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Article Cite This: ACS Omega 2018, 3, 12936−12943
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Energetics and Vibrational Signatures of Nucleobase Argyrophilic Interactions Suhwan Paul Lee,†,§ Sarah N. Johnson,† Thomas L. Ellington,† Nasrin Mirsaleh-Kohan,‡ and Gregory S. Tschumper*,† †
Department of Chemistry and Biochemistry, University of Mississippi, University, Mississippi 38677-1848, United States Department of Chemistry and Biochemistry, Texas Woman’s University, Denton, Texas 76204, United States
‡
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S Supporting Information *
ABSTRACT: This study investigates the interactions of both purine (adenine and guanine) and pyrimidine (cytosine, thymine, and uracil) nucleobases with a pair of silver atoms (Ag2). Full geometry optimizations were performed on several structures of each nucleobase/Ag2 complex and the corresponding isolated monomers using the M06-2X density functional with a correlation consistent triple-ζ basis set augmented with diffuse functions on all atoms and a relativistic pseudopotential on Ag (aug-cc-pVTZ for H, C, N, and O and aug-cc-pVTZ-PP for Ag; denoted aVTZ). Harmonic vibrational frequency computations indicate that each optimized structure corresponds to a minimum on the M06-2X/aVTZ potential energy surface. Relative electronic energies for interactions between Ag2 and each nucleobase were compared to elucidate energetic differences between isomers. Further analysis of the changes in vibrational frequencies, infrared intensities, and Raman scattering activities reveals how different Ag2 binding sites might be differentiated spectroscopically. These results provide molecular-level insight into the interactions between nucleobases and silver, which may lead to better understanding and interpretation of surface-enhanced Raman spectroscopy experiments on nucleobases and related systems.
1. INTRODUCTION
Fortunately, these issues can sometimes be circumvented via surface-enhanced Raman spectroscopy (SERS). First discovered in 1974 through pyridine adsorption at a silver electrode, SERS provides an attractive solution for weak scattering in many cases.19 Upon binding of a molecule onto a specially prepared metal surface or nanoparticle, such as silver or gold, the weak Raman activity can be greatly enhanced (by up to a factor of 1014). This optical enhancement can even provide sufficient sensitivity for single-molecule detection.15,20−28 These enhancement factors facilitate the acquisition of high-resolution vibrational spectra of biomolecules from very dilute aqueous solutions down to 10−8 M.13,16,29−36 As such, the detection and identification of nucleotides have become possible due to the unique SERS spectra of nucleobases.12,22,29,37−52 Although these nucleobases can exist in different tautomeric forms, Figure 1 depicts the structures studied here that are typically found in DNA and RNA53,54 along with the common numbering convention for the ring atoms that has been adopted for this work. Unlike pyridine, multiple adsorption sites are available in the nucleobases, leading to greater
The groundbreaking scientific research to determine the structures of DNA and RNA spanned several decades from the first discovery of nucleic acids by Miescher to the famous double helix model by Watson and Crick using Franklin’s Xray crystallography work.1−3 These nucleotides are composed of a phosphate group, a pentose sugar (ribose for RNA and deoxyribose for DNA), and one of five nucleobases. The latter is classified as either purine-based (adenine and guanine) or pyrimidine-based (cytosine, thymine, and uracil) and are the only varying component of nucleotides. Because they encode genetic information and are involved in many cellular processes, the ability to detect and identify the individual nucleobases is a significant asset to many fields of science, such as biology, biochemistry, analytical chemistry, and medicine.4−8 Raman spectroscopy serves as a powerful analytical tool that can provide molecular fingerprints for vibrational modes that cause an appreciable change in the polarizability of the molecule.9−15 Sensitivity, however, can sometimes be an issue because the technique relies on relatively rare inelastic scattering events. For example, the characterization of biomolecules with this technique becomes challenging when concentrations and/or scattering cross-sections are low.14,16−18 © 2018 American Chemical Society
Received: August 3, 2018 Accepted: September 27, 2018 Published: October 10, 2018 12936
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Figure 1. Structures of the isolated nucleobases and the numbering convention for atoms in their rings.
complexity surrounding the spectral interpretation from SERS experiments. The position and magnitude of the Raman peaks depend on the detailed interactions between the nucleobases and metal substrate.55−63 To provide detailed molecular-level insight into this phenomenon, the present study employs density functional theory (DFT) to probe the strength of the interactions between a pair of silver atoms (Ag2) and the various binding sites on each nucleobase. In addition, the resulting perturbations to the IR and Raman spectra are also computed to help discern the vibrational signatures associated to each binding site of each nucleobase. This small Ag2 model has been shown to reliably capture the key trends in the binding energetics and spectra because the site of adsorption is typically considered more important than the number of silver atoms at that site.17,25,56,64 Further, the enhancement mechanism and intermolecular distance dependence are similar for small and large Ag clusters.17,25,37,56,64,65
value of all of the complexes, whereas the relative energies (ΔE) effectively do the same thing for each nucleobase individually rather than collectively. All computations were performed using analytic gradients and Hessians available in the Gaussian09 software package.71 Pure angular momentum (5d, 7f, etc) atomic orbital basis functions were used in place of their Cartesian counterparts (6d, 10f, etc.) functions. Additionally, a pruned numerical integration grid having 99 radial shells and 590 angular points per shell was adopted. All electronic energies were converged to at least 1.0 × 10−10 Eh, and the maximum Cartesian forces in the optimized structures were below 1.2 × 10−5 Eh au−1.
3. RESULTS AND DISCUSSION 3.1. Structures and Energetics. There are a variety of interactions between Ag2 and electron-rich regions of the nucleobases (i.e., π, N, and O). The adsorption process is thought to involve an interaction of the π−electron system of the heteroaromatic ring with a silver electrode.72 Nevertheless, all initial structures collapsed during the geometry optimization procedure to those depicted in Figure 2, all of which exhibit either N or O contacts with the Ag2 unit. The optimized Cartesian coordinates of the nucleobase structures and nucleobase/Ag2 complexes are reported in the Supporting Information. Using these structures, intermolecular distances, defined by the shortest distance between one of the Ag atoms and a nucleobase atom, were computed and are denoted by the dashed lines in each structure in Figure 2. Table 1 compares electronic binding energies (Ebind), relative electronic energies (ΔE), relative electronic binding energies (ΔEbind), and intermolecular distances (R) of each nucleobase/Ag2 complex shown in Figure 2. In the cytosine/ Ag2 complex, three potential binding sites were identified, all of which show substantial differences in their electronic energetics. The site with the Ag2 interacting with the sp2 hybridized N (N3) exhibits the strongest binding (Ebind = −17.4 kcal mol−1). The binding at the sp2 hybridized O site is 3 kcal mol−1 higher and the sp3 NH2@C4 site is more than 9
2. COMPUTATIONAL DETAILS Full geometry optimizations were performed on several structures of each nucleobase/Ag2 complex and the corresponding isolated fragments using the global hybrid M06-2X density functional66 with a correlation consistent triple-ζ basis set augmented with diffuse functions on all atoms and a relativistic pseudopotential on Ag centers (aug-cc-pVTZ for H, C, N, and O and aug-cc-pVTZ-PP for Ag; denoted aVTZ).67−70 Harmonic vibrational frequencies (ω), IR intensities, and Raman scattering activities (RA) were computed to confirm that each optimized structure corresponds to a minimum (ni = 0) on the M06-2X/aVTZ potential energy surface and to investigate changes in the vibrational spectra of the nucleobase induced by complex formation. The electronic energies of the fully optimized minima have been used to quantify the strength of the various interactions between the Ag2 unit and the nucleobases. The binding energy (Ebind) is defined as the energy of a particular nucleobase/Ag2 complex relative to the isolated fragments (Ebind = Ecomplex − Enucleobase − EAg2). The relative binding energies (ΔEbind) compare all binding energies to the largest magnitude Ebind 12937
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Figure 2. Structures of each nucleobase/Ag2 complex with varying binding sites.
kcal mol−1 higher when compared to that of the N3 site, as indicated by the ΔE values in column 4. This large energetic difference among the three possible binding sites in the cytosine/Ag2 complexes indicates that the silver will most likely to bind to the N3 site of cytosine. As seen in the last column of Table 1, the intermolecular distance for the N3 and sp2 O site are similar (around 2.34 Å), where the sp3 N site is 0.16 Å longer than that of the N3 site. These trends in Ebind, ΔE, and R are not unique to cytosine/Ag2 and can also be seen in adenine/Ag2 and guanine/Ag2 complexes, as discussed below in the following paragraphs. Four potential binding sites were identified in the adenine/ Ag2 complexes seen in the first row of Figure 2. Similar to that of cytosine/Ag2, the site with Ag2 interacting with N3 exhibits
the strongest binding (Ebind = −15.4 kcal mol−1). However, all of the sp2 hybridized N binding sites (N3, N1, and N7) have very similar electronic energies and fall within ±0.5 kcal mol−1 of each other (i.e., ΔE = 1 kcal mol−1). The out-of-plane binding at the sp3 N (NH2@C6), on the other hand, is 7 kcal mol−1 higher in energy than that of the sp2-hybridized N binding sites. In addition, the intermolecular distance for the NH2 site increases by around 0.15 Å when compared to that of the more energetically competitive binding sites (2.33−2.35 Å). As previously discussed for the cytosine/Ag2 and adenine/ Ag2 complexes, the guanine/Ag2 complex exhibits the strongest binding at the sp2 hybridized N sites (Ebind = −14 kcal mol−1 at N3 and −15 kcal mol−1 at N7) with nearly identical R values 12938
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mol−1 and an R value of 2.50 Å, when compared to 2.35 or 2.36 Å for the other binding sites. All of the binding sites identified for thymine/Ag2 and uracil/Ag2 have similar relative electronic energies (ΔE ≤ 1.4 kcal mol−1 for both nucleobase/Ag2 complexes). This is due to the absence of sp2- or sp3-hybridized N site, which limits nucleobase/Ag2 interactions to sp2-hybridized O at C2 and C4 (rows 4 and 5 of Figure 2). In a similar fashion, the intermolecular distances across all binding motifs are virtually identical with R values at either 2.38 or 2.39 Å for the thymine/Ag2 and uracil/Ag2 complexes. The Ebind column in Table 1 indicates that the strongest interaction between the Ag2 unit and any of these five nucleobases occurs at the N3 site of cytosine. This reference value of Ebind = −17.7 kcal mol−1 is used to define the relative binding energies (ΔEbind) that are also reported in column 5 of Table 1. These ΔEbind values provide a convenient comparison of the competitive binding energetics between the different nucleobases in contrast to ΔE, which quantifies the competitive binding energetics between different sites within the same nucleobase. The data in the penultimate column of Table 1 help highlight that even though adenine and guanine can bind the Ag2 unit by more than −15 kcal mol −1 electronically, those interactions are more than 2 kcal mol−1 weaker than at the N3 sight of cytosine. Similarly, thymine and uracil exhibit appreciable electronic binding energies (Ebind = −10.4 ± 0.9 kcal mol−1), but the corresponding ΔEbind values show that the binding is at least 6.1 kcal mol−1 weaker than the reference value for Ag2 binding to cytosine at the N3 position, as shown in Figure 2. These relative electronic binding energies suggest the likelihood of binding silver in a competitive environment should decrease in the following order: cytosine > adenine ≈ guanine > thymine ≈ uracil.
Table 1. Electronic Binding Energies, Relative Energies, and Relative Binding Energies (Ebind, ΔE, and ΔEbind in kcal mol−1) of Nucleobase/Ag2 Complexes with Varying Binding Sites Computed at the M06-2X/aVTZ Level of Theory as Well as Intermolecular Distances (R in Å) Denoted by the Dashed Lines in Figure 2 nucleobase
binding site
Ebind
ΔE
ΔEbind
R
cytosine
N3 O@C2 NH2@C4 N3 N1 N7 NH2@C6 N7 N3 O@C6 NH2@C2 O@C2/N1 O@C4/C5 O@C4/N3 O@C2/N3 O@C2/N1 O@C4/C5 O@C4/N3 O@C2/N3
−17.4 −14.4 −7.7 −15.4 −15.2 −14.8 −8.2 −15.1 −14.0 −13.6 −7.4 −11.3 −10.7 −10.3 −9.9 −10.9 −10.6 −10.2 −9.5
0.0 +3.0 +9.7 0.0 +0.2 +0.6 +7.2 0.0 +1.1 +1.4 +7.7 0.0 +0.6 +1.0 +1.4 0.0 +0.3 +0.7 +1.4
0.0 +3.0 +9.7 +2.0 +2.2 +2.6 +9.2 +2.3 +3.4 +3.8 +10.0 +6.1 +7.7 +7.1 +7.5 +6.5 +6.8 +7.2 +7.9
2.35 2.33 2.51 2.34 2.35 2.33 2.50 2.35 2.35 2.36 2.50 2.39 2.38 2.38 2.38 2.39 2.39 2.38 2.39
adenine
guanine
thymine
uracil
for both of these structures. The sp2 O@C6 binding site exhibits binding similar to the sp2 O site available in cytosine with Ebind approaching −14 kcal mol−1. The sp3 N (NH2@C2) is again the weakest binding site, with a Ebind of only −7.4 kcal
Table 2. Vibrational Signatures of Isolated Nucleobases and Nucleobase/Ag2 Complexes Computed at the M06-2X/aVTZ Level of Theorya
Selected harmonic vibrational frequencies (ω in cm−1), Raman scattering activities (RA in Å4 amu−1), and corresponding changes upon complexation (Δω and ΔRA), respectively. a
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the −76 cm−1 frequency shift predicted for the cytosine/Ag2 complexes. Additionally, a mode at 1342 cm−1 can be described as the wagging motion of the NH group nearest to the carbonyl. When Ag2 binds to the O@C6 site, the frequency and Raman activity both increase by +31 cm−1 and +61 Å4 amu−1, respectively. The N7 binding site can be differentiated through a solitary increase in frequency (+15 cm−1) of the 1081 cm−1 mode upon Ag2 binding, which consists of stretching of the five-membered ring. The N3 binding site, on the other hand, can be distinguished through the frequency shift of +18 cm−1 for the 845 cm−1 mode. In the thymine/Ag2 complex, the mode at 1840 cm−1 corresponds to the C2O stretching, whereas the C4O stretching is predicted to be at 1806 cm−1. When Ag2 binds to either of the two binding sites present at the oxygen atom involved in CO stretching, the frequency significantly decreases (approximately −60 cm−1), whereas the Raman activity is notably enhanced for both sites. When Ag2 binds to the oxygen atom not involved in the CO stretching, the mode shifts to higher energy (approximately +15 cm−1), whereas the Raman activity is only slightly affected. Experimentally, the SERS spectra of cytosine and uracil have been found to be similar due to the same pyrimidine moiety and a similar geometry on the surface.76 Additionally, the aforementioned trends in the thymine/Ag2 complex apply directly to all of the uracil/Ag2 complex modes, especially the carbonyl stretches at 1846 and 1821 cm−1.
3.2. Vibrational Signatures. Table 2 shows the vibrational frequencies (ω), Raman scattering activities (RA), and the corresponding changes (Δω and ΔRA, respectively) associated to each nucleobase/Ag2 complex depicted in Figure 2. The sp3-hybridized N binding sites for cytosine/Ag2, adenine/Ag2, and guanine/Ag2 have been omitted from the following discussion due to their large relative energies (ΔE > +7.5 kcal mol−1). However, all frequencies and Raman activities are reported in the Supporting Information. Vibrational modes in the spectral region of 800−2000 cm−1 have been found to contain a significant amount of vibrational information about nucleobases73 and tend to produce intense Raman bands corresponding to the motion of nonhydrogen atoms. In addition, this region has been found to be the most effective at reproducing experimental frequency shifts in a previous study of pyrimidine and its interactions with Ag2 and H2O molecules using the same level of theory utilized here (M06-2X/aVTZ).17 Additional factors also influence both the enhancement and the shifts of the Raman peaks in SERS experiments, including the shape of the substrate/nanoparticle, the dielectric constant of the material, and the surrounding medium (solvent and other solute particles). These and other effects, such as anharmonicity, complicate any direct comparison between computational and experimental spectra, which is why previous attempts to do so have met with varying degrees of success.23−25 As noted in the previous section, the binding energies of the cytosine/Ag2 complex are well resolved for the different binding sites, and this feature extends to the corresponding vibrational signatures. Each of the six modes listed in Table 2 exhibits an appreciable change in the vibrational frequency (Δω) and/or Raman scattering activity (ΔRA). The RA of the N1−H wagging mode at 1454 cm−1, for example, is significantly enhanced by more than an order of magnitude when Ag2 binds to the O@C2 site. However, there is no substantial enhancement of this mode when Ag2 binds to the N3 site. The CO stretching mode of the cytosine monomer at 1815 cm−1 decreases in frequency by −76 cm−1 and increases in Raman activity by +102 Å4 amu−1 when Ag2 binds to the O@C2 site. In several experiments, this behavior was attributed to a decrease in the double bond character of the carbonyl group as electrons are donated to the silver surface.25,74,75 The same phenomenon in the carbonyl stretching modes is also predicted in guanine/Ag2, thymine/ Ag2, and uracil/Ag2 complexes and is discussed below. Experimentally, the presence of a decrease in frequency and enhancement in Raman activity of the CO stretching band revealed the proximity of the carbonyl group to the silver surface.74 In the adenine/Ag2 complex, a synchronous C2N1/C2N3 stretching mode within the pyrimidine ring is predicted at 906 cm−1. When Ag2 binds to the N1 or N3 site, there is an increase in frequency (+11 and +18 cm−1, respectively), but when Ag2 binds to the N7 site no change in frequency or Raman activity is exhibited. An asynchronous C2N1/C2N3 stretching mode is predicted at 1340 cm−1, where a similar change could be expected upon Ag2 binding. Indeed, a shift to higher energy (+18 cm−1) is predicted when Ag2 binds to the N1 site. However, there is essentially no frequency shift (+1 cm−1) when Ag2 binds to the N3 site. In the guanine/Ag2 complex, a CO stretching mode at 1841 cm−1 experiences a substantial shift to lower energy (−73 cm−1) when Ag2 binds to the O@C6 site, which is similar to
4. CONCLUSIONS A DFT analysis of the intermolecular interaction between each nucleobase and a pair of silver atoms along with the concurrent perturbations to their Raman spectra have been presented in this work. All geometry optimizations of a wide range of initial structures collapsed to minima, in which the Ag2 unit was bound to either an N or O atom (Figure 2). For all purine- and pyrimidine-based nucleobase/Ag2 complexes, intermolecular separations (R) range from 2.33 to 2.39 Å for all sp2 contacts and 2.50−2.51 Å for the sp3 contacts. The electronic binding energies of these complexes are significant and range from −7.4 to −17.4 kcal mol−1. With only sp2 O binding sites available in thymine and uracil, the Ebind values are very similar and only span a narrow range of −10.4 ± 0.9 kcal mol−1. In contrast, the other three nucleobases have very different binding energies (by as much as 10.0 kcal mol−1) for the sp2 O, sp2 N, and sp3 N sites that can bind Ag2. Binding is consistently weakest between the Ag2 fragment and the sp3 N atoms of the amino groups in cytosine, adenine, and guanine, and it is consistently the strongest to the sp2 N atoms. These results imply the following trend for the relative binding strengths of the different Ag2 binding sites within a given nucleobase: sp2 N > sp2 O ≫ sp3 N. The computed electronic binding energies also reveal that cytosine binds Ag2 more strongly than the other nucleobases by at least 2.0 kcal mol−1, whereas thymine and uracil bind it more weakly than the others by at least 3.8 kcal mol−1, which leads to the following relative binding strengths: cytosine > adenine ≈ guanine ≫ thymine ≈ uracil. Perturbations to the Raman spectra of the nucleobases from Ag2 binding were also examined. When Ag2 binds to the O or N atom of the nucleobases, certain vibrational modes shift to higher energy (blue shift) by up to +34 cm−1, whereas others shift to lower energy (red shift) by as much as −76 cm−1. The Raman scattering activities of many modes also increase appreciably when certain complexes form, but the enhance12940
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nucleobases - adenine as a case-study. New J. Chem. 2013, 37, 2691− 2699. (8) Shang, Z.-G.; Ting, D.-N.; Wong, Y.-T.; Tan, Y.-C.; Ying, B.; Mo, Y.-J. A study of DFT and surface enhanced Raman scattering in silver colloids for thymine. J. Mol. Struct. 2007, 826, 64−67. (9) Raman, C. V.; Krishnan, K. S. A new type of secondary radiation. Nature 1928, 121, 501−502. (10) Raman, C. V. A new radiation. Indian J. Phys. 1928, 2, 387− 398. (11) Placzek, G. The theory of the Raman effect. Z. Phys. 1929, 58, 585−594. (12) Kneipp, K.; Kneipp, H.; Itzkan, I.; Dasari, R. R.; Feld, M. S. Surface-enhanced Raman scattering and biophysics. J. Phys.: Condens. Matter 2002, 14, R597−R624. (13) Rasmussen, A.; Deckert, V. Surface- and tip-enhanced Raman scattering of DNA components. J. Raman Spectrosc. 2006, 37, 311− 317. (14) Muniz-Miranda, M.; Gellini, C.; Pagliai, M.; Innocenti, M.; Salvi, P. R.; Schettino, V. SERS and Computational Studies on MicroRNA Chains Adsorbed on Silver Surfaces. J. Phys. Chem. C 2010, 114, 13730−13735. (15) Valley, N.; Greeneltch, N.; Duyne, R. P. V.; Schatz, G. C. A Look at the Origin and Magnitude of the Chemical Contribution to the Enhancement Mechanism of Surface-Enhanced Raman Spectroscopy (SERS): Theory and Experiment. J. Phys. Chem. Lett. 2013, 4, 2599−2604. (16) Koglin, E.; Séquaris, J. M. Surface Enhanced Raman Scattering of Biomolecules. Top. Curr. Chem. 1986, 134, 1−57. (17) Kelly, J. T.; McClellan, A. K.; Joe, L. V.; Wright, A. M.; Lloyd, L. T.; Tschumper, G. S.; Hammer, N. I. Competition between Hydrophilic and Argyrophilic Interactions in Surface Enhanced Raman Spectroscopy. ChemPhysChem 2016, 17, 2782−2786. (18) Otto, C.; van den Tweel, T. J. J.; de Mul, F. F. M.; Greve, J. Surface-Enhanced Raman Spectroscopy of DNA Bases. J. Raman Spectrosc. 1986, 17, 289−298. (19) Fleischmann, M.; Hendra, P. J.; McQuillan, A. J. Raman Spectra of Pyridine Adsorbed at a Silver Electrode. Chem. Phys. Lett. 1974, 26, 163−166. (20) Koglin, E.; Séquaris, J. M.; Fritz, J. C.; Valenta, P. Surface Enhanced Raman Scattering (SERS) of Nucleic Acid Bases Adsorbed on Silver Colloids. J. Mol. Struct. 1984, 114, 219−223. (21) Campion, A.; Kambhampati, P. Surface-enhanced Raman scattering. Chem. Soc. Rev. 1998, 27, 241−250. (22) Kneipp, K.; Kneipp, H.; Kartha, V. B.; Manoharan, R.; Deinum, G.; Itzkan, I.; Dasari, R. R.; Feld, M. S. Detection and identification of a single DNA base molecule using surface-enhanced Raman scattering (SERS). Phys. Rev. E 1998, 57, R6281−R6284. (23) Giese, B.; McNaughton, D. Surface-Enhanced Raman Spectroscopic and Density Functional Theory Study of Adenine Adsorption to Silver Surfaces. J. Phys. Chem. B 2002, 106, 101−112. (24) Giese, B.; McNaughton, D. Density functional theoretical (DFT) and surface-enhanced Raman spectroscopic study of guanine and its alkylated derivatives. Part 1. DFT calculations on neutral, protonated and deprotonated guanine. Phys. Chem. Chem. Phys. 2002, 4, 5161−5170. (25) Giese, B.; McNaughton, D. Density functional theoretical (DFT) and surface-enhanced Raman spectroscopic study of guanine and its alkylated derivatives. Part 2: Surface-enhanced Raman scattering on silver surfaces. Phys. Chem. Chem. Phys. 2002, 4, 5171−5182. (26) Aikens, C. M.; Schatz, G. C. TDDFT Studies of Absorption and SERS Spectra of Pyridine Interacting with Au20. J. Phys. Chem. A 2006, 110, 13317−13324. (27) Bhunia, S.; Forster, S.; Vyas, N.; Schmitt, H.-C.; Ojha, A. K. Direct visual evidence of end-on adsorption geometry of pyridine on silver surface investigated by surface enhanced Raman scattering and density functional theory calculations. Spectrochim. Acta, Part A 2015, 151, 888−894.
ment is less than 2 orders of magnitude suggesting the simple Ag2 unit is not large enough to completely capture that effect of the SERS substrate. Nevertheless, the results presented here suggest that these differences could be used to discriminate between particular binding motifs between the nucleobases and silver. Direct comparison to experiment, however, will require consideration of various environmental effects, such as the solvent and other solute particles.
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ASSOCIATED CONTENT
* Supporting Information S
The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acsomega.8b01895.
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Harmonic vibrational frequencies; infrared intensities; Raman activities and Cartesian coordinates for all optimized structures are provided at the M06-2X/ aVTZ level of theory (PDF)
AUTHOR INFORMATION
Corresponding Author
*E-mail:
[email protected]. Tel: +1 662 915 7301. Fax: +1 662 915 7300. ORCID
Suhwan Paul Lee: 0000-0003-2658-4641 Nasrin Mirsaleh-Kohan: 0000-0001-9655-9711 Gregory S. Tschumper: 0000-0002-3933-2200 Present Address §
NIH-NINDS, 35A Convent Drive, Room 3D-908H, Bethesda, MD 20892, United States (S.P.L.). Notes
The authors declare no competing financial interest.
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ACKNOWLEDGMENTS This work was supported in part by the National Science Foundation (CHE-1338056 and CHE-1664998) and the Mississippi Center for Supercomputing Research (MCSR) for generous allocation of their computational resources. Katelyn M. Dreux and Hailey B. Reed at the University of Mississippi are thanked for helpful discussions and technical expertise.
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REFERENCES
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DOI: 10.1021/acsomega.8b01895 ACS Omega 2018, 3, 12936−12943
