Tautomerization, Solvent Effect and Binding ... - ACS Publications

ARTICLE pubs.acs.org/JPCC

Tautomerization, Solvent Effect and Binding Interaction on Vibrational Spectra of Adenine Ag+ Complexes on Silver Surfaces: A DFT Study Rong Huang, Liu-Bin Zhao, De-Yin Wu,* and Zhong-Qun Tian State Key Laboratory of Physical Chemistry of Solid Surfaces and College of Chemistry and Chemical Engineering, Xiamen University, Xiamen 361005, Fujian, China

bS Supporting Information ABSTRACT: Stable structures and vibrational spectra of adenine and adenine Ag+ complexes which might exist on silver surfaces have been investigated by hybrid density functional B3LYP and ab initio MP2 methods. For adenine Ag+ complexes, considered as monomeric species, there are two stable structures (i-1H-9H-Ag7 and 7H-Ag3) in the gas phase and four stable structures (9H-Ag1, 9H-Ag3, 9H-Ag7 and 7H-Ag3) in aqueous solution calculated with a solvation model of density (SMD). Analyzing the vibrational spectra of these stable structures in the gas phase and in aqueous solution, we can find that Ag+ influences the spectra significantly and different tautomers can be distinguished from each other on the basis of characteristic bands of their vibrational spectra. Furthermore, we propose that the dimer of 7H-Ag3 should be the most stable structure in aqueous solution though 7H-Ag3 is not the most stable one in the gas phase. This is supported by the predicted Gibbs free energy of the dimerization process and experimental Raman spectra of the adenine Ag+ complex.

’ INTRODUCTION Adenine is thought to have single molecule sensitivity by surface-enhanced Raman spectroscopy (SERS)1,2 and dominates the SERS of DNA oligonucleotides.3 However, it is hard to make clear the mechanism of adenine on metal surfaces due to the complexity of SERS. On the surface of silver nanostructures used in SERS experiments, it is possible to have silver ion during the preparation of silver nanoparticles, or because of the introduction of positive potential polarization, the light radiation, the existence of oxygen and so on.4 6 People thought that, in the SERS of adenine, there might exist adenine Ag+ complexes and some abnormal SERS signals of adenine came from the interaction between adenine and Ag+ (charged Ag nanoparticles).4,7 11 Apart from the particularity in SERS, adenine is one of the most important components because it is not only an integral part of biomolecules (such as DNA, RNA, NADH and FADH) but also a part of ATP which determines the key energy releasing process.12 Meanwhile, the interaction of metal ions with biomolecules is of great importance both in chemistry and in life science. Metal ions may bind to the phosphates, sugars or the bases in nucleobases. For example, Na+, Mg2+, Al3+, Mn2+ and Fe3+ are inclined to interact with phosphates while they show weak affinity toward the bases.13 However, as a common metal ion, Ag+ can form complexes with nucleic acids and with polynucleotides specifically to the heterocyclic bases.14 Ag+ also has a strong interaction with bases in DNA while it has no affinity r 2011 American Chemical Society

toward the backbone phosphate group no matter whether at low or high concentration.15,16 Therefore, to understand the interaction between adenine and silver ion is very fascinating. At present, the interaction of adenine with Ag+ has been studied by different experimental measurements and theoretical calculations. Experimentally, potentiometric titration, precipitate analysis,15 flow linear dichroism,17,18 UV absorption,19,20 X-ray crystal diffraction,21,22 ESI/MS23,24 and Raman spectroscopy8,10,11 were used to characterize adenine Ag+ complexes. Theoretically, the reports concentrated on the relative stabilities, electronic structures, and Raman spectra of different adenine Ag+ complexes.19,20,24,25 We can summarize different experimental and theoretical studies in the literature as three points. The possible structures of adenine and adenine Ag+ complexes are given in Figure 1. First, by potentiometric titration and precipitate analysis, Gillen et al. determined for the first time that adenine lost the hydrogen of N9 and the amino group when it reacted with silver ion to form a complex consisting of 1.5 2.0 Ag+ per adenine at pH around 7 in aqueous solutions.15 Matsuoka et al. thought adenine formed linear polymers with silver ion via N1 and N9 through linear dichroism.17,18 Analysis of crystal structures of the complexes formed by adenine and silver nitrate or silver Received: March 1, 2011 Revised: June 7, 2011 Published: June 10, 2011 13739

dx.doi.org/10.1021/jp201977z | J. Phys. Chem. C 2011, 115, 13739–13750

The Journal of Physical Chemistry C

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Figure 1. Optimized structures of four adenine tautomers (N9H, N7H, N3H and i-1H-N9H), eight adenine Ag+ complexes (i-1H-9H-Ag7 and 7H-Ag3 are given in the gas phase; 9H-Ag1, 9H-Ag3, 9H-Ag7, i-3H-9H-Ag7, i-3H-9H-Ag1, 1H-Ag9 are given in aqueous solution with SMD model) and three dimers ([7H-Ag3]24+, [7H-Ag3]22+, and [7H-Ag3]2) optimized with the SMD model. Note that 9H-Ag7 denotes an Ag+ ion binding to the N7 site of the N9H tautomer and i-1H-9H-Ag7 represents a silver ion binding to the N7 and N10 sites of the i-1H-N9H imino tautomer.

perchlorate in acid solutions indicated a bidentate coordination via N3 and N9 nitrogen atoms of two adenine molecules.21,22 Second, the combined studies of UV absorption spectra with theoretical calculations were used to infer the structures of the complexes at low concentration. Rubina et al. detected a redshifted and broadened band in the UV absorption spectrum of adenine Ag+ complex in acetate buffer (pH = 6) compared to adenine itself.20 On the basis of DFT calculation, they noted that the first electronic transition energies of 9H-Ag1 and 9H-Ag7 in the gas phase red shift, in agreement with the experimental observation.20 Here 9H-Ag1 means the adenine part is an N9H adenine tautomer, and then Ag+ binds to adenine via N1. Schreiber et al. calculated the excitation energies of adenine Ag+ complexes in the gas phase and compared to the UV absorption spectra.25 They thought there were two stable tautomers, like 1H-Ag9 and 9H-Ag3. Cheng et al. considered that there are two kinds of adenine Ag+ complexes in aqueous solutions, one of which was 9H-Ag7, and the other was two Ag+ ions interacting with the N1 and N7 of N9H.19 Through EMI/MS and DFT calculations, Vrkic et al.23,24 thought there were series of [Adx+Agy zH](y z)+ complexes in the solution of adenine and AgNO3 dissolved in a 50:50 mixture of H2O and CH3OH (1% acetic acid). Their calculated results indicated that in the gas phase the most stable structure should be i-1H-9H-Ag7 and two adjacent silver atoms bridged by two N7H adenine tautomers via N3 and N9 bidentate interactions should be the most stable dimer, which was similar to the crystal structure measurements.21,22

Table 1. The Relative Energies (kcal/mol) of Three Selected Tautomers Calculated in the Gas Phase and in Aqueous Solution with the SMD Model B3LYP/6-311+

B3LYP/

MP2/6-311+

G(d,p)

aug-cc-PVTZ

G(d,p)

species

gas

SMD

gas

SMD

gas

SMD

N9H N7H

0 8.30

0 1.12

0 7.83

0 0.92

0 7.68

0 1.32

N3H

8.09

4.29

7.84

4.16

8.46

4.93

Third, in the SERS of adenine, people thought some signals should come from adenine Ag+ complexes and adenine tautomerized on silver surfaces.4,7,26 28 More recently, Raman spectroscopy was used to infer the structures of adenine Ag+ complexes. Muniz-Miranda and his co-workers calculated the Raman spectra of several adenine Ag+ complexes and compared to the experimental results. They thought the adenine interacted with Ag+ by N3.8 Papadopoulou et al. got the SERS of adenine adsorbed on silver at different pH values and thought adenine did not interact with Ag+ in acid solutions, while in neutral and alkaline solutions, adenine deprotonated and formed two complexes with silver ion of 9H-Ag9 and i-1H-9H-Ag7 as shown in Figure 1.11 From the above brief review, we can find that the stable configurations proposed in previous works are different. 13740

dx.doi.org/10.1021/jp201977z |J. Phys. Chem. C 2011, 115, 13739–13750


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Table 2. Comparison of the Optimized Bond Lengths (Å) of N9H, N7H, and N3H Tautomers along with Experimental Valuesa N9H

expt

N7H

N3H

B3LYP

SMDb

B3LYPc

MP2

GEDd

X-raye

B3LYP

SMD

B3LYP

SMD

C2 N1

1.341

1.341

1.338

1.352

1.344

1.338

1.348

1.344

1.307

1.312

C2 N3

1.334

1.333

1.331

1.338

1.330

1.332

1.325

1.329

1.355

1.347

C4 N3

1.336

1.342

1.333

1.340

1.333

1.342

1.342

1.350

1.373

1.369

C4 C5

1.397

1.395

1.393

1.402

1.401

1.382

1.406

1.398

1.415

1.404

C5 C6

1.409

1.409

1.406

1.410

1.409

1.409

1.401

1.404

1.396

1.404

C6 N1

1.342

1.350

1.339

1.339

1.332

1.349

1.333

1.346

1.368

1.368

C5 N7

1.384

1.388

1.382

1.380

1.380

1.385

1.385

1.381

1.368

1.376

C4 N9 C8 N7

1.377 1.308

1.372 1.314

1.374 1.305

1.378 1.326

1.377 1.319

1.376 1.312

1.382 1.385

1.378 1.357

1.327 1.336

1.339 1.335

C8 N9

1.380

1.370

1.376

1.373

1.371

1.367

1.306

1.321

1.373

1.366

C6 N10

1.353

1.349

1.350

1.367

1.357

1.337

1.379

1.355

1.346

1.339

C2 H11

1.086

1.085

1.083

1.087

1.086

1.085

1.084

1.082

C8 H12

1.080

1.079

1.078

1.082

1.081

1.079

1.082

1.081

Nx H13f

1.008

1.012

1.006

1.011

1.007

1.012

1.012

1.015

N10 H14

1.006

1.010

1.004

1.010

1.011

1.010

1.006

1.009

N10 H15

1.006

1.008

1.003

1.010

1.009

1.010

1.007

1.009

bonds

a

The basis set used in the present calculations is 6-311+G(d,p) except for the special notation. b The theoretical calculation was carried by combining the SMD with B3LYP/6-311+G(d,p). c The basis set of aug-cc-pVTZ was used. d From ref 36. e From ref 58. f x denotes a number of 9, 7, or 3 in N9H, N7H, or N3H tautomers.

This may imply that the binding interaction is sensitive to the experimental conditions such as the concentrations of adenine and silver ion, the pH value, applied potentials and the solvent environment. Until now it seems difficult to make clear line to the interaction of adenine with silver ion (Ag+). Vibrational spectroscopy (i.e., infrared and Raman spectroscopy) has made important contributions to many areas of chemistry because of its high sensitivity to the molecular structure as well as the environment factors; it can provide fingerprint information and has been used to study the tautomerization of adenine.27,29 32 In fact, most biological processes and chemical measurements happen in aqueous solutions or at solid/liquid interfaces. The importance of solvent effect has been shown in a previous study concerning the interaction of adenine with metal ions.33 However, there is a lack of systematic theoretical study on the influence of the solvent effect on the binding interaction of adenine and Ag+ as well as the analysis of vibrational spectra. In this study, we have two goals. One is to theoretically determine the stable structures and vibrational spectra of adenine Ag+ complexes. The other is to analyze the dependence of the vibrational spectra of adenine on different tautomers, the binding interaction with silver ion, and the solvent effect. Our results indicate that the silver ion effect and the solvent effect play important roles in the relative stability of different tautomers and the dimer [7H-Ag3]22+ is the most stable form in aqueous solutions.

’ COMPUTATIONAL DETAILS Adenine itself has 14 tautomers. N9H is the global minimum of the potential energy surface, and N7H and N3H are less stable with energy differences being 7 8 kcal/mol while the other tautomers are much higher.24,34 36 i-1H-N9H is a special structure which is one part of the most stable adenine Ag+ complex in the gas phase.24,25 Thus we consider four adenine tautomers in the present calculation.

Adenine Ag+ complexes can be classified into three categories in terms of the adenine structure. The first one is that adenine keeps the canonical form N9H, and Ag+ binds to adenine at different nitrogen sites. There are three low-energy configurations, just like, 9H-Ag3, 9H-Ag7, and 9H-Ag1. The second category is that adenine tautomerizes to N7H or N1H, and then Ag+ interacts with different nitrogen positions, such as 7H-Ag3 and 1H-Ag7. The third one is that Ag+ forms a complex with an imino form of adenine, such as i-1H-9H-Ag7, i-3H-9H-Ag7 and i-3H-9H-Ag1. On account of the three circumstances, and referring to the previous study,25 we considered eight adenine Ag+ complexes as well as three [adenine Ag]2n+ (n = 0, 2, and 4) dimer complexes, as presented in Figure 1. Because the complexes of adenine with silver ion have positive charges, we add nitrate ions as a counterion to check the influence of the counterion on the stable structures and their vibrational spectra. Quantum chemistry calculations were carried out for geometry optimizations by using B3LYP37 39 and MP240 methods. For C, H, N, and O atoms, the basis sets used were 6-311+G(d,f)41,42 and aug-cc-pVTZ.43 For Ag+, we adopted the small core pseudopotential basis set LanL2DZ.44,45 In order to consider the influence of the Ag+ and the solvent effect on electronic structures of excited states, we further performed time-dependent DFT calculations (TD-DFT) to get excitation energies and oscillator strengths for predicting the vertical excited transitions of the most stable structures. On the basis of the optimized structures, we calculated the vibrational frequencies, proving that all structures reported here were the minima on the potential energy surfaces, which had no imaginary frequency. From vibrational analysis, we got IR intensity and Raman activity of the optimized structures. To make clear the assignment of the vibrational fundamentals in different tautomers, the scaled quantum mechanics force field (SQMF) procedure46 was used to analyze all the fundamental vibrational bands on the basis of the potential energy distribution 13741



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model to consider the hydrogen bond between adenine and water molecules. In addition, we further used the SMD model on the adenine water complexes to have a deeper insight on the solvation influence. Finally, the SMD model was also used to calculate vibrational spectra of adenine Ag+ complexes. All the above quantum chemical calculations were performed with the Gaussian 09 package.50

’ RESULTS AND DISCUSSION

Figure 2. Simulated IR spectra of three low-energy tautomers (N9H, N7H, and N3H) of adenine calculated at the B3LYP/6-311+G(d,p) level. Here a Lorentzian line width of 10 cm 1 was used. (a) IR spectra in the gas phase, and (b) IR spectra in aqueous solution with the SMD model.

(PED). The local symmetry internal coordinates for adenine and adenine Ag+ were defined using the method given by Pulay et al.47 In this study, N9H was selected as the reference molecule for fitting the scaling factors of the B3LYP/6-311+G(d,p) force constants. We chose scaling factors for different kinds of internal coordinates by fitting experimental frequencies from IR spectra of adenine in the Ar matrix-isolated30 and in the gas phase.29 The scaling factors were 0.975 for X Y stretches, X Y Z bends, X Y H bends, 0.982 for all torsions and X Y, X H, Y H out-of-plane bend, 1.000 for H X H bends, 0.924 for C H stretches and 0.916 for N H stretches (X, Y, Z = C and N). The mean deviation was around 8 cm 1, which indicated a good accord with the experiments. Then the scaling factors were used in normal-mode analysis of other adenine tautomers and adenine Ag+ complexes. Scale 2.0 program was used to optimize the scaling factors and to calculate the potential energy distribution.48 To take the solvent effect into account, we used two kinds of solvation models. The first one was the solvation model of density (SMD) approach,49 which considered the nonelectrostatic terms and was recommended to well predict solvation Gibbs free energies (ΔG) of ions and molecules. We chose water with dielectric constant (ε = 78.3) as the solvent. The second one was to directly add water to the adenine molecule, as an explicit

Relative Energies and Structures of Adenine Tautomers. To evaluate the influence of Ag+ on adenine well, we first calculate relative stability and structures of the low-energy tautomers N9H, N7H, and N3H of adenine. Although there are 14 possible tautomeric forms of adenine, the most stable three tautomers are N9H, N7H, and N3H with relative energies 7 8 kcal/mol.24,34,35 Experimentally, only the N9H tautomer could be observed in the gas phase,29 matrix-isolated spectra30 and microwave experiment.51 The coexistence of the less favorable N7H tautomer in energy was proved in the matrix-isolated,52 gasphase (at ∼280 C) IR studies,32 NMR study in DMSO as well as aqueous solution53,54 and T-jump relaxation measurements in water.55 Besides, the NMR measurement showed that N3H coexisted with N9H and N7H in DMSO solution.56 Table 1 shows our calculated results of the relative energies for the three tautomers in the gas phase and in aqueous solution. No matter in the gas phase or in aqueous solution, N9H is always the most stable one, which agrees with the previous studies.34,54,57 Comparing their energy differences listed in Table 1, we can find that the solvent effect dramatically decreases the relative energies of N7H and N3H tautomers. Taking the B3LYP/6-311+G(d,p) calculated results for example, the energy difference between N9H and N7H comes down from 8.30 to 1.12 kcal/mol and the relative Gibbs free energy (ΔG) decreases from 9.07 to 1.24 kcal/mol due to the solvent effect. This is in accord with the NMR results and the T-jump measurement with their ΔG values being about 1.1 and 0.7 kcal/mol, respectively.31,53,55 At the same time, the energy difference between N9H and N3H comes down slightly from 8.09 to 4.29 kcal/mol and the relative Gibbs free energy (ΔG) decreases from 8.93 to 3.90 kcal/mol. This significant change comes from the large difference in the dipole moments of the three structures. The dipole moments of N9H, N7H, and N3H are predicted to be 2.48, 7.56, and 4.36 D at the B3LYP/ 6-311+G(d,p) level. The polarity of the solvent and the hydrogen bonding between tautomer and the solvent will be expected to influence their relative stability. The energy difference in the present calculation for N9H and N7H is smaller while being larger for N9H and N3H than the result calculated by Hanus et al. with thermodynamic integration method; 34 the main reason is probably due to the different solvation models used. Table 2 presents the optimized bond distances along with experimental data.36,58 It is found that the optimized structures at the MP2/6-311+G(d,p) level have about 0.007 Å derivations from the experimental data at several bond lengths, such as N1 C2, C2 N3, N3 C4, C6 N1, C8 N7 and C6 N10. Although the B3LYP/6-311+G(d,p) predicted the bond lengths of C6 N1, C8 N7, C8 N9 not well, it is slightly better than MP2/6-311+G(d,p). When increasing the basis set to aug-ccpVTZ, it does not improve the accuracy markedly but it takes a longer time than that with 6-311+G(d,p). In previous studies, B3LYP was thought to be more reliable than MP2 in calculating 13742



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Table 3. Calculated Frequencies, IR Intensity (IIR, km/mol), Raman Activity (AR, Å4/amu), and Assignment of N9H and N7H Tautomers along with the Experimental Dataa expt ν

b

νc

N9H IIR

AR

N7H IIR

PED (%)

AR

PED (%)

0 ωNH2(91)

153

4

Q2

214

162 163

30

0 τR2(62), τR3(17)

200

23

Q3 Q4

242 276

208 214 270 273

0 12

0 τC4C5(68), τR1(17) 3 βNH2 (54), βR1 (12)

284 295

1 3

296

1

0 τR1(58), τr1(23)

352

71

Q6

503

506 512

72

1 γN9H(77)

392 114

Q7

513

515 514

4

3 βR1(31), βNH2(25), νC4N9(11)

517

2

3 βR2(56), βNH2(10), ωNH2 (11)

525

2

3 βR2(61), βR1(13)

528

62

9 βR1(34), βNH2(14), ωNH2(11)

Q1

53 190

Q5

Q8

0 τR2(64), τR3(19), γNH2 (11) 0 τC4C5(64), τR1(20) 3 βNH2(51), βR1(11) 0 τR1(52), τr1(15), τC4C5 (13) 1 τNH2(74), ωNH2(15) 1 γN7H(92)

534

3

0 τNH2(90)

547

14

3 ωNH2(47), βR1(11)

Q10 566

576 570

53

1 τR2(26), τR3(23), τr1(20), γN9H (18)

577

32

1 τR2(27), τR3 (24), τr1(16), ωNH2(12)

Q11 610 Q12 655

600 611 650 661

1 7

7 νC5C6(23), βr1(18), βr2(18), βR1 (17) 0 τr2(76), τr1(12)

606 628

1 18

6 νC5C6(21), βr1(16), βr2(17), βR1(17) 1 τr2(74)

Q13

679

1

695

16

1 γNH2(45), τr1(26), τC4C5(11)

Q14 717

716

2

716

3

26 νN3C4(24), βr2(20), νC5N7(10)

Q15 802

801 801

11

Q16 848

847 843

8

Q9

0 γNH2(46), τr1(26), τR1(14), τC4C5 (13) 25 νN3 C4(21), βr2(15), νC5N7(11), νC4N9(10) 1 τR3(48), γNH2(22), τr2(14), τr1(10)

791

16

0 τR3(56), τR1(27), γNH2(10)

1 γC8H(96)

867

15

1 γC8H(100)

Q17 887

889

12

2 βR3(49), βR2(15)

883

14

Q18 927

926 933

14

4 βr1(55), βr2(20), νC4C5(11)

935

2

Q19 958 Q20 1005

957 967 1018 996

4 5

967 1018

5 31

0 γC2H(100) 5 NH2 rock(48), νC6N1(28), νN1C2(9)

1 βR3(46), βR2(15) 4 βr1(53), βr2(18), νC4C5(16) 0 γC2H(100) 6 NH2 rock(38), νC6N1(26), νN1C2(10)

Q21 10611065 1053 1066

21

8 νC8N9(57), βN9H(31)

1078

25

Q22 1127

1126 1128

23

2 νC4N9(20), βr2(15), νC6N10(10), βC8H(10)

1110

9

5 νN7C8(45), βN7H(24), βC8H(13)

Q23 1229

1234 1226

15

15 NH2 rock(25), νC5N7(24), νC2N3(10)

1218

10

6 νC5N7(19), βC8H(18), NH2 rock (17), νN1C2(10)

Q24 1240

1250

27

17 βC8H(36), νN7C8(16), βN9H(10)

1268

12

2 νN1C2(24), βC8H(24), νC6N1(15)

6 νC4N9(19), νN7C8(18)

Q25 1290

1280 1310

75

18 νC2N3(47), νN1C2(14), νC5N7(9)

1290

0

15 νC2N3(22), νN1C2(20), νC6N1(15)

Q26 1328

1326 1339

40

46 νN1C2(30), νC5N7(22), νC4C5(10)

1336

23

12 βC2H(38), νC4N9(14), νN3C4(12)

Q27 1345

1346 1347

26

39 βC2H(20), νC8N9(14), βC8H (11), νC6N10(10), βN9H (9)

1359

24

90 νC4N9(17), βR3(13), νC8N9(12), βC8H (10)

27 βN9H(28), βC2H(23), νC4N9(14), νC8N9(13) 1371

87

15 νC4C5(26), βC2H(18), νC2N3(17), νC5N7(15)

Q28 1389

1397

14

Q29 1419

1415 1415

20

Q30 1474

1468 1483

85

Q31 1482

1495

9

Q32

1596

15

Q33 1612

1614 119

1 νC4C5(26), νC4N9(16), βC2H(14)

1400 174

13 νC6N1(25), βC2H(20), νC2N3(14), νC6N10(13)1484

22

77 νN7C8(43), βC8H(19)

39

1508

4 βNH2 sci(35), νC4C5(17), νC5C6(14)

1568 135

22 νN3C4(26), νC5C6(12)

1630

Q34 1633 Q35 3041

1625 1644 654 9 βNH2 sci(49), νC6N10(19), νC5C6(14) 3045 18 137 νC2H(100) 3061 3111

3434 3451 103 174 νNH2 sym(100)

Q383508d

3501 3497

90 144 νN9H(100)

Q393569d

3552 3587

65

17 νC8N9(55), βC8H (17) 17 νN3C4(28), νC4C5(20), νC6N1(17) 3 νC5C6(27), βNH2 sci(27)

1650 397 13 βNH2 sci(63), νC5C6(12), νC6N10(10) 3047 20 141 νC2H(100)

0 120 νC8H(100)

Q36 3057 Q373452d

37

6 βN7H(44), νN7C8(23), νC6N10(10) 24 βC2H(37), νC6N1(18), νC2N3(16)

3108

46 νNH2 antisym (100)

1 124 νC8H(100)

3412

44 198 νNH2 sym(100)

3497

64 118 νN7H(100)

3517

32

57 νNH2 antisym(100)

ν, stretching; β, bending; γ, out; ω, wagging; sci, scissoring; rock, rocking; τ, torsion; r, five-membered ring; R, six-membered ring; βr1 = β1 + a(β2 + β5) + b(β3 + β4); βr2 = (a b)(β2 β5) + (1 a)(β3 + β4); βR1 = 2R1 R2 R3 + 2R4 R5 R6; βR2 = R2 R3 + R5 R6; βR3 = R1 R2 + R3 R4 + R5 R6; τr1 = b(τ1 + τ5) + (τ2 + τ4) + τ3; τr2 = (a b)(τ4 τ2) + (1 a)(τ5 τ1); τR1 = μ2 μ3 + μ5 μ6; τR2 = 2μ1 μ2 μ3 + 2μ4 μ5 μ6; τR3 = μ1 μ2 + μ3 μ4 + μ5 μ6. b Argon matrix IR data from ref 30. c IR data in the gas phase in ref 29. d From IR UV data in ref 32.

a

vibrational frequencies and potential energy distribution.59 Considering the above two reasons, the vibrational spectra and the potential energy distribution are given at the B3LYP/6-311 +G(d,p) level in this study. Vibrational Spectra of N9H, N7H and N3H. Figure 2 presents the simulated IR spectra of N9H, N7H, and N3H calculated at the B3LYP/6-311+G(d,p) level. In order to understand the

spectra of the three tautomers well, we analyze the fundamental vibrational bands by reassigning the vibrational frequencies according to the PED values of the three tautomers though there are numerous studies on this subject. For example, Nowak et al.,30 Xue et al.,60 Giese et al.61 and Mohamed et al.62 made detailed assignments of N9H. Kuczera et al.31 assigned the fundamental vibrations of N7H on the basis of the force 13743



Figure 3. Simulated Raman spectra of three low-energy tautomers (N9H, N7H, and N3H) of adenine calculated at the B3LYP/6-311 +G(d,p) level. The incident wavelength of 514.5 nm was used here with a Lorentzian line width of 10 cm 1. (a) Raman spectra in the gas phase, and (b) Raman spectra in aqueous solution with the SMD model.

constants calculated at the HF/4 31G level. Since the tautomerization of adenine in different conditions has been suggested in many experimental studies, it is necessary to further do normalmode analysis for interpreting the change of the observed vibrational spectra due to the possible tautomerization.63,64 Table 3 presents scaled frequencies, IR intensities, Raman activities and the assignment along with the experimental data of N9H and N7H. The data for N3H are presented in Table 1S in the Supporting Information. At first we compared the IR spectra of the three tautomers (Figure 2a). We can find that the band near 1650 cm 1 related to the NH2 scissoring vibration dominates in the whole spectrum, that is to say it is the most intensive band. The frequencies of this band are 1644, 1650, and 1658 cm 1 for N9H, N7H, and N3H, respectively, while the corresponding intensities are 654, 397, and 766 km/mol. This band can be attributed to a mixed vibration of the amino scissoring, C6 N10 and C5 C6 stretching coordinates. For N9H and N7H, the PED values of the amino scissoring are 49 and 63, respectively, indicating that this mode mainly comes from the amino scissoring vibration. For N3H, this mode mainly comes from the mixture of the C5 C6 stretches with a PED of 26 and the amino scissoring with a PED of 24. Because of the small frequency difference of the three tautomers and NH2 vibration

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being sensitive to the experimental conditions,65,66 it is not the best indicator to infer whether there are other tautomers. Although it is not easy to identify the three tautomers by the most intensive IR band, one can get the other characteristic bands with one-tenth of IR intensity of the scissoring vibration. For example, we note that N9H has a band at 512 cm 1 (γN9H); N7H has three bands 352 cm 1 (τNH2), 392 cm 1 (γN7H), and 547 cm 1 (ωNH2) below 600 cm 1, as well as three bands 1018 cm 1 (NH2 rock coupling with the νC6N1), 1371 cm 1 and 1568 cm 1 in the range of 1000 1600 cm 1. For N3H, there are three characteristic IR bands at 228 cm 1 (ωNH2), 1158 cm 1 (νC8N9 coupling with βC8H) and 1452 cm 1. Having the characteristic bands, we can find that the characteristic bands 352, 392, 547, 1371, and 1568 cm 1 of N7H and 1452 cm 1 of N3H do not appear in the Ar matrix-isolated30 and in the gas phase29 IR spectra of adenine, which means only N9H exists in the gas phase. Figure 3 presents simulated Raman spectra of three tautomers at the B3LYP/6-311+G(d,p) level. They are quite different from each other. This provides the possibility to easily identify these different tautomers, especially the bands located in the range of 1200 1600 cm 1, which mainly come from C C and C N stretching coordinates mixing with the N H and C H in-plane bending coordinates (see Table 3). In this range, N9H has two characteristic bands, 1340 and 1495 cm 1. The former band consists of two strong fundamentals of 1339 and 1347 cm 1. This is in good accord with the experimental results of polycrystalline adenine that has a strong band at 1333 cm 1 and a broad band at 1483 cm 1.61 Our DFT calculation predicts that N7H has only one strong band at 1359 cm 1 in this range; its Raman scatting factor is predicted to be about 90 Å4/amu, which is larger than that of the other fundamentals. N3H has two strong bands at 1282 and 1423 cm 1 in this range. It should be emphasized that, for all three tautomers, their breathing modes are very intensive ones in the whole wavenumber region in the normal Raman spectra. Numerous studies involving adenine concentrated on this band.5,6,8,67 The frequencies of the three tautomers are 716 (N9H), 716 (N7H), and 710 cm 1 (N3H). From the PED in Table 3, the main contributions to this mode are from the C4 N3 stretches and the five-membered ring deformation. Owing to the slight change of the five-membered ring deformation, we focus on the disparity of the C4 N3 stretches. Indeed, the C4 N3 bond lengths are 1.336, 1.342, and 1.373 Å, corresponding to the breathing mode with vibrational frequencies in the order 716, 716, and 710 cm 1 for N9H, N7H, and N3H, respectively. Solvent Effect. Figures 2b and 3b give simulated IR and Raman spectra of the three structures with the SMD solvation model. Compared with the simulated spectra in the gas phase, the solvent effect obviously affects the spectra of the three tautomers in both band intensities and frequencies, especially for N3H and N7H. For intensity, both IR and Raman signals increase because of the solvent effect. This is in good agreement with the prediction of IR and Raman intensities for pyridine in aqueous solutions.68,69 For frequencies, there are large changes of N7H and N3H. This is in accord with variation of their structures under the solvation condition (See Tables 1 and 2). The changes of N3H and N7H structures lead to the significant changes of their vibrational spectra. This can be understood due to their large dipole moments, as mentioned above. Similar to the gas phase, we can also get the characteristic bands of the three tautomers in aqueous solution. As shown in Figure 2b, the 13744



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Figure 4. The optimized structures of water N9H along with the frequencies (ω in cm 1) of NH2 scissoring mode and the IR intensity (IIR in km/mol). The vibrational frequencies are calculated at the B3LYP/6-311+G(d,p) level without scaling.

characteristic band of N9H is 574 cm 1; then there are two characteristic bands 280 and 1388 cm 1 for N7H and 624, 1173, 1443 cm 1 for N3H, respectively. Observing the IR intensities of NH2 scissoring vibration of the three tautomers (see Table 3), N7H is much weaker than the other two tautomers. To further investigate the relationship between the IR intensity and structures, we choose N9H as the model to analyze the environment effect, referring to the stable structure of water N9H complexes predicted by Hanus et al.;34 we add water molecules one by one to study the influence of water through the hydrogen bonding on the amino scissoring mode. As shown in Figure 4, the water molecule near the amino group significantly affects this mode. Its frequency has a large blue shift which agrees with the previous study,57 but its intensity decreases obviously. With increasing to three waters, not only the blue shift extent increases, but also the intensity further decreases. This can explain the frequency blue shift and the relative intensity decrease of this mode in the solid adenine due to the intermolecular interaction just like the hydrogen bond and π π stacking.62,70,71 We also examine the influence of the solvent effect on the structure, IR and Raman spectra by directly adding a water molecule to an adenine molecule. The structural parameters of N9H and N7H from the SMD model are compared with the PCM model, an explicit model with water molecules as shown in Table S2 in the Supporting Information; small differences can be found from these different solvation models. Moreover, for the vibrational spectra, taking N7H for example, adding one water, one can find that the intensities of several bands in 1200 1600 cm 1 increase in the Raman spectrum, and continuing to add one more water, the intensities increase more. The result of the explicit water model agrees well with the SMD model, as shown in Figure 1S in the Supporting Information. Relative Stability of Adenine Ag+. Table 5 presents the relative energies of eight tautomers with different theoretical methods and with taking account of the nitrate ion. According to the energy data, we can easily find that there are two stable forms of i-1H9H-Ag7 and 7H-Ag3 in the gas phase. The energy of i-1H-9H-Ag7 is 1.60 kcal/mol lower than that of 7H-Ag3 calculated at the B3LYP/ 6-311+G(d,p) level. We further calculated the two structures at the MP2/aug-cc-pVTZ level. Their energy difference increases to 4.20 kcal/mol. It is worth mentioning that the adenine part of the two stable structures occurred the tautomerized, in accord with previous studies.24,25 That indicates that through the interaction of adenine with Ag+ the strong electrostatic interaction and the coordination bonding can stabilize the higher energy tautomers in the gas phase. As shown in Figure 5, the 5s unoccupied orbital of Ag+ which locates at 0.38 au simultaneously interacts with the lonepaired orbitals of N7 and N10 in i-1H-N9H adenine imino tautomer at 0.28 au to form a strong coordination bond at 0.52 au, which dramatically stabilizes the i-1H-9H-Ag7 complex. Meanwhile, the electrostatic interaction plays an important role in the binding interaction of the adenine Ag+ complexes.

Figure 5. The orbital plots of the lone pairs of i-1H-N9H adenine imino tautomer and its silver ionic complexes.

By inspecting the relative energies of the eight tautomers calculated from the SMD model in Table 4, it is found that there are four stable structures of 9H-Ag3, 9H-Ag1, 9H-Ag7, and 7HAg3 with small energy differences in the range of 0.10 1.32 kcal/mol. However, the most stable structure of i-1H-9H-Ag7 in the gas phase becomes very unstable. For i-1H-9H-Ag7, the N7 Ag bond length remarkably increases from 2.43 Å to 2.64 Å. For 7H-Ag3, the location of Ag+ changes obviously that the angle of — C4 N3 Ag increases from 108.3 to 121.8 and the N3 Ag bond length comes up from 2.206 Å to 2.235 Å. This means that the strong polarity of water dramatically weakens the interaction between Ag+ and adenine. We note that the N Ag bond distances also increase in the other structures if considering the solvent effect. In addition, the most obvious change is the amino group intending to be planar with the solvent effect as shown in Figure 1, compared with the nonplanarity due to the interaction between the lone-pair electrons of the amino group and Ag+ in the gas phase. Finally, three of the four stable structures belong to the canonical adenine N9H interacting with Ag+, only the other one is the N7H tautomer binding to Ag+. So we can infer that adenine inclines to interact with Ag+ in a canonical form in aqueous solution if the adenine Ag+ complex is a monomeric form. To consider the influence of the counterion effect, we added nitrate ion to the complexes to inspect their relative stability. As shown in Table 5, in the gas phase, with the nitrate ion, the relative stability changes significantly. The nitrate ion weakens the interaction between adenine and silver ion, leading to the two stable structures in the gas phase without nitrate ion having much higher energies, while 9H-Ag3 becomes the most stable one among them. When the SMD model is used, there are four stable structures 9H-Ag1, 9H-Ag3, 9H-Ag7 and 7H-Ag3 with small energy differences within 1 kcal/mol. This is similar to the above case without the counterion effect. Vibrational Spectra of Adenine Ag+. To understand the influence of the binding interaction on vibrational spectra of adenine, we mainly discuss three aspects here. The first one is the influence of Ag+ on the structure and Raman spectrum of adenine. The second one is the difference between two stable adenine Ag+ complexes in the gas phase. And the third one is 13745



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Table 4. Relative Energies (kcal/mol) of Eight Adenine Ag+ Complexes with Nitrate Ion and without Nitrate Ion in the Gas Phase and in Aqueous Solution by the SMD Solvation Model along with Data from Previous Theoretical Studies B3LYP/6-311+G(d,p)

a

b

species

gas

NO3

SMD

i-1H-9H-Ag7

0.00

17.53

6.12

7H-Ag3

1.60

11.42

0.25

9H-Ag1 9H-Ag3

9.61 7.47

2.77 0.00

0.00 0.43

9H-Ag7

7.73

2.40

1H-Ag9

6.00

17.48

i-3H-9H-Ag7

7.48

26.46

i-3H-9H-Ag1

11.06

26.79

B3LYP/aug-cc-pVTZ NO3

c

MP2/6-311+G(d,p)

MP2/cc-pVTZa

gas

SMD

gas

SMD

gas

7.15

0.00

5.95

0.00

7.05

0.0

0.65

1.56

0.00

1.76

1.32

3.3

0.00 0.50

7.82 7.38

0.12 0.37

6.61 9.38

0.25 0.00

9.0 10.3

0.20

0.21

8.76

0.10

4.03

0.55

5.8

2.64

2.76

5.87

2.44

6.41

4.58

7.2

11.89

15.44

7.24

11.52

8.55

13.93

8.3

12.04

12.28

10.88

11.56

13.38

15.67

From ref 25. b With nitrate ion in the gas phase. c With nitrate ion in aqueous solution by the SMD solvation model.

Table 5. Scaled Vibrational Frequencies (ν, cm 1), Raman Activity (AR, Å4/amu), and Assignments of Selected Vibrational Modes of i-1H-N9H and i-1H-9H-Ag7 Calculated at the B3LYP/6-311+G(d,p) Level i-1H-N9H freq

AR

i-1H-9H-Ag7

PED (%)

689

18

νN3C4(24), νC6N1(17) βr2(14)

1276

22

βC8H(25), C5N7(20) νN7C8(12), νN3C4(10)

freq

AR

PED (%)

709

20

νN3C4(20), νC6N1(12), βr2(14)

1299

36

C5N7(31), βC8H(12)

1364

40

νC5N7(24), νC5C6(11) βC2H(10), νC2N3(10)

1392

38

νC2N3(19), νC5C6(16), νC5N7(14) βN1H(13)

1388

70

βC2H(32), βN9H(24), νC8N9(18)

1404

68

βN9H(35), νC8N9 (23), βC2H(18)

1423

44

βN1H(20), νN7C8(14), νC4C5(12), νN1C2(12) βC2H(11)

1427

22

βC2H(19), βN1H(18), νC4C5(11)

1456 1502

73 99

βN1H(28), νN7C8(25) νC4C5(23), νN7C8(13), βC8H(11), νC6N10(11)

1458 1517

32 60

νN7C8(25), νC6N10(16), βC8H(12) νC4C5(15), νN7C8(14), νC6N10(14), βC8H (12)

1563

62

νN3C4(23), νC4C5(22), βN9H(15) νN7C8(13), νC4N9(11)

1588

60

νC4C5(24), νN3C4(24), βN9H(13)

1608

72

νC2N3(57), βC2H(13), βN1H(10)

1609

38

νC2N3(43), βN1H(15), βC2H(11)

1708

96

ν C6N10(55), νC5C6(17)

1680

47

νC6N10(35), νC5C6(24)

Figure 6. Simulated Raman spectra of adenine and adenine Ag+ complex (a) 7H-Ag3, (b) i-1H-9H-Ag7, and (c) i-1H-N9H calculated at the B3LYP/6-311+G(d,p) level. The other parameters are the same as in Figure 3.

Figure 7. Simulated Raman spectra of the four most stable adenine Ag+ complexes calculated at the B3LYP/6-311+G(d,p) level with the SMD model in aqueous solution (ε = 78.3). (a) 7H-Ag3, (b) 9H-Ag3, (c) 9H-Ag1, and (d) 9H-Ag7. The incident wavelength of 632.8 nm was used here with a Lorentzian line width of 10 cm 1.

what should be responsible for the observed Raman spectra of adenine Ag+ complexes in aqueous solution.

First of all, taking the most stable imino tautomer i-1H-9HAg7 for example, the binding interaction to Ag+ affects the 13746


νN3C4(29), νC4C5(22) 1591 νC4C5(27), νN3C4(26) 1601

1497 νN7C8(28), βC8H(21),

νC6N10(10)

1507

νN7C8(15), νC6N10(21), βC2H(13)

1602

1500

νN3C4(23), νC4C5(28)

νN7C8(24), νC6N10(14), βC8H(14)

1566

1483

νN3C4(30), νC4C5(23)

νC8N9(18), βC2H(13), βC8H(14)

νN7C8(32), νC6N10(13) 1420 βC2H(28), νC6N1(14), νN7C8(14) 1474 νN7C8(13)

βC2H(16), νC2N3(13), νC6N1(12), 1481 βC2H(29), νC6N1(18), νC2N3(12) 1480

νC6N1(10)

νC4C5(24), βC2H(17) 1402 βN9H(20), βC2H(17), νN1C2(14), νC6N1 (14), νC8N9(12) 1409 1396 βN9H(26), νC8N9(21), νN3C4(19) 1408

βC2H(31), νC4N9(17), βN9H(17), νC8N9(11)

νN1C2(33), νC2N3(24), νN3C4(13),

νC4N9(29), νC8N9(18), βC2H(10) 1341

1350 νC8N9(23), βC8H(12), βN9H(17)

νC2N3(39), νC5N7(22) 1307

1351

1323

1360

νN1C2 (45), νC5N7(12)

νC6N10 (12), βC2H(20)

1346

νN1C2(38), νC5N7(15), νC6N1(10)

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1354

νC2N3(23), νC8N9(13), νN3C4(10

νC2N3(31), νC8N9(24), βC8H(20) 1258 νN7C8(16), βN9H(12)

βC8H(34), νC2N3(17), 1247 1240 βC8H(33), νN7C8(19), νC2N3(10) 1254

βC8H(32), νN7C8(18), νN1C2(15)

νC5N7(20), βC8H(18), NH2 rock(18)

νN3C4(21), βr2(17) 729

1219 NH2 rock(27), νC5N7(21), C2N3(10),

νN3C4(18), βr2(13) 725

1220 NH2 rock (29), νN1C2(12), νC5N7(20)

νN3C4(20), βr2(12), νC5N7(10) 717

1229

νN3C4(21), βr2(18), νC5N7(10)

NH2 rock(26), νC5N7(25)

718

1219

PED (%) 7H-Ag3 PED 9H-Ag3 PED (%) 9H-Ag1 PED (%) 9H-Ag7

Table 6. Scaled Frequencies (cm 1) and Potential Energy Distribution (PED) of Selected Vibrational Modes in 9H-Ag7, 9H-Ag1, 9H-Ag3, and 7H-Ag3 Complexes Based on the Force Constants Calculated at the B3LYP/6-311+G(d,p) Level


structural parameters of adenine near Ag+ obviously. The bond distance decreases from 1.433 Å to 1.396 Å for the N1 C6 bond and from 1.450 Å to 1.430 Å for the C5 C6 bond. The binding interaction also leads to the significant increase of the C6 N10 bond distance from 1.276 Å to 1.296 Å while the changes of the structural parameters in the five-membered ring are relatively small. Figure 6 presents the simulated the Raman spectra of i-1HN9H, i-1H-9H-Ag7 and 7H-Ag3 in the gas phase. As an imino form, i-1H-N9H is very different from other tautomers for there are several strong bands in the range 1200 1700 cm 1. We can see significant changes of the Raman spectrum after i-1H-N9H binds to Ag+. Here we concentrate on the variations of the strong Raman bands. Table 4 gives the frequencies, the Raman activity and PED of the strong bands of i-1H-N9H and i-1H-9H-Ag7. Through the comparison of the frequencies of selected ten strong bands, it is noted the bands at 689, 1276, 1364, 1388, 1502, and 1563 cm 1 blue shift, only the 1708 cm 1 band red shifts, and the bands at 1423, 1456, and 1608 cm 1 almost keep constant. For the Raman intensity, five bands at 1423, 1456, 1502, 1608, and 1708 cm 1 decrease dramatically, four bands at 689, 1364, 1388, and 1563 cm 1 almost keep the same while only 1276 cm 1 increases. The breathing mode of the i-1H-N9H has a fundamental frequency at 689 cm 1; this mode blue shifts to 709 cm 1 after interacting with Ag+. This is because the N3 C4 and N1 C6 bond distances shorten after interacting with Ag+, while the band corresponding to the vibration mixed by the C6 N10 and C5 C6 stretches red shifts from 1708 to 1680 cm 1. As for the second problem, Figure 6 gives the Raman spectra of the two stable tautomers i-1H-9H-Ag7 and 7H-Ag3: they are distinct from each other. This is mainly due to the large difference of their structures. The above discussion has mentioned that the imino species has several strong bands in the range 1200 1700 cm 1, while the N7H has only one strong band in this range. Meanwhile, when Ag+ binds to different nitrogen sites in the two tautomers, their Raman band shapes are quite different. Thus it is easy to identify the two complexes if their experimental spectra will be obtained in the gas phase. Besides the difference in the range 1200 1700 cm 1, the most characteristic breathing mode of adenine also can be used to identify the two tautomers. We can see the frequencies of i-1H-9H-Ag7 and 7H-Ag3 are 709 cm 1 as well as 729 cm 1, and the corresponding Raman activities of 19.6 and 40.13 Å4/amu, respectively. Figure 7 presents the Raman spectra of the four stable adenine Ag+ complexes calculated with the SMD model. The PED values of the strong bands of interest are also given in Table 6. This can help us to understand the third problem. Comparing the spectra of 9H-Ag3, 9H-Ag1, 9H-Ag7, and 7HAg3, it is similar to the case in the gas phase in which the intensities and frequencies change remarkably in different tautomers. Different tautomers can be distinguished from each other. Considering the small energy difference of the four structures, according to the Boltzmann distribution, if the complex adopts a monomeric form, the mixture of four complexes contributes to the measured Raman spectrum. However, as seen in the next section, the adenine Ag+ monomer may easily convert to a dimer, which is more stable thermodynamically in fact. The results of considering the nitrate ion are not given here because of the similarity to the one which does not include nitrate ion as shown in Figure 2S in the Support Information. Adenine Ag+ Dimer [7H-Ag3]2n+ (n = 0, 2, or 4). Comparing the relative energies of the eight tautomers, the results show 13747



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Table 7. Comparison of Influences of the Tautomerization Effect, the Silver Ion Effect, and the Solvent Effect on Electronic Transition Energy (ETE/eV), Oscillator Strength (f) of the Low-lying Singlet Excited States for Adenine, 7H-Ag3, and [7H-Ag3]22+ Calculated at the B3LYP/ 6-311+G(d,p) Level gas structure

that 7H-Ag3 is a special stable configuration in the gas phase and in aqueous solution. Gagnon and Beauchamp measured the structure of adenine with silver perchlorate.21 Their results showed that a bidentate coordination via N3 and N9 nitrogen atoms of two adenine molecules was formed. Recently, Mishra et al. measured the crystal structure formed by adenine with silver nitrate in acid solution; they obtained a similar crystal structure.22 However, while the defined constituent was obtained in crystal structure, the states of adenine Ag+ complexes in aqueous solution are unknown to us. Obtaining the two stable adenine Ag+ monomeric complexes in the gas phase, we calculated the optimized structures of two dimers which consisted of i-1H-9HAg7 and 7H-Ag3, respectively. The calculated results indicated that the dimer of 7H-Ag3 is a planar and centrosymmetric structure while the dimer of i-1H-9H-Ag7 is a nonplanar structure, in which the angle between the two purine rings is about 10. Our calculated results also show that the dimer of 7H-Ag3 is more stable than the dimer of i-1H-9H-Ag7 with the Gibbs free energy (ΔG) being 13.65 kcal/mol. So we only consider the dimer of 7H-Ag3 in the prediction of Raman spectra.

f

assignment ETE/eV

f

assignment

S1

4.93

0.0050 n f π*

4.95

0.2918 π f π*

S2

4.99

0.2046 π f π*

5.17

0.0021 n f π*

N7H

S1

4.68

0.0052 π f π*

4.88

0.2211 π f π*

7H-Ag3

S2 S1

4.92 2.89

0.1096 π f π* 0.0006 π f 5s

5.15 4.01

0.0033 n f π* 0.0018 π f 5s

N9H

Figure 8. Comparison of simulated Raman spectra of the dimer of 7H-Ag3 in different configurations with experimental Raman spectra recorded at excitation wavelength of 632.8 nm. (a) The experimental Raman spectrum of adenine and silver nitrate in acid, neutral and basic aqueous solution from top to bottom; the 1050 cm 1 band arises from NO3 . (b) The deprotonated dimer form of 7H-Ag3, the dimer of 7HAg3 with positive charge of +2, and the dimer of 7H-Ag3 protonated at the N1 site with positive charge of +4, respectively. The theoretical spectra were calculated at the B3LYP/6-311+G(d,p) level with the SMD model in aqueous solution (ε = 78.3). The other parameters are the same as in Figure 7.

state ETE/eV

SMD

S2

3.89

0.0589 π f 5s

4.37

0.0727 n f 5s

[7H-Ag3]22+ S1

4.74

0.2727 π f π*

4.71

0.0022 d f π*

S2

4.80

0.0000 π f π*

4.74

0.0000 d f π*

S3

4.82

0.0016 d f π*

4.80

0.5821 π f π*

Now we check the possibility of dimerization of 7H-Ag3. At the B3LYP/6-311+G(d,p) level, we can estimate the ΔG energy of 7H-Ag3 to [7H-Ag3]22+ at about 8.03 kcal/mol in the gas phase. This shows that [7H-Ag3]22+ should be unstable in the gas phase. Nevertheless, the ΔG energy of 7H-Ag3 to [7H-Ag3]22+ is predicted to be 14.51 kcal/mol with the SMD solvation model. That indicates that adenine Ag+ complexes are inclined to form the dimer in neutral aqueous solution. Considering the pH effect, we further calculated the other two dimers of 7H-Ag3, one of which is protonated in N1, and the other is deprotonated in N7, to simulate the possible species in the acidic and basic solutions.11,72 The Gibbs free energies of their dimerization processes are 3.45 and 21.98 kcal/mol for the [7H-Ag3]24+ and [7H-Ag3]2, respectively. This means that the dimerization processes should be thermodynamically favorable for the dimer of 7H-Ag3 in different pH solutions. Figure 8 gives the simulated Raman spectra of the three dimers along with our experimental Raman spectra of the complexes which were formed by adenine and silver nitrate in acid, neutral and basic aqueous solutions, respectively. The sample preparation and the Raman measurement are provided in the Supporting Information. By comparison with the observed Raman spectra, the simulated Raman spectra of the complexes agree well with the experiment. It was noted that the vibrational frequency of the breathing mode of adenine in neutral and basic aqueous solutions is 740 cm 1 larger than 729 cm 1 in acid solution, which is also the same in our simulated Raman spectra. It is clear that the simulated Raman spectra of [7H-Ag3]22+ is different from the other two structures and the experimental results have the same conclusion. The most obvious difference comes from the relative intensity in the region of 1200 1600 cm 1. [7H-Ag3]22+ has two strong bands at 1340 cm 1, which comes from the stretching coordinates of νC2N3, νC8N9 coupling with N1H inplane bends, and 1406 cm 1 contributed by νC4C5 and βC2H in-plane bend. The [7H-Ag3]24+ possesses a very strong band at 1416 cm 1, which is contributed by three stretching coordinates of νC2N3, νN3C4 and νC5C6 coupling with the N1H in-plane bends. For [7H-Ag3]2, the peak at 1281 cm 1 is the strongest band, which can be assigned to the νN7C8, νC8N9 stretches and the βC8H in-plane bends. The above calculated result clearly indicates that the dimer should be the most stable species of 13748


The Journal of Physical Chemistry C adenine Ag+ complexes and responsible for the observed Raman spectra. Finally, we further compare the UV visible absorption spectra from the TD-DFT calculations (see Table 7) with the experimental spectra reported in previous study. Here we consider two adenine tautomers of N9H and N7H, the adenine Ag+ complexes of 7H-Ag3 and its dimer [7H-Ag3]22+. In previous studies, two peaks located at 4.40 and 4.48 eV were observed in the experimental R2PI spectra of adenine.73 76 Form our calculation, there are two absorption peaks involved to two excited states (S1 and S2) with the excitation energy 4.93 and 4.99 eV which are about 0.5 eV larger than the experimental data. They correspond to n f π and π f π* transitions with oscillator strengths of 0.0050 and 0.2046, respectively. Considering the solvent effect with the SMD model, the excitation energy changes a little, which means the solvent effect does not influence the transition energy much for N9H. In contrast with the adenine itself in aqueous solution, the strong and broad peak of the adenine Ag+ complex in solution red shifts about 0.16 eV from 4.64 to 4.48 eV.20 For the dimer [7H-Ag3]22+, our TDDFT calculation predicts the transition energy of the first three singlet excited states (S1, S2, and S3) at 4.71 4.80 eV. But only the oscillator strength of the S3 is quite large, about 0.5821, corresponding to a π f π* transition, compared to the π f π* transition of N9H. It moves about 0.15 eV from 4.95 to 4.80 eV. These results are in good agreement with the experimental observation. Since the low-lying excited energies are close to the UV region, the nonresonance Raman spectrum in the present calculation should be similar to the experimentally measured Raman spectra of adenine Ag+ complexes with visible light excitation.

’ CONCLUSION In this paper, on account of the possible surface species adenine Ag+ in the SERS of adenine on silver substrate, we inspect the influence of the tautomerization, solvent effect, and the binding interaction on vibrational spectra of adenine and adenine silver ion complexes using quantum chemistry calculations. Our results show that the adenine N9H tautomer dominates in the gas phase. However, the energy differences of N9H, N7H, and N3H observably decrease after considering the solvent effect, particularly the energy difference between N9H and N7H decreasing to 1.3 kcal/mol. Therefore, this proposes that the N9H and N7H tautomers possibly coexist in aqueous solution and contribute to the observed spectra. From theoretical analysis on vibrational spectra, we assign the characteristic vibrational bands of N9H, N7H and N3H tautomers. Our calculated results also show that the solvent effect markedly influences geometric structures and vibrational spectra of the N7H and N3H tautomers. For adenine Ag+ monomeric complexes, there are two stable structures of i-1H-9H-Ag7 and 7H-Ag3 in the gas phase. The adenine parts of the two structures have been tautomerized due to the strong electrostatic interaction and coordination bonding. However, after considering the solvent effect, four structures of 9H-Ag3, 9H-Ag1, 9H-Ag7, and 7H-Ag3 become more stable, three of which consist of the canonical adenine due to the weakening of electrostatic interaction between adenine and silver ion. Though adenine is inclined to keep its canonical form in aqueous solution, it is worth noting that the 7H-Ag3 tautomer still has a relatively lower energy comparable to the others.

ARTICLE

After analysis of thermodynamical parameters of different adenine Ag+ complexes, we find that the formation of [7HAg3]22+ is thermodynamically favorable in aqueous solution, which is similar to the structure of crystallographic measurements. We further confirm this structure by comparing simulated and experimental Raman spectra of the complexes formed by adenine with silver ions in different pH solutions. Finally, we also predicted the UV visible adsorption spectra of these stable complexes. Getting the stable structures of the 7H-Ag3 dimer complex in aqueous solution indicates that Ag+ indeed induces the tautomerization of adenine no matter whether in the gas phase or in aqueous solution. Furthermore, our present combination study of DFT calculations with Raman spectroscopy can be used to make clear the binding interaction and to explain abnormal peaks in the SERS of adenine on silver substrates.

’ ASSOCIATED CONTENT

bS

Supporting Information. Tables 1S and 2S showing the assignments of N3H and the structural parameters of N9H and N7H with different solvation models, respectively. The simulated Raman spectra of N7H with an explicit solvent water model and the comparison of Raman spectra of [9H-Ag3], [9H-Ag3][NO3 ], [7H-Ag3]22+ and [7H-Ag3]2[NO3]2. This material is available free of charge via the Internet at http://pubs.acs.org.

’ AUTHOR INFORMATION Corresponding Author

*E-mail: [email protected].

’ ACKNOWLEDGMENT We are grateful for the financial support of this work by the NSF of China (Nos. 20973143, 21021002, and 91027009), National Basic Research Programs (Nos. 2007CB815303 and 2009CB930703) and Xiamen University (Nos. 2010121020). D.-Y.W is grateful for the support from HPC of Xiamen University. ’ REFERENCES (1) Kneipp, K.; Kneipp, H.; Kartha, V. B.; Manoharan, R.; Deinum, G.; Itzkan, I.; Dasari, R. R.; Feld, M. S. Phys. Rev. E 1998, 57, R6281. (2) Maruyama, Y.; Ishikawa, M.; Futamata, M. Chem. Lett. 2001, 30, 834. (3) Barhoumi, A.; Zhang, D.; Tam, F.; Halas, N. J. J. Am. Chem. Soc. 2008, 130, 5523. (4) Otto, C.; Hoeben, F. P.; Greve, J. J. Raman Spectrosc. 1991, 22, 791. (5) Otto, C.; Mul, F. F. M. d.; Huizinga, A.; Greve, J. J. Phys. Chem. 1988, 92, 1239. (6) Otto, C.; Tweel, T. J. J. v. d.; Mul, F. F. M. d.; Greve, J. J. Raman Spectrosc. 1986, 17, 289. (7) Suh, J. S.; Moskovits, M. J. Am. Chem. Soc. 1986, 108, 4711. (8) Muniz-Miranda, M.; Gellini, C.; Pagliai, M.; Massimo, I.; Salvi, P. R.; Schettino, V. J. Phys. Chem. C 2010, 114, 13730. (9) Bell, S. E. J.; Sirimuthu, N. M. S. J. Am. Chem. Soc. 2006, 128, 15580. (10) Papadopoulou, E.; Bell, S. E. J. Analyst. 2010, 135, 3034. (11) Papadopoulou, E.; Bell, S. E. J. J. Phys. Chem. C 2010, 114, 22644. (12) Lehninger, A. L.; Nelson, D. L.; Cox, M. M. Principles of Biochemistry; Worth Publishers: New York, 1993. (13) Sigel, H. Chem. Soc. Rev. 1993, 22, 255. 13749


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Tautomerization, Solvent Effect and Binding ... - ACS Publications

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