Spectrochimica Acta Part A: Molecular and Biomolecular Spectroscopy 136 (2015) 979–985

Contents lists available at ScienceDirect

Spectrochimica Acta Part A: Molecular and Biomolecular Spectroscopy journal homepage: www.elsevier.com/locate/saa

Adsorption study of antibiotics on silver nanoparticle surfaces by surface-enhanced Raman scattering spectroscopy Aline Luciano Filgueiras a, Diego Paschoal b, Hélio F. Dos Santos b, Antonio C. Sant’Ana a,⇑ a b

Laboratório de Nanoestruturas Plasmônicas (LabNano), Departamento de Química, ICE, Universidade Federal de Juiz de Fora, 36036-900 Juiz de Fora, MG, Brazil Núcleo de Estudos em Química computacional (NEQC), Departamento de Química, ICE, Universidade Federal de Juiz de Fora, 36036-900 Juiz de Fora, MG, Brazil

h i g h l i g h t s

g r a p h i c a l a b s t r a c t

 Levofloxacin adsorbs strongly on

The adsorption geometries of the antibiotics tetracycline, levofloxacin and benzylpenicillin on the surfaces of silver nanoparticles were investigated by SERS spectroscopy.

silver surface by carboxylate moiety.  Tetracycline adsorbs strongly on silver surface by carbonyl and hydroxyl moieties.  Benzylpenicillin adsorbs weakly on silver surface by carbonyl from acyclic amide.  SERS spectroscopy is outstanding technique for molecular adsorption analysis.

a r t i c l e

i n f o

Article history: Received 24 July 2014 Received in revised form 23 September 2014 Accepted 25 September 2014 Available online 5 October 2014 Keywords: Antimicrobial Biomolecules Synergy Chemisorption Resistant bacteria

a b s t r a c t In this work the adsorption of the antibiotics levofloxacin (LV), tetracycline (TC) and benzylpenicillin (BP) on the surface of silver nanoparticles (AgNP) have been investigated through both surface-enhanced Raman scattering (SERS) and UV–VIS–NIR spectroscopies. The SERS spectra were obtained using 1064 nm exciting radiation. Theoretical models for the antibiotic molecules were obtained from DFT calculations, and used in the vibrational assignment. The adsorption geometries were proposed based on the changes in the spectral patterns. The LV compound adsorbs through carboxylate group, TC compound interacts with silver atoms through carbonyl from intermediate ring, and BP compound adsorbs by carbonyl moieties from carboxylate and acyclic amide. Ó 2014 Elsevier B.V. All rights reserved.

Introduction The surface-enhanced Raman scattering (SERS) effect is responsible for the enhancement of Raman signal of molecules adsorbed on metallic nanostructures. The enhancing factor can attain 1011 ⇑ Corresponding author. Tel.: +55 32 2102 3310. E-mail address: [email protected] (A.C. Sant’Ana). http://dx.doi.org/10.1016/j.saa.2014.09.120 1386-1425/Ó 2014 Elsevier B.V. All rights reserved.

times [1–4], allowing to obtain SERS spectrum from very diluted solutions. The signal enhancement is explained by two mechanisms: the electromagnetic one, by which the interaction of light with metallic nanoparticles produces large amplifications of the electric field on the surface through electronic excitations known as localized surface plasmon resonance [5–14], and the chemical one, which implies in a resonance involving a photon assisted charge transfer process [15–18]. The interpretation of SERS

980

A.L. Filgueiras et al. / Spectrochimica Acta Part A: Molecular and Biomolecular Spectroscopy 136 (2015) 979–985

spectrum gives information about the orientation of molecules on the metallic surfaces in submonolayer regime, the molecular moieties involved in such interaction, and how strong is the adsorption process [19–23]. In the last decades antibiotics have been losing effectiveness due to the emergence of biological resistance [24–26]. Such problem leads to demand for the development of new strategies for the treatment of infections [25]. The use of silver nanoparticles (AgNP), which are known by the antibacterial properties [27–31] in association with antibiotic drugs can be an alternative for such treatments [32,33]. The knowledge of the molecular sites that are interacting with the metallic surface allows inferring if the mechanism of action of the drug is preserved or not. In another way the intensity of the interaction of the molecule with the silver surface could be useful for estimate the capability of AgNP to act as a vehicle for drug delivery as well as to facilitate the drug entrance through cell walls and membranes [34]. In suitable conditions, the antibiotic activity could be enhanced by silver nanoparticles in the biological medium [35]. In this way, SERS spectroscopy is an outstanding technique for investigations of the surface interactions of organic compounds on metallic surfaces. In this work SERS spectroscopy have been using aiming to obtain information about the adsorption of the antibiotics levofloxacin (LV), tetracycline (TC) and benzylpenicillin (BP) on silver surface for understanding some additive or synergic antibacterial effects observed in vitro in our previous results [36]. The antibiotic LV is a fluoroquinolone compound, with broad action range against Gram-positive and Gram-negative bacteria, and such class of antibiotics acts by inhibition of DNA synthesis [37]. The mechanism is not completely known, but possibly involves interactions with fluorine and others lateral structures around aromatic nucleus [38,39]. Copper(II)–LV complex involving coordination by carboxylic moiety, presented enhanced antibacterial activity [40,41]. In another system, gold(III)–LV complex, formed by coordination through piperazine moiety, presents anticancer properties [42]. The antibiotic TC has a mechanism of antibacterial action involving the presence of dimethylamine moiety [43]. Such a compound forms complexes with different metals as platinum(II) [44], palladium [45] or copper(II) [32,46], changing its chemical properties, and being used in biological applications such as anticancer action [44,47], DNA interactions [32], and antimicrobial activity against resistant bacteria [48–50]. The antibiotic BP has the beta-lactam ring as the biological active site, acting through inhibiting of protein syntheses, which are necessary for the formation of bacterial cell wall [51]. Complexes involving beta-lactam ring have been synthesized and characterized by infrared spectroscopy, shown that such molecular moiety is an important interaction site with metals [52,53]. The SERS and resonance Raman spectra of some quinolones and the FTIR spectrum of LV, with vibrational assignments based on DFT calculations are reported [54–56]. The Raman, resonance Raman and FTIR spectra of TC, derivative species and metallic complexes, with the vibrational assignments have also been reported [44,48,57,58]. The Raman and FTIR spectra of beta-lactam ring compounds [52,59], as well as the SERS spectra of BP adsorbed on AgNP aqueous suspension or on silver electrode are reported [60–62], but the adsorption mechanism is yet no clear. In the present work it was studied the interaction of LV, TC and BP antibiotics, with AgNP through SERS experiments, with excitation in the near infrared. The vibrational assignment of each SERS spectrum was proposed based on DFT calculations of the compounds, in appropriate protonation states, taking into account the pKa values (Scheme 1). The results allowed inferring the molecular anchor sites, the adsorption geometries and the nature of the surface interaction forces. All assumptions on the interactions of the antibiotics with silver surface were also supported by UV–VIS–NIR

spectroscopy studies based on changes in the localized surface plasmon resonance (LSPR) features. Materials and methods Materials The chemicals sodium borohydride, trisodium citrate dihydrate, silver nitrate, BP, LV and TC were purchased from Sigma–Aldrich and used without additional purification. The deionized water with Milli-Q pattern (18.2 MX cm resistivity) was used in all aqueous solution preparation. All glass containers were cleaned using aqua regia (HCl:3HNO3) and copiously rinsed with deionized water. AgNP aqueous suspension preparation AgNP aqueous suspension was prepared as the synthesis of Creighton et al. [63], modified as described: 20 mL of 2.0  103 mol L1 of silver nitrate aqueous solution was added dropwise to 40 mL of 8.0  103 mol L1 sodium borohydride aqueous solution in ice bath, with continuous stirring, and 600 lL of 3.4  102 mol L1 trisodium citrate dihydrate aqueous solution was added after 30 min for stabilizing the AgNP suspension. The resultant colloidal suspension, with 9.8  104 mol L1 Ag concentration, was yellowish gray, has been used in SERS experiments when recently prepared. Conditions for obtaining spectroscopic results The UV–VIS–NIR spectra of adsorbates and AgNP aqueous suspensions were obtained in a Shimadzu spectrophotometer, model UV-1800, using 0.1 cm path length quartz cuvette. The SERS and Raman spectra were obtained from a Bruker spectrometer, model RFS-100, using a Nd3+/YAG laser line with wavelength at 1064 nm, coupled with a germanium detector, cooled with liquid nitrogen. The spectral resolution used in all Raman spectra was 4 cm1. The Raman spectra of the BP, TC, and LV in solid state were obtained with a 30 mW laser power, accumulated with typically 100 scans. The SERS spectra of antibiotics were obtained in silver aqueous suspension using 1.0  103 mol L1 concentration for TC and BP and 1.0  104 mol L1 for LV, and for all samples the pH remained around 6.0. In SERS experiments it was used a 500 mW laser power, accumulated with typically 200 scans. Several spectra were recorded in different points of the suspension to check the reproducibility. It was not observed any light–induced aggregation process at these accumulation conditions that was monitored by the stability of the SERS background [64,65]. Since the Raman signals from antibiotics solutions were rather weak, even in higher concentration, their contributions were not considered in the SERS spectra, for all analytes. Such discussion, together the Raman spectra of the analytes in aqueous solutions are presented in Supplementary Material. Computation details The geometries for the free ligands were fully optimized in gas phase and characterized as stationary points on the potential energy surface (PES) through harmonic frequency calculations at DFT level with the PBE1PBE functional [66] and LANL2DZ ECP basis set for Ag [67] atom and 6-31 + G(2d) [68] basis set for all other atoms. Raman spectra were calculated at the same level of theory and the frequencies and intensities [69] used as input to fit a Lorentzian function [70] in order to represent the band spectra. The main bands were assigned by visual inspection of the normal modes. All calculations were carried out using Gaussian 09 package, revision A.02 [71].

A.L. Filgueiras et al. / Spectrochimica Acta Part A: Molecular and Biomolecular Spectroscopy 136 (2015) 979–985

981

Scheme 1. Molecular structures of the investigated antibiotics, with the atomic labels, and optimized molecular models in the protonation states proposed for the adsorbed species.

Results and discussions Fig. 1 presents the UV–VIS–NIR spectra of the AgNP aqueous suspensions in the absence and presence of the antibiotics, and the absorption spectra of the antibiotics in aqueous solutions. In the spectrum of AgNP suspension the LSPR band has a maximum at 390 nm, assigned to dipole surface-plasmon transition from small nanoparticles, with typical dimension of ca. 5–20 nm [63]. Such a band has a broad shoulder, extended from ultraviolet to near-infrared region that can be ascribed to a broad AgNP size distribution (see Fig. S1, Supplementary Material). Such optical properties were suitable for the excitation of the localized surface plasmon in SERS experiments using 1064 nm exciting radiation, since the presence of AgNP with diameter ca. 100 nm are necessary for the resonance between surface plasmon transitions and the laser line. The presence of LV, TC and BP in the AgNP suspension, at millimolar concentrations induced small changes in the LSPR band preserving the spectral shape. This means that the aggregation of AgNP, induced by the adsorption, was not meaningful at this conditions and the resonance between surface plasmon transition and exciting radiation at 1064 nm was conserved. On the other hand, the interactions of LV and TC species with the surfaces of the AgNP lead to relevant spectral changes in both, the adsorption bands of the adsorbates and LSPR band of AgNP, allowing to infer chemisorption is present in both cases (see Fig. S2, Supplementary Material). All investigated antibiotics have acidic hydrogens and the protonated state of each species predominant in the medium is

strongly pH-dependent. LV antibiotic has two pKa values: 5.5, involving the deprotonation of the carboxylate group, and 7.4, involving the deprotonation of the ammonium group in the N15 atom (LVH+2 M LVH± M LV) [72], so the predominant species at pH = 6.0 is the zwitterionic species. TC compound has three pKa values: 3.3, involving the deprotonation of the hydroxyl from O11 atom, 7.7, involving the deprotonation of the hydroxyl from the O14 atom, and 9.7, involving the deprotonation of the ammonium group from N16 atom (TCH+3 M TCH±2 M TCH M TC2) [57], so the predominant species in solution in the SERS experiments is TCH±2. The pKa values of BP is 3.04 [73], involving the deprotonation of the carboxylate group (BPH M BP). Therefore the deprotonated species is predominant at AgNP suspension in the SERS conditions. Fig. 2 shows the observed Raman and SERS spectra of LV species. In the Raman spectrum, the presence of the band at 1710 cm1, assigned to the carbonyl from carboxylic acid, suggests such a group is protonated in the solid state. In the SERS spectrum the band observed at 1556 cm1 was assigned to the CO stretching mode of the carboxylate moiety. This wavenumber values is in agreement with proposal for bidentate quelate coordination based on spectral patterns of similar complexes [74], allowing to suggest carboxylate is the anchor site of LV adsorption. The band at 1698 cm1, observed in the Raman spectrum as a shoulder, assigned to the carbonyl from A ring, was not observed in the SERS spectrum due to the coupling with CC and CN stretching modes from A and B aromatic rings. The intense SERS bands at 1622, 1401, 1367, 1341, 1051, 785 and 550 cm1 have important contributions in the normal modes from

982

A.L. Filgueiras et al. / Spectrochimica Acta Part A: Molecular and Biomolecular Spectroscopy 136 (2015) 979–985

Fig. 1. UV–VIS–NIR spectra of the AgNP aqueous suspension in the absence and presence of the antibiotics, in the same concentration used in the SERS experiments, and the absorption spectra of the antibiotic in aqueous solutions (LV: 1.0  105 mol L1; TC and BP: 1.0  103 mol L1).

Fig. 2. (A) SERS spectrum of LVH± 1.0  104 mol L1 in AgNP aqueous suspension (k0 = 1064 nm); (B) Raman spectrum of LVH2+ in solid state; (k0 = 1064 nm);

CC, CN stretching vibrations from A and B rings. Considering the surface selection rules, such enhanced bands can be ascribed to the almost perpendicular orientation of these rings on the surface [75,76]. In despite of the hot spot be a small region in the junction of the AgNP, the intricate geometries of these sites preclude inferences about details of the surface, but certainly there is a component of the electrical field perpendicular to the surface at the molecular adsorption spot, responsible for changes in the spectral features. The SERS bands at 1556, 1341, 1051, 894, 785 and 550 cm1 have significant contribution in the normal modes from C2C3 and carboxylate stretching allowing to infer such molecular moieties are involved in the interaction with the metallic surface. The bands in the Raman spectrum at 1544, 1463, 1448, 1120 and 849 cm1 can be assigned to the normal modes involving contributions from piperazine moiety and angular deformation from CH2 and CH3 groups. This set of bands has its relative intensities decreased in

the SERS spectrum, reinforce that the ring D is not involved in the interaction with the metal. The SERS spectral pattern has considerable differences from the Raman spectrum of the solid compound which allows to suggest the formation of a surface complex, with carboxylate group been an anchor site. Such adsorption proposal is in agreement with adsorption model calculated by DFT, involving optimization of the geometry of LVH± and two silver atoms (see Fig. S8 in the Supplementary Materials). Table 1 (Supplementary Materials) presents vibrational assignments for the bands observed in the Raman and SERS spectra, based on the DFT calculation of the LVH+2 and LVH± compounds. Fig. 3 shows the Raman and SERS spectra of TC species. The more intense SERS bands at 1613, 1591 and 1563 cm1, assigned to the normal modes involving CC stretching from aromatic ring D and CO stretching from the carbonyl present in the ring C, allow suggesting this carbonyl group is involved in the interaction with the silver surface, been the anchor site of the adsorption. Such a hypothesis is reinforced since the SERS bands at 1613 and 1591 cm1 are shifted in relation to the Raman bands at 1624 and 1585 cm1, both with carbonyl stretching from C ring as component of the normal modes. In agreement with this adsorption proposal there are enhancements of the SERS bands at 1515, 1447, 1403, 1310, 1248, 1242, 1196, 1129 and 1065 cm1, which have in the normal modes the contributions of the vibrations from the hydroxyl of the ring D, as well as the stretching or bending of CC from rings D and C. Therefore, the oxygen atom O31 is probably in the proximity of the metallic surface and the rings D and C are almost perpendicular to the surface [75,76]. In the same way, the Raman bands at 1638, 1467 and 1292 cm1, assigned to modes composed of the vibrations from amine, amide and carbonyl groups from the ring A, have loss of intensity in the SERS spectrum, suggesting that such groups are not involved in the adsorption. Such SERS spectral pattern is very different from the obtained in the Raman of the solid compound that is a characteristic of strong adsorption, with the formation of a surface complex. Such adsorption proposal is in agreement with adsorption model calculated by DFT, involving optimization of the geometry of TCH±2

A.L. Filgueiras et al. / Spectrochimica Acta Part A: Molecular and Biomolecular Spectroscopy 136 (2015) 979–985

Fig. 3. (A) SERS spectrum of TCH±2 1.0  103 mol L1 in AgNP aqueous suspension (k0 = 1064 nm); Raman spectrum of TCH±2 in solid state (k0 = 1064 nm).

and two silver atoms (see Fig. S8 in the Supplementary Materials). Table 2 (Supplementary Materials) presents vibrational assignments for the bands observed in the Raman and SERS spectra, based on the DFT calculation of TCH±2 compound. Fig. 4 shows the Raman and SERS spectra of BP species. In the solid state the compound is protonated, as suggested by the presence of the Raman band at 1751 cm1, assigned to the carbonyl stretching mode of the carboxylic acid, and BPH was considered in the DFT calculation of the free compound. Besides the band at 1751 cm1, two others are assigned to carbonyl stretching at 1760 (shoulder) and 1661 cm1, from b-lactam ring and acyclic amide, respectively. In the SERS spectrum the band assigned to carbonyl stretching of the acyclic amide shifted to 1684 cm1 and a new band at 1655 cm1 was assigned to the carbonyl stretching from carboxylate group. Therefore, it can be claimed that the deprotonated BP anion adsorbs on the silver surface. Since the band at 1760 cm1, observed in the Raman spectrum of the solid material was not enhanced in the SERS spectrum, it can be inferred that the carbonyl from b-lactam ring is not interacting with the metallic surface. The presence of the shifted SERS bands at 1684, 1445 and 1202 cm1, assigned to the normal modes involving acyclic amide, as well as 1655 cm1, assigned to carboxylate group, suggests that such molecular moieties are involved in the interaction with the silver surface, probably through carbonyl groups. The intense SERS

Fig. 4. (A) SERS spectrum of BP 1.0  103 mol L1 in AgNP aqueous suspension (k0 = 1064 nm); (B) Raman spectrum of BPH in solid state (k0 = 1064 nm).

983

bands at 1603, 1585, 1031 and 1003 cm1, assigned to the CC stretching modes from phenyl moiety suggest the ring is almost perpendicular to the silver surface [75,76]. In both spectra, the more intense bands have preserved the relative intensities, allowing to infer the molecular polarizability has no significant changes due to the adsorption. Nevertheless, bands with low intensities present some changes in the SERS spectrum, as well as enlargement of bands were observed around 1100, 1450 and 1650 cm1 spectral regions. Such differences can be ascribed to the interaction of the molecule with the surface (see Fig. S6 in the Supplementary Materials). Such adsorption proposal is in agreement with adsorption model calculated by DFT, involving optimization of the geometry of BP with silver atoms (see Fig. S8 in the Supplementary Materials). In this way, the SERS and the Raman spectra can be rationalize as BP adsorbs weakly on silver surface, without coordination of Lewis base moieties with silver atoms. Such a hypothesis is reinforced also by the similarity of the pattern of the LSPR band of the silver suspension in the presence and absence of the antibiotic. Table 3 (Supplementary Materials) presents vibrational assignments for the bands observed in the Raman and SERS spectra, based on the DFT calculation of the BPH and BP compounds. The SERS spectra of BP are discussed in the literature by Iliescu et al. [60], Clarke et al. [62] and Reipa and Horvath [61] The first ones obtained the SERS of BP adsorbed on AgNP at relative high concentration (ca. 1  101 mol L1) and only after the addition of NaCl. Such approach leads to the occlusion of the molecule into clusters of AgNP, formed by the change of the ionic force of the suspension. The last one studied the adsorption on silver electrode, and obtained the SERS spectrum with applied potential that could induce different adsorption geometries. The SERS spectral patterns from BP presenting in these cited works are different between them and not equivalent with that here showed (Fig. 4A). The differences can be justified by the use of NaCl for aggregation of the nanoparticle suspensions or the use of applied potential. In this way, the results here presented can be ascribed to a free adsorption, which is week as suggested by the similarity of spectra of the Fig. 4 and the small changes in the UV–VIS–NIR spectrum in the presence of the adsorbate (Fig. 1).

Conclusions The adsorption of the antibiotics on the silver surface preserved the stability of the AgNP suspensions, as observed in the UV–VIS– NIR spectra, precluding aggregation process during the records of the SERS spectra and preserving the resonance conditions with 1064 nm exciting radiation. The SERS spectral patterns allowed to infer the adsorption geometries and interaction forces for all adsorbates here studied. LV interacts through carboxylate group with aromatic rings A and B almost perpendicular to the silver surface. TC adsorbs through carbonyl from ring C with hydroxyl from ring D also near to the silver surface. Both compounds have strong interactions with the metallic surfaces characterized by the great differences with the Raman spectra of the solids compounds. In such analyses, all adsorption geometries are in accordance with the surface selection rules. BP adsorbs as deprotonated anion, interacting with silver surface through carbonyl groups from carboxylate and acyclic amide. Such interaction is not as strong as the observed for the other adsorbates that can be inferred by the similarity of the SERS spectrum and the Raman spectrum of the solid and small changes in the LSPR band. For all compounds, the predominant species in solution, in the pH of the colloidal suspension, was considered as the same that interacts with the metallic surface. All SERS spectra were assigned using DFT calculations of the species in the protonation state proposed based on pKa values.

984

A.L. Filgueiras et al. / Spectrochimica Acta Part A: Molecular and Biomolecular Spectroscopy 136 (2015) 979–985

The proposed adsorption geometries allowed to infer that some groups known to be involved in the biological action were not participating in the interaction with silver surface, as fluoro and piperazine moieties in LV, amine and amide groups in TC and heteroatoms from beta-lactam ring in BP. Acknowledgements The authors would like to thanks the FAPEMIG (CEX-APQ00061/09), UFJF, CNPq and CAPES Brazilian financial foundations for the grants and research support, and the INMETRO for using the electron microscopy facilities. The authors are also grateful to the support from FAPEMIG-PRONEX APQ-04730-10. Appendix A. Supplementary material Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/j.saa.2014.09.120. References [1] E.L. Ru, P. Etchegoin, Principles of Surface-Enhanced Raman Spectroscopy: and Related Plasmonic Effects, Elsevier ed., Elsevier, New Zealand, 2008. [2] R. Aroca, Surface enhanced vibrational spectroscopy, Wiley ed., Wiley, Canada, 2006. [3] E.C. Le Ru, E. Blackie, M. Meyer, P.G. Etchegoin, Surface enhanced raman scattering enhancement factors: a comprehensive study, J. Phys. Chem. C 111 (2007) 13794–13803. [4] C.L. Haynes, A.D. McFarland, R.P.V. Duyne, Surface-Enhanced Raman Spectroscopy, Anal. Chem. 77 (2005). 338 A-346 A. [5] K. Kneipp, H. Kneipp, J. Kneipp, Surface-enhanced raman scattering in local optical fields of silver and gold nanoaggregates from single-molecule raman spectroscopy to ultrasensitive probing in live cells, Account Chem. Res. 39 (2006) 443–450. [6] M. Moskovits, Surface-enhanced Raman spectroscopy: a brief retrospective, J. Raman Spectrosc. 36 (2005) 485–496. [7] S.M. Morton, D.W. Silverstein, L. Jensen, theoretical studies of plasmonics using electronic structure methods, Chem. Rev. 111 (2011) 3962–3994. [8] M.E. Stewart, C.R. Anderton, L.B. Thompson, J. Maria, S.K. Gray, J.A. Rogers, R.G. Nuzzo, Nanostructured plasmonic sensors, Chem. Rev. 108 (2008) 494–521. [9] C.L. Haynes, R.P. Van Duyne, Plasmon-sampled surface-enhanced raman excitation spectroscopy , J. Phys. Chem. B 107 (2003) 7426–7433. [10] S.J. Lee, A.R. Morrill, M. Moskovits, Hot spots in silver nanowire bundles for surface-enhanced Raman spectroscopy, J. Am. Chem. Soc. 128 (2006) 2200– 2201. [11] Y. Fang, N.-H. Seong, D.D. Dlott, Measurement of the distribution of site enhancements in surface-enhanced Raman scattering, Science 321 (2008) 388–392. [12] J.P. Camden, J.A. Dieringer, J. Zhao, R.P. Van Duyne, Controlled plasmonic nanostructures for surface-enhanced spectroscopy and sensing, Account Chem. Res. 41 (2008) 1653–1661. [13] J. Zhang, X. Li, X. Sun, Y. Li, Surface enhanced Raman scattering effects of silver colloids with different shapes, J. Phys. Chem. B 109 (2005) 12544–12548. [14] R.J.C. Brown, M.J.T. Milton, Nanostructures and nanostructured substrates for surface—enhanced Raman scattering (SERS), J. Raman Spectrosc. 39 (2008) 1313–1326. [15] P. Corio, M.L.A. Temperini, P.S. Santos, J.C. Rubim, Contribution of the charge transfer mechanism to the surface-enhanced Raman scattering of the binuclear ion complex [Fe2((Bpe)(CN)10]6- adsorbed on a silver electrode in different solvents, Langmuir 15 (1999) 2500–2507. [16] J.C. Rubim, P. Corio, M.C.C. Ribeiro, M. Matz, Contribution of resonance Raman scattering to the surface-enhanced raman effect on electrode surfaces. A description using the time dependent formalism, J. Phys. Chem. 99 (1995) 15765–15774. [17] M. Osawa, N. Matsuda, K. Yoshii, I. Uchida, Charge transfer resonance Raman process in surface-enhanced Raman scattering from p-aminothiophenol adsorbed on silver: Herzberg–Teller contribution, J. Phys. Chem. 98 (1994) 12702–12707. [18] A. Otto, The ‘chemical’ (electronic) contribution to surface-enhanced Raman scattering, J. Raman Spectrosc. 36 (2005) 497–509. [19] A.C. Sant’Ana, W.A. Alves, R.H.A. Santos, A.M.D. Ferreira, M.L.A. Temperini, The adsorption of 2,20 :60 ,200 -terpyridine, 40 -(5-mercaptopentyl)-2,20 :60 ,200 terpyridinyl, and perchlorate on silver and copper surfaces monitored by SERS, Polyhedron 22 (2003) 1673–1682. [20] K. Zawada, J. Bukowska, An interaction of 1,10-phenantroline with the copper electrode in neutral and acidic aqueous solutions: a surface enhanced Raman scattering study, J. Mol. Struct. 555 (2000) 425–432. [21] A. Otto, Surface-enhanced Raman scattering of adsorbates, J. Raman Spectrosc. 22 (1991) 743–752.

[22] Z.Q. Tian, Surface-enhanced Raman spectroscopy: advancements and applications, J. Raman Spectrosc. 36 (2005) 466–470. [23] B. Wrzosek, J. Cukras, J. Bukowska, Adsorption of 1,2,4-triazole on a silver electrode: surface-enhanced Raman spectroscopy and density functional theory studies, J. Raman Spectrosc. 43 (2012) 1010–1017. [24] M. Fernández-Delgado, P. Suárez, Multiple antibiotic resistances of enteric bacteria isolated from recreational coastal waters and oysters of the Caribbean Sea, Annal. Microbiol. 59 (2009) 409–414. [25] S.N. Cohen, A.C.Y. Chang, L. Hsu, nonchromosomal antibiotic resistance in bacteria: genetic transformation of Escherichia coli by R-Factor DNA, Proc. Natl. Acad. Sci. 69 (1972) 2110–2114. [26] M. Kuroda, T. Ohta, I. Uchiyama, T. Baba, H. Yuzawa, I. Kobayashi, L. Cui, A. Oguchi, K.-I. Aoki, Y. Nagai, J. Lian, T. Ito, M. Kanamori, H. Matsumaru, A. Maruyama, H. Murakami, A. Hosoyama, Y. Mizutani-Ui, N.K. Takahashi, T. Sawano, R.-I. Inoue, C. Kaito, K. Sekimizu, H. Hirakawa, S. Kuhara, S. Goto, J. Yabuzaki, M. Kanehisa, A. Yamashita, K. Oshima, K. Furuya, C. Yoshino, T. Shiba, M. Hattori, N. Ogasawara, H. Hayashi, K. Hiramatsu, Whole genome sequencing of meticillin-resistant Staphylococcus aureus, Lancet 357 (2001) 1225–1240. [27] J. García-Barrasa, J. López-de-Luzuriaga, M. Monge, Silver nanoparticles: synthesis through chemical methods in solution and biomedical applications, Centr. Euro. J. Chem. 9 (2011) 7–19. [28] X. Cao, C. Cheng, Y. Ma, C. Zhao, Preparation of silver nanoparticles with antimicrobial activities and the researches of their biocompatibilities, J. Mater. Sci.: Mater. Med. 21 (2010) 2861–2868. [29] L.F. Espinosa-Cristóbal, G.A. Martínez-Castañón, R.E. Martínez-Martínez, J.P. Loyola-Rodríguez, N. Patiño-Marín, J.F. Reyes-Macías, F. Ruiz, Antibacterial effect of silver nanoparticles against Streptococcus mutans, Mater. Lett. 63 (2009) 2603–2606. [30] M. Rai, A. Yadav, A. Gade, Silver nanoparticles as a new generation of antimicrobials, Biotechnol. Adv. 27 (2009) 76–83. [31] M.K. Rai, S.D. Deshmukh, A.P. Ingle, A.K. Gade, Silver nanoparticles: the powerful nanoweapon against multidrug-resistant bacteria, J. Appl. Microbiol. 112 (2012) 841–852. [32] M.A. Khan, J. Musarrat, Interactions of tetracycline and its derivatives with DNA in vitro in presence of metal ions, Int. J. Biol. Macromol. 33 (2003) 49–56. [33] A.R. Shahverdi, A. Fakhimi, H.R. Shahverdi, S. Minaian, Synthesis and effect of silver nanoparticles on the antibacterial activity of different antibiotics against Staphylococcus aureus and Escherichia coli, Nanomed.: Nanotechnol., Biol., Med. 3 (2007) 168–171. [34] J.R. Morones, J.L. Elechiguerra, A. Camacho, K. Holt, J.B. Kouri, J.T. Ramírez, M.J. Yacaman, The bactericidal effect of silver nanoparticles, Nanotechnology 16 (2005) 2346. [35] A.R. Shahverdi, A. Fakhimi, H.R. Shahverdi, S. Minaian, Synthesis and effect of silver nanoparticles on the antibacterial activity of different antibiotics against Staphylococcus aureus and Escherichia coli, Nanomed.: Nanotechnol., Biol. Med. 3 (2007) 168–171. [36] A.C. Sant’Ana, A.L. Filgueiras, M. Lopes, V.L. da Silva, C.G. Diniz, Composition involving silver nanoparticles, chitosan and antibiotics with combined antibacterial potential. Patent request at INPI, n° BR 1020120273357, Brasil, 2012. [37] V. Uivarosi, Metal complexes of quinolone antibiotics and their applications: an update, Molecules 18 (2013) 11153–11197. [38] A. Maxwell, The molecular basis of quinolone action, J. Antimicrob. Chemoth. 30 (1992) 409–414. [39] L.A. Mitscher, Bacterial topoisomerase inhibitors: quinolone and pyridone antibacterial agents, Chem. Rev. 105 (2005) 559–592. [40] D. Martins, L. Gouvea, D. da Gama Jean Batista, P. da Silva, S. Louro, M.deNazaréC. Soeiro, L. Teixeira, Copper(II)–fluoroquinolone complexes with anti-Trypanosoma cruzi activity and DNA binding ability, BioMetals 25 (2012) 951–960. [41] I. Sousa, V. Claro, J.L. Pereira, A.L. Amaral, L. Cunha-Silva, B. de Castro, M.J. Feio, E. Pereira, P. Gameiro, Synthesis, characterization and antibacterial studies of a copper(II) levofloxacin ternary complex, J. Inorg. Biochem. 110 (2012) 64–71. [42] L.R. Gouvea, L.S. Garcia, D.R. Lachter, P.R. Nunes, F. de Castro Pereira, E.P. Silveira-Lacerda, S.R.W. Louro, P.J.S. Barbeira, L.R. Teixeira, Atypical fluoroquinolone gold(III) chelates as potential anticancer agents: relevance of DNA and protein interactions for their mechanism of action, Euro. J. Med. Chem. 55 (2012) 67–73. [43] E.C. Pereira-Maia, P.P. Silva, W.B.d. Almeida, H.F.d. Santos, B.L. Marcial, R. Ruggiero, W. Guerra, Tetraciclinas e glicilciclinas: uma visão geral, Química Nova 33 (2010) 700–706. [44] P.P. Silva, F.C.S.d. Paula, W. Guerra, J.N. Silveira, F.V. Botelho, L.Q. Vieira, T. Bortolotto, F.L. Fischer, G. Bussi, H. Terenzi, E.C. Pereira-Maia, Platinum(II) compounds of tetracyclines as potential anticancer agents: cytotoxicity, uptake and interactions with DNA, J. Brazilian Chem. Soc. 21 (2010) 1237– 1246. [45] F.C.S. de Paula, W. Guerra, I.R. Silva, J.N. Silveira, F.V. Botelho, L.Q. Vieira, E.C. Pereira-Maia, Cytotoxicity and cellular accumulation of palladium(II) complexes of tetracyclines, Chem. Biodivers. 5 (2008) 2124–2130. [46] M.A. Khan, J. Mustafa, J. Musarrat, Mechanism of DNA strand breakage induced by photosensitized tetracycline–Cu(II) complex, Mutat. Res./Fundam. Mol. Mech. Mutagenesis 525 (2003) 109–119. [47] B.L. Marcial, L.A.S. Costa, W.B. De Almeida, H.F. Dos Santos, Reactivity of 5a,6anhydrotetracycline platinum(II) complex with biological nucleophiles: a theoretical study, J. Brazilian Chem. Soc. 19 (2008) 1437–1449.

A.L. Filgueiras et al. / Spectrochimica Acta Part A: Molecular and Biomolecular Spectroscopy 136 (2015) 979–985 [48] W. Guerra, E. de Andrade Azevedo, A.R. de Souza Monteiro, M. BucciarelliRodriguez, E. Chartone-Souza, A.M.A. Nascimento, A.P.S. Fontes, L. Le Moyec, E.C. Pereira-Maia, Synthesis, characterization, and antibacterial activity of three palladium(II) complexes of tetracyclines, J. Inorg. Biochem. 99 (2005) 2348–2354. [49] W. Guerra, I.R. Silva, E.A. Azevedo, A.R.d.S. Monteiro, M. Bucciarelli-Rodriguez, E. Chartone-Souza, J.N. Silveira, A.P.S. Fontes, E.C. Pereira-Maia, Three new complexes of platinum(II) with doxycycline, oxytetracycline and chlortetracycline and their antimicrobial activity, J. Brazilian Chem. Soc. 17 (2006) 1627–1633. [50] L.-J. Ming, Structure and function of ‘‘metalloantibiotics’’, Med. Res. Rev. 23 (2003) 697–762. [51] D. Niccolai, L. Tarsi, R.J. Thomas, The renewed challenge of antibacterial chemotherapy[dagger], Chem. Commun. (1997) 2333–2342. [52] T. Kupka, b-Lactam antibiotics. Spectroscopy and molecular orbital (MO) calculations: Part I: IR studies of complexation in penicillin-transition metal ion systems and semi-empirical PM3 calculations on simple model compounds, Spectrochim. Acta Part A: Mol. Biomol. Spectrosc. 53 (1997) 2649–2658. [53] S. Regupathy, M.S. Nair, Studies on Cu(II) ternary complexes involving an aminopenicillin drug and imidazole containing ligands, Spectrochim. Acta Part A: Mol. Biomol. Spectrosc. 75 (2010) 656–663. [54] L. He, M. Lin, H. Li, N.-J. Kim, Surface-enhanced Raman spectroscopy coupled with dendritic silver nanosubstrate for detection of restricted antibiotics, J. Raman Spectrosc. 41 (2010) 739–744. [55] U. Neugebauer, A. Szeghalmi, M. Schmitt, W. Kiefer, J. Popp, U. Holzgrabe, Vibrational spectroscopic characterization of fluoroquinolones, Spectrochim. Acta Part A: Mol. Biomol. Spectrosc. 61 (2005) 1505–1517. [56] S. Gunasekaran, K. Rajalakshmi, S. Kumaresan, Vibrational analysis, electronic structure and nonlinear optical properties of Levofloxacin by density functional theory, Spectrochim. Acta Part A: Mol. Biomol. Spectrosc. 112 (2013) 351–363. [57] C.F. Leypold, M. Reiher, G. Brehm, M.O. Schmitt, S. Schneider, P. Matousek, M. Towrie, Tetracycline and derivatives-assignment of IR and Raman spectra via DFT calculations, Phys. Chem. Chem. Phys. 5 (2003) 1149–1157. [58] F.C.S. de Paula, S. Carvalho, H.A. Duarte, E.B. Paniago, A.S. Mangrich, E.C. Pereira-Maia, A physicochemical study of the tetracycline coordination to oxovanadium(IV), J. Inorg. Biochem. 76 (1999) 221–230. [59] J.E. Rode, J.C. Dobrowolski, Density functional IR, Raman, and VCD spectra of halogen substituted b-lactams, J. Mol. Struct. 651–653 (2003) 705–717. [60] T. Iliescu, M. Baia, I. Pavel, Raman and SERS investigations of potassium benzylpenicillin, J. Raman Spectrosc. 37 (2006) 318–325. [61] V. Reipa, J.J. Horvath, Surface-enhanced raman study of benzylpenicillin, Appl. Spectrosc. 46 (1992) 1009–1013.

985

[62] S.J. Clarke, R.E. Littleford, W.E. Smith, R. Goodacre, Rapid monitoring of antibiotics using Raman and surface enhanced Raman spectroscopy, Analyst 130 (2005) 1019–1026. [63] J.A. Creighton, C.G. Blatchford, M.G. Albrecht, Plasma resonance enhancement of Raman scattering by pyridine adsorbed on silver or gold sol particles of size comparable to the excitation wavelength, J. Chem. Soc., Faraday Trans. 2: Mol. Chem. Phys. 75 (1979) 790–798. [64] J.C. Rubim, F.A. Trindade, M.A. Gelesky, R.F. Aroca, J. Dupont, Surface-enhanced vibrational spectroscopy of tetrafluoroborate 1-n-Butyl-3-methylimidazolium (BMIBF4) ionic liquid on silver surfaces, J. Phys. Chem. C 112 (2008) 19670– 19675. [65] H.S. Schrekker, M.A. Gelesky, M.P. Stracke, C.M.L. Schrekker, G. Machado, S.R. Teixeira, J.C. Rubim, J. Dupont, Disclosure of the imidazolium cation coordination and stabilization mode in ionic liquid stabilized gold(0) nanoparticles, J. Colloid Interf. Sci. 316 (2007) 189–195. [66] C. Adamo, V. Barone, Toward reliable density functional methods without adjustable parameters: the PBE0 model, J. Chem. Phys. 110 (1999) 6158–6170. [67] P.J. Hay, W.R. Wadt, Ab initio effective core potentials for molecular calculations, potentials for the transition metal atoms Sc to Hg, J. Chem. Phys. 82 (1985) 270–283. [68] P.C. Hariharan, J.A. Pople, Theor. Chem. Acc. 28 (1973) 213. [69] R. Wysokin´ski, K. Hernik, R. Szostak, D. Michalska, Electronic structure and vibrational spectra of cis-diammine(orotato)platinum(II), a potential cisplatin analogue: DFT and experimental study, Chem. Phys. 333 (2007) 37–48. [70] H.F.d. Santos, W.B.d. Almeida, A.M.G.d. Val, A.C. Guimarães, Espectro infravermelho e análise conformacional do composto 3-fenil-2-oxo-1,2,3oxatiazolidina, Química Nova 22 (1999) 732–736. [71] M.J. Frisch, G.W. Trucks, H.B. Schlegel, G.E. Scuseria, M.A. Robb, J.R. Cheeseman, G. Scalmani, V. Barone, B. Mennucci, G.A. Petersson, in Inc:Wallingford, Gaussian 09, revision A.02 CT.2009. [72] T. Hirano, S. Yasuda, Y. Osaka, M. Kobayashi, S. Itagaki, K. Iseki, Mechanism of the inhibitory effect of zwitterionic drugs (levofloxacin and grepafloxacin) on carnitine transporter (OCTN2) in Caco-2 cells, Biochimica et Biophysica Acta (BBA), Biomembranes 1758 (2006) 1743–1750. [73] V.G. Alekseev, I.A. Volkova, Acid-base properties of some penicillins, Russian J. Gener. Chem. 73 (2003) 1616–1618. [74] K. Nakamoto, Infrared and Raman Spectra of Inorganic and Coordination Compounds, in: Wiley (Ed.), Wiley, New York, 1986. [75] M. Moskovits, Surface selection rules, J. Chem. Phys. 77 (1982) 4408–4416. [76] M. Moskovits, J.S. Suh, Surface selection rules for surface-enhanced Raman spectroscopy: calculations and application to the surface-enhanced Raman spectrum of phthalazine on silver, J. Phys. Chem. 88 (1984) 5526–5530.