the nucleic acid bases on the clay mineral surface. The presence of proton-donors (OH groups of the octahedral fragment or water) and proton-acceptors (oxygen atoms of the octahedral fragment or water) accounts for such an adsorption. The presence of only proton-acceptors in the case of tetrahedral systems causes that the N1–H group (proton-donor) surrounded by other proton-donors (the C–H groups) governs the intermolecular binding (the orientation of the target molecule by the N3–H group is unfavorable since this group is surrounded only by proton-acceptors which behave repulsively towards the tetrahedral surface). Experimental evidence of stronger hydrogen bonds in RNA A:U than in DNA A:T base pairs has been reported [68,69]. 3.2. Changes in geometric parameters Fig. 8. Two views of the optimized structure of thymine adsorbed on a hydrated octahedral surface of dickite (D(o)w–TH) obtained at the B3LYP/6-31G(d) level of theory.
The main geometrical features of all studied systems are presented in Tables 2 and 3. Generally, the bond lengths of
Table 1 ˚ ) and X—H...Y angles (°) and electron density characteristics q (e/au3) and Calculated B3LYP/6-31G(d) H Y and X Y (in parentheses) distances (A 2 5 $ q (e/au ) H Y (X Y)
X–H Y
q
$2q
H Y (X Y)
174.0 –
0.013623 –
0.044342 –
1.943 (2.826) 1.944 (2.836)
D(t)–TH HB1 HB2
2.256 (3.266) –
2.315 (3.324) –
1.717 1.942 2.308 2.597 2.238
(2.671) (2.814) (3.201) (3.089) (3.188)
173.5 –
0.012022 –
0.040263 –
1.676 2.193 – 2.973 2.179
(2.612) (3.145) (3.157) (3.055)
148.5 143.2
0.028468 0.030139
0.085066 0.086666
1.948 (2.828) 1.936 (2.829)
148.1 143.3
0.028166 0.030674
0.084055 0.088160
159.3 159.2 156.2 131.2 113.9
0.039510 0.038997 0.0664101 0.013103 0.016074
0.115736 0.114656 0.189244 0.043656 0.064250
157.4 162.1 158.4 129.7 113.9
0.033303 0.069656 0.041854 0.011535 0.015864
0.097080 0.195016 0.123007 0.046139 0.062716
D(o)w–TH 158.1 148.8 145.1 106.8 172.9
0.042008 0.025348 0.013117 0.009190 0.014693
0.124199 0.086811 0.040986 0.035118 0.063514
D(o)–U HB1 HB2 HB3 HB4 HB5
$2q
D(t)w–U
D(o)–TH HB1 HB2 HB3 HB4 HB5
q
D(t)w–TH
D(t)–U HB1 HB2
X–H Y
1.776 1.526 1.797 2.354 2.226
(2.732) (2.487) (2.781) (3.175) (2.797)
D(o)w–U 154.1 167.8 – 91.7 150.6
0.046337 0.014265 – 0.070223 0.019331
0.139734 0.048726 – 0.024906 0.060563
1.852 1.505 1.764 2.421 2.237
(2.795) (2.476) (2.764) (3.223) (2.808)
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Fig. 9. Two views of the optimized structure of uracil adsorbed on a hydrated octahedral surface of dickite (D(o)w–U) obtained at the B3LYP/ 6-31G(d) level of theory.
thymine and uracil were not modified by the adsorption on the tetrahedral surface but the adsorption on the octahedral surface leads to more significant changes. The largest
changes were found for the D(o)w–TH and D(o)w–U complexes in which the strongest intermolecular interactions are revealed. The N1–C2 bond length is decreased about ˚ and the N1–H bond length is increased about 0.03 A ˚ comparing the isolated thymine and uracil. The dif0.03 A ference in these bond lengths for the D(o)w–U system is ˚ , respectively. Changes of bond lengths in the 0.035 A non-hydrated octahedral systems are less significant than previously discussed modification. However, they still remain larger than the changes in bond distances of the tetrahedral systems. The formation of weak intermolecular interactions between thymine, uracil and the mineral surface results in small changes in angles of adsorbed thymine and uracil comparing to the isolated target molecule. The changes in the octahedral systems are not significant but they are larger than in the systems with the tetrahedral fragment. For example, the N1–C2–O2, N1–C2–N3, and C2–N3–C4 angles in the D(o)w–U system are changed about 3° in comparison with the isolated uracil. On the other hand, a significant change of the C2–N3–C4–O4 dihedral angle (about 30°) was revealed in the D(o)–TH, D(o)w–TH, D(o)–U, and D(o)w–U systems. It means that the interactions of thymine and uracil with the non-hydrated and hydrated octahedral mineral fragment largely affect planarity of the target molecule. Uracil–water complexes were found to be also non-planar [48] but the change of dihedral angles is much less than in our systems. 3.3. Changes in atomic charges Tables 4 and 5 present the ESP charges of the adsorbed and isolated thymine and uracil. The results obtained from comparison of these atomic charges allow us to estimate
Table 2 Geometric parameters of isolated thymine (TH) and thymine adsorbed on the tetrahedral and octahedral surface of dickite obtained at the B3LYP/631G(d) level of theory System/parametersa
D(t)–TH
D(t)w–TH
D(N1–C2) D(N1–H) D(C2@O) D(C2–N3) D(N3–C4) D(C4@O4) D(C4–C5) D(C5–C(–H3))b a(N1–C2–O2) a(N1–C2–N3) a(C2–N3–C4) a(N3–C4–O4) a(N3–C4–C5) a(C4–C5–C(–H3))b c(N1–C2–O2–N3) c(C2–N3–C4–O4) c(N3–C4–O4–C5)
1.386 1.013 1.219 1.388 1.408 1.224 1.464 1.502 123.8 112.4 128.4 120.2 114.3 118.1 179.9 179.6 179.9
1.393 1.012 1.218 1.386 1.396 1.236 1.461 1.502 122.9 112.8 127.3 120.5 115.7 118.4 179.5 174.9 179.4
a b
˚ and angles (a) and dihedral angles (c) are in degrees. Bond lengths (D) are in A Average value.
D(o)–TH 1.378 1.024 1.223 1.391 1.393 1.249 1.449 1.513 125.9 112.6 126.3 118.3 114.3 121.1 178.8 151.3 178.04
D(o)W–TH 1.357 1.040 1.253 1.369 1.405 1.239 1.446 1.502 125.3 114.7 125.7 118.2 114.9 118.8 179.5 157.8 176.1
TH 1.390 1.010 1.217 1.386 1.408 1.222 1.468 1.501 123.2 112.4 128.3 120.4 114.5 117.8 179.9 179.9 179.9
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Table 3 Geometric parameters of isolated uracil (u) and uracil adsorbed on the tetrahedral and octahedral surface of dickite obtained at the B3LYP/6-31G(d) level of theory System/parametersa
D(t)–U
D(N1–C2) D(N1–H) D(C2@O) D(C2–N3) D(N3–C4) D(C4@O4) D(C4–C5) D(C5–C6) a(N1–C2–O2) a(N1–C2–N3) a(C2–N3–C4) a(N3–C4–O4) a(N3–C4–C5) a(C4-C5-C6) c(N1–C2–O2–N3) c(C2–N3–C4–O4) c(N3–C4–O4–C5) a
1.391 1.013 1.218 1.387 1.413 1.222 1.456 1.353 123.3 112.8 128.4 120.1 113.2 120.0 179.7 179.6 180.0
D(t)w–U
D(o)–U
D(o)W–U
1.398 1.011 1.217 1.384 1.400 1.234 1.453 1.352 122.4 113.2 127.3 120.5 114.6 119.4 179.6 174.6 179.3
1.388 1.018 1.214 1.401 1.388 1.250 1.441 1.362 124.9 113.0 125.9 119.3 113.6 118.4 179.7 154.0 179.5
1.361 1.044 1.250 1.368 1.410 1.234 1.441 1.357 124.9 115.2 125.5 118.4 113.4 118.6 179.8 155.6 176.1
U 1.396 1.010 1.216 1.385 1.414 1.219 1.460 1.350 122.7 112.7 128.4 120.4 113.3 119.9 179.9 179.9 179.9
˚ and angles (a) and dihedral angles (c) are in degrees. Bond lengths (D) are in A
Table 4 ESP atomic charges (e) of isolated uracil (U) and uracil adsorbed on the tetrahedral and octahedral surface of dickite obtained at the B3LYP/631G(d) level of theory System N1 C2 O2 N3 C4 O4 C5 C6
D(t)–U 0.459 0.813 0.564 0.656 0.743 0.561 0.408 0.139
D(t)w–U
D(o)–U
D(o)w–U
0.658 0.825 0.548 0.613 0.809 0.606 0.401 0.139
0.549 0.831 0.534 0.663 0.833 0.625 0.504 0.319
0.520 0.881 0.660 0.637 0.786 0.569 0.469 0.279
U 0.473 0.735 0.548 0.602 0.750 0.542 0.436 0.146
the polarization of the target molecule caused by the binding with the mineral surface. One can see that for both molecules the adsorption leads to the same trend in changes of charges. The largest changes were found for the D(o)–TH and D(o)–U systems for the N3, C4, O4, C5, and C6 atoms. The modification is more significant in the system containing thymine than uracil. For example, the charge of the C4 atom in the D(o)–TH complex Table 5 ESP atomic charges (e) of isolated thymine (TH) and thymine adsorbed on the tetrahedral and octahedral surface of dickite obtained at the B3LYP/631G(d) level of theory System N1 C2 O2 N3 C4 O4 C5 C6
D(t)–TH 0.535 0.814 0.579 0.681 0.651 0.524 0.077 0.115
D(t)W–TH 0.627 0.785 0.543 0.581 0.679 0.568 0.041 0.020
D(o)–TH 0.483 0.815 0.577 0.659 0.745 0.604 0.269 0.158
D(o)W–TH 0.525 0.898 0.670 0.679 0.725 0.547 0.190 0.155
TH 0.453 0.707 0.546 0.578 0.629 0.513 0.079 0.014
decreased about 0.116e and for the O4 atom the charge 0.09e. increased due to the adsorption. In the D(o)w–TH and D(o)–U systems the changes were found to be the largest for the C2 and N3 atoms which are the most significant among all changes (the charge of the C2 atom increased about 0.190e in the D(o)W–TH system and about 0.15e in the D(o)w–U system). In the D(t)w–TH and D(t)w–U complexes only the charge of the N1 atom was changed significantly since only the N1–H group of the target molecule is involved in the hydrogen binding with the surface. One can see that the adsorption on the octahedral fragment causes larger changes in charges than the adsorption on the tetrahedral surface. The presence of water on the mineral surfaces increases the variations of the atomic charges. 3.4. Energetics One can see that for very weak interacting systems the BSSE values are quite large. The same situation occurs in several other theoretical studies of adsorption systems containing clay mineral or metal oxide fragments [70–72]. It can be caused by using of relatively small basis se in the calculations of such systems. It was confirmed by calculations of the interaction energy and the BSSE energy at the B3LYP/6-31++G(d,p) level. The BSSE value decreased about two times for the D(t)–TH system and about three times for the D(t)–U complex. However, such a decrease did not affect the trend in the stability of the studied systems and did not change the fact that these two systems remain the least stable among all studied complexes. Therefore, we have selected a level of theory that provides a compromise between the time of calculation and the used basis set with respect to characteristics applied for studies of large systems. As it
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T.L. Robinson et al. / Journal of Molecular Structure 844–845 (2007) 48–58
Table 6 BSSE corrected interaction energies (kcal/mol) of thymine systems calculated at the B3LYP/6-31G(d) and B3LYP/6-31++G(d,p) levels of theory System/E
D(t)–TH 6-31G(d)
Eint EBSSE Ecorr
7.7 6.3 1.4
6-31++G(d,p) 6.1 2.0 4.1
D(t)w–TH
D(o)–TH
D(o)w–TH
6-31G(d)
6-31G(d)
6-31G(d)
17.4 9.2 8.2
39.5 18.4 21.1
55.2 9.5 45.7
Table 7 BSSE corrected interaction energies (kcal/mol) of uracil systems calculated at the B3LYP/6-31G(d) and B3LYP/6-31++G(d,p) levels of theory System/E
D(t)–U 6-31G(d)
Eint EBSSE Ecorr
7.4 3.8 3.6
6-31++G(d,p) 5.8 1.6 4.2
was discussed above the results of the AIM analysis obtained using larger basis set did not show any significant differences in intermolecular interactions comparing the results obtained using the 6-31G(d) basis set. Based on this conclusion and our results the 6-31G(d) basis set was chosen as sufficient to study the interaction energies of the thymine and uracil adsorption systems despite large values of BSSE for weakly interacting systems. The calculated interaction energies of the studied systems with thymine and uracil are presented in Tables 6 and 7. BSSE was taken into account by applying the counterpoise correction [62]. The interaction energy values of the systems with the tetrahedral fragment are very small because of the formation of only one weak hydrogen bond. The interaction energies amount to 1.4 and 3.5 kcal/ mol for the D(t)–TH and D(t)–U complexes and to 8.2 and 8.5 kcal/mol for the D(t)w–H and D(t)w–U systems. Generally, uracil is better stabilized on the clay mineral surface than thymine. The interaction energy is larger about 9 and 2 kcal/mol for the D(o)–U and D(o)w–U systems than for the D(o)–TH and D(o)w–TH systems. In experimental work Vakonakis and LiWang [68] have concluded that the RNA A:U base pair is about 0.08 kcal/mol more strongly bound than the DNA A:T base pair (the interaction energy of adenine:thymine base pair obtained at the DFT and MP2 level amounts to 12.6 and 11.7 kcal/mol [67]). Similar results concerning stronger interactions for the complexes formed by uracil than thymine were reported by Fonesca et al. [69] and by Swart et al. [73]. Our work shows that the interactions of these two nucleic acid bases with mineral fragments lead to much larger differences in the binding energies. It implies a significant impact of the clay mineral surface on the energetics of nucleic acid bases. Moreover, comparison of the interaction energy values reveals that the target molecule is better stabilized on the mineral surfaces than in the isolated base pairs. The presence of water almost double the interaction energy of the systems with thymine adsorbed on the clay mineral surface. Increase in the interaction energy upon the hydration is shown also for the systems containing ura-
D(t)w–U
D(o)–U
D(o)w–U
6-31G(d)
6-31G(d)
6-31G(d)
17.4 8.8 8.6
36.2 5.9 30.3
52.1 4.3 47.8
cil adsorbed on octahedral mineral fragment. Such an influence suggests a significant role of water in the intermolecular interactions of the nucleic acids with the clay mineral fragments. Thymine and uracil were found to be the most favorable adsorbed on the hydrated octahedral surface. The interaction energies of these two D(o)w–TH and D(o)w–U systems amount to 45.7 and 47.8 kcal/mol. 4. Conclusions The adsorption of thymine and uracil on hydrated and non-hydrated tetrahedral and octahedral surface of dickite was calculated using the B3LYP/6-31G(d) level of theory. Thymine and uracil are adsorbed in a very similar way on the surface of dickite implying that the methyl group does not influence the intermolecular interactions between the nucleic base and the mineral fragment. The most important component of the interactions is due to the formation of hydrogen bond of O–H O, N–H O, and C– H O type with the mineral fragment. In most cases thymine and uracil are oriented in the same way towards the mineral surface (an exception is the D(t)w–U system where uracil is parallel towards the surface while thymine is oriented almost perpendicularly). The tetrahedral systems are characterized by the same number of the intermolecular interactions. The octahedral complex with thymine forms larger number of the hydrogen bonds than the octahedral systems with uracil. The adsorption leads to the changes of the geometrical parameters and the atomic charges of thymine and uracil. The largest geometrical changes were found for the D(o)w–TH and D(o)w–U systems and they are more significant for the systems with uracil. The changes of charges were found to be the largest for the D(o)–TH and D(o)w–TH and D(o)–U and D(o)w–U systems. The changes are more significant for the systems containing thymine. The adsorption on the octahedral mineral surface leads to the non-planarity of thymine and uracil. Thymine and uracil are the most preferably adsorbed on the hydrated octahedral surface of clay minerals. The pres-
T.L. Robinson et al. / Journal of Molecular Structure 844–845 (2007) 48–58
ence of water plays an important role in the stabilization of the target molecule on the surface. The D(o)w–TH and D(o)w–U systems characterized by 45.7 and 47.8 kcal/ mol interaction energies were found the most stable.
[25] [26] [27] [28] [29]
Acknowledgments [30]
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