Halloysite nanotubes with immobilized silver nanoparticles for anti-bacterial application

Colloids and Surfaces B: Biointerfaces 151 (2017) 249–254

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Halloysite nanotubes with immobilized silver nanoparticles for anti-bacterial application Subhra Jana a,∗ , Anastasiya V. Kondakova b , Svetlana N. Shevchenko b , Eugene V. Sheval b , Kirill A. Gonchar b,c , Victor Yu. Timoshenko b,d , Alexander N. Vasiliev b,c a Department of Chemical, Biological & Macro-Molecular Sciences, S. N. Bose National Centre for Basic Sciences, Block – JD, Sector-III, Salt Lake, Kolkata,700106, India b Lomonosov Moscow State University, 119991 Moscow, Russia c Ural Federal University, 620002 Ekaterinburg, Russia d National Research Nuclear University “MEPhI”, 115409 Moscow, Russia

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Article history: Received 24 September 2016 Received in revised form 8 December 2016 Accepted 14 December 2016 Available online 21 December 2016 Keywords: Halloysite clay Wet chemistry Immobilization Metal nanoparticles Plasmonic Bactericidal effect

a b s t r a c t Halloysite nanotubes (HNTs) with immobilized silver (Ag) nanoparticles (NPs) were prepared by methods of wet chemistry and were characterized by using the transmission electron microscopy, x-ray diffraction, optical spectroscopy and experiments with E. coli bacteria in-vitro. It was found that Ag NPs with almost perfect crystalline structure and sizes from ∼9 nm were mainly attached over the external surface of HNTs. The optical absorption measurement revealed a broad plasmonic resonance in the region of 400–600 nm for HNTs with Ag NPs. The later samples exhibit bactericidal effect, which is more pronounced under illumination. A role of the plasmonic excitation of Ag NPs for their bioactive properties is discussed. The obtained results show that Ag NPs–decorated HNTs are promising agents for the antibacterial treatment. © 2016 Elsevier B.V. All rights reserved.

1. Introduction An ability to integrate nanotechnology with biotechnology ensures the greatest impact in biology and biomedicine, since the convergence of these two fields gives rise to a combinatorial field of nanobiotechnology [1]. As the noble metal nanoparticles demonstrate unique optical, electronic, photonic, and catalytic properties, thus integration of these nanoparticles (NPs) with biocompatible clays produces novel hybrid nanocomposites to be explored in different fields. In noble metal nanoparticles, the fascinating optical properties originates from resonant oscillation of their free electrons in the presence of light, also known as localized surface plasmon resonance, which can be visualized from their bright intense color [1,2]. In the recent years, anti-bacterial materials have widely been used in our day-today life as they effectively protect our health. A wide variety of anti-bacterial materials have been reported to prevent attachment and proliferation of microbes [3–6]. However, their usage sometime is limited owing to the concerns of antibiotic resistance, environmental pollution, relatively complex

∗ Corresponding author. E-mail address: [email protected] (S. Jana). http://dx.doi.org/10.1016/j.colsurfb.2016.12.017 0927-7765/© 2016 Elsevier B.V. All rights reserved.

processing, and high cost [7,8]. Therefore, it is an urgent need to develop an anti-bacterial material which will be devoid of these concerns and at the same time has low toxicity, high thermal stability and low volatility. Halloysite nanotubes (HNTs) are a kind of kaolinite clay with a hollow tubular structure produced by the surface weathering of aluminosilicate minerals, having chemical structure of Al2 Si2 O5 (OH)4 ·nH2 O. The adjacent alumina and silica layers with their water of hydration, give rise to a packing disorder and help the nanotubes to curve and roll up to form multilayers [9,10]. As the internal and external surfaces of HNTs consist of gibbsite-like array of Al-OH groups and Si-O-Si groups respectively, they possess positive and negative charge at the inner and outer surfaces which result in different inner/outer surface chemistry as well as help to manipulate their chemico-physical properties through the control of the chemistry of the constituent elements [11,12]. According to the state of hydration, HNTs are of two types: hydrated halloysite−10 ◦ A with one layer of water molecules between the multi-layer and dehydrated halloysite−7 ◦ A achieved by an irreversible phase transition with loss of adsorbed water [10,13,14]. Modification of HNTs by different metal NPs is a promising approach to form new nanocomposites with interesting optical, sensor and biochemical functionalities [15,16]. For example, HNTs

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with deposited gold (Au) NPs can exhibit surface plasmon resonance (SPR) [17,18], which is widely used in surface-enhanced Raman scattering (SERS) for detection of small amount of molecules [19]. We have also shown that silver (Ag) NPs deposited on the surface of HNTs could result in SPR and SERS [20]. In the present paper, we report the synthesis of a nanocomposite, consisting of Ag NPs immobilized on HNTs and study the antibacterial application of the prepared nanocomposites for E. coli bacteria. We have also demonstrated the role of the plasmonic excitation of Ag NPs for their bioactive properties. 2. Experimental 2.1. Materials All chemicals were used as received. HNTs, silver nitrate (AgNO3 , 99.9999%) and sodium borohydride (NaBH4 ) were purchased from Sigma-Aldrich. (3-aminopropyl) triethoxysilane (97%) was received from Alfa Aesar. Toluene was obtained from Merck. 2.2. Sample preparation Prior immobilization of Ag nanoparticles (NPs) over the surface of halloysite nanotubes (HNTs), the outer surface of HNTs was modified with an aminosilane, (3-aminopropyl) triethoxysilane through grafting reaction [21]. The reaction was performed under nitrogen atmosphere using standard air-free technique. A threenecked round bottom flask containing 3.0 g of HNTs and 20.0 mL of toluene was fitted with a condenser, rubber septum, thermocouple adaptor, and a quartz sheath through which a thermocouple was inserted. The reaction mixture was then heated with a heating mantle; once the reaction temperature reached to 60 ◦ C, 3.0 mL of (3-aminopropyl) triethoxysilane was injected to the reaction flask and the temperature was increased to 120 ◦ C, followed by refluxed the reaction solution for 12 h. After the completion of the reaction, the product was washed several times with toluene and ethanol respectively to remove excess aminosilane and then dried at 100 ◦ C under vacuum. The aminosilane modified HNTs were referred to as HNTs-NH2 . HNTs loaded with Ag NPs have been prepared based on the immobilization of silver precursors over the surface of HNTs-NH2 followed by the reduction with ice cold aqueous solution of sodium borohydride. First, 2.0 g HNTs-NH2 were taken in beaker containing 25 mL 10−2 M AgNO3 solution. The reaction mixture was now stirred on a magnetic stirrer for 10 h to complete immobilization of Ag ions onto the surface of HNTs-NH2 . Once the HNTs-NH2 gets saturated with AgNO3 , the product was washed several times with Mili-Q water to remove the unadsorbed AgNO3 if any. After complete loading of Ag ions onto HNTs, dilute HCl solution was added to the supernatant solution, which produces a white precipitation of silver chloride, demonstrating the presence of excess Ag ions in the supernatant solution even after complete immobilization. Finally, HNTs-NH2 loaded with Ag ions was reduced with ice cold aqueous solution of NaBH4 to produce Ag loaded HNTs, which in turn changes the colourless halloysite into yellow, owing to the immobilization of Ag NPs over the surface of HNTs-NH2 (see Scheme 1). At the end of the reduction reaction, nanotubes decorated with Ag NPs were washed several times with de-ionized water to remove the excess borohydride and finally dried in air to study their optical properties and bioactivity. 2.3. Sample characterization The morphology of HNTs before and after immobilization of Ag NPs was investigated using a transmission electron microscope (TEM: FEI TECNAI G2 F20-ST) operating at 200 kV, after drop casting

a drop of solution of the sample onto a carbon coated copper grid. High resolution transmission electron microscopy (HR-TEM) and Energy dispersive X-ray spectroscopy (EDX) have been performed in the above mentioned TEM operating at 200 kV. Field emission scanning electron microscopy has also been performed for HNTs and HNTs-NH2 (FESEM: FEI QUANTA FEG 250) by drop casting a drop of sample solution on silicon wafer. CHN analysis was done by using a PerkinElmer 2400 Series II CHNS Elemental Analyzer. Fourier transform infrared (FTIR) spectra were recorded in the range of 500–4000 cm−1 by using a JASCO FT/IR 6300 apparatus. Powder X-ray diffraction (XRD) analysis was performed by a RIGAKU MiniFlex II powder diffractometer using Cu K␣ radiation with 35 kV beam voltage and 15 mA beam current. Measurements of the total (specular together with diffusive) reflectance/transmission spectra in the region from 200 to 1500 nm were carried out with a Perkin Elmer Lambda 950 spectrometer equipped with an integrating sphere. Samples for the optical measurement were prepared in the form of 100 ␮m-thick layers deposited on optically polished quartz substrates by using spin coating from aqueous suspensions. The suspensions were formed by mixing HNT powder in de-ionized water followed with sonification in an ultrasonic bath for 30 min the initial concentration of HNTs in suspension was 10 g/L. After the spin coating the layers were dried in air for1 h.

2.4. Experiments in-vitro Bacteria Escherichia coli (E. coli) were grown by the standard method in agar medium at 37 ◦ C. For the experiment with HNTs loaded with Ag NPs, the bacterial cell suspension was used at concentration of 108 per 1 mL. The experiment was carried out in several stages. At the first stage, 1 mL of the bacteria suspension was mixed with 1 mL of the aqueous suspension of HNTs-Ag with concentration of 0.4–2 g/L and the mixture was put in optically transparent plastic cuvette. At the second stage, a part of the obtained mixtures were homogeneously illuminated by white light at room temperature. The light of a tungsten lamp was passed through the filter to get the spectral band from 400 to 800 nm. The light intensity and illumination time were 100 mW/cm2 and 10 min, respectively. Additionally, the experiments were carried out with laser irradiation at 488 nm with intensity 10 mW/cm2 for 15 min. A special attention was paid to keep the constant temperature of the bacteria cell suspension during the illumination with an accuracy of 1–2 ◦ C. Another part of the samples was kept in darkness for the same time. At the third stage, all the samples were transferred in Petri dishes and incubated at 37 ◦ C for 12 h. Finally, the result of bacterial growth was evaluated by comparing the number of colony formed in the experimental (with HNTs-Ag) and control dishes. The results were averaged for 3 series of the samples.

3. Results and discussion The grafting of aminosilane, (3-aminopropyl) triethoxysilane over the outer surface of HNTs was confirmed by Fourier transform infrared (FTIR) spectroscopy. FTIR spectra of HNTs and HNTs-NH2 are shown in Fig. 1A. The observed three new peaks at 1563, 2933 and 3452 cm−1 in case of HNTs NH2 are attributed to the N H deformation, stretching vibration of C H, and the stretching vibration of N H respectively, demonstrating the grafting of the aminosilane onto the surface of HNTs [22,23]. Additionally, presence of two well-defined bands at 3621 and 3697 cm−1 in both HNTs and HNTs-NH2 owing to the stretching vibrations of inner hydroxyl group and inner surface hydroxyl group respectively,

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Scheme 1. Schematic presentation of the surface modification of halloysite nanotubes (HNTs) using (3-aminopropyl) triethoxysilane, followed by synthesis of Ag NPs over the surface of aminosilane modified HNTs.

Fig. 1. (A) FTIR spectra and (B, C) EDX spectra of HNTs and aminosilane modified HNTs (HNTs-NH2 ) respectively.

Fig. 2. FESEM and TEM images of (A, C) HNTs and (B, D) HNTs-NH2 , demonstrating cylindrical shaped tubes with an open ended lumen along the tube.

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Fig. 3. (A, B) TEM micrographs of the nanotubes loaded with Ag NPs at two different magnifications, synthesized through the immobilization of the silver precursors over the surface of HNTs-NH2 followed by the reduction to produce Ag NPs. (C) corresponding EDX spectra of the Ag NPs loaded clay nanotubes. (D) XRD patterns of HNTs, HNTs-NH2 and after the immobilization of Ag NPs over the surface of HNTs-NH2 .

which in turn exhibit that the basic structure of HNTs before and after grafting are the same. Energy dispersive X-ray (EDX) analysis further reveals the presence of carbon and nitrogen along with the three main constituents, oxygen, aluminium, and silicon in HNTs-NH2 ; signifying the functionalization of HNTs with the aminosilane (Fig. 1B and C). CHN elemental analysis has been performed to determine the mass fraction of nitrogen present in HNTs-NH2 and it has been found to be 0.51 wt% i.e.; 0.37 mmol of amino groups per 1 g of HNTs-NH2 . The structure and morphology of HNTs before and after surface functionalization were studied by field emission scanning electron microscopy (FESEM) and transmission electron microscopy (TEM). Both FESEM and TEM images (Fig. 2) reveal that HNTs are cylindrical shaped tubes with an open ended lumen along the tube. The inner and outer diameter of the tubes are 15–20 and 50–100 nm respectively along with a typical length of the tube is around 1.0–1.5 ␮m, representing irregularity in their length. From the TEM image, one can clearly observe that these cylindrical shaped tubes have some defects on the outer surfaces, most probably due to the mechanical damage or by crystallographic defects. A facile wet-chemical approach was followed to synthesize clay nanotubes loaded with Ag NPs, which has schematically been presented in Scheme 1. The synthetic procedure involved immobilization of the silver precursors over the surface of HNTs-NH2 , followed by the reduction to achieve metal NPs loaded over the outer surface of nanotubes. The morphology of Ag NPs loaded HNTs has been characterized using TEM analysis (Fig. 3). TEM image

represents that the cylindrical shaped tubes were decorated with spherical Ag NPs, having particle size of ∼9 nm. All the NPs are well-dispersed over the surface of the tubes without any agglomeration. EDX spectra demonstrate the obvious signals for Ag along with the other constituents of HNTs-NH2 , shown in Fig. 3C. The amount of the Ag NPs immobilized on the halloysite nanotubes has been found to be ∼1.01 atomic%. X-ray diffraction (XRD) pattern further authenticates the formation of Ag NPs onto the nanotube surfaces owing to the presence of two newly emerged peaks for (111) and (200) planes of face centered cubic (fcc) Ag (Fig. 3D) [24]. However, it is important to note that the observed (020) peak is the characteristic of tubular halloysite clay and the diffraction pattern of HNT-NH2 is similar to that of bare HNTs [25]. Moreover, there is no intercalation of the aminosilane into the interlayer of HNTs even after grafting, as (001) reflection does not shift to the lower angles. All these Ag NPs decorated clay nanotubes have been utilized to suppress the bacteria growth. It is important to note that this procedure can be extended for the synthesis of silver nanoparticles exclusively inside the tube. However, a minor modification is necessary to achieve silver nanoparticles with in the lumen of the tube. The reaction flask consisting of halloysite clay and aqueous solution of silver precursors needs to be evacuated using a vacuum pump at room temperature. To achieve maximum loading of silver precursors inside the lumen of halloysite, the process of evacuation and cycling back to atmospheric pressure must be repeated for several times under stirring condition. Then, the product was washed with Milli-Q water to remove unadsorbed precursors, subsequently

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Fig. 4. (A) Absorption spectra of the bare HNTs (red line) and those with Ag NPs (blue line) deposited on quartz substrate. Vertical arrows indicate features of the plasmon resonance in Ag NPs. (B) Relative number of E. coli bacteria after incubation without (control) and with bare HNTs (1 g/L) in darkness (grey bars) and under illumination (pattern grey bars) as well as with HNTs (0.2 g/L) covered by Ag NPs (blue bars) in darkness and under illumination at 488 nm (blue pattern bars), and HNTs (1 g/L) covered by Ag NPs (red bars) in darkness and under illumination with white light (red pattern bars). (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

calcined at an appropriate temperature or in situ reduction using a reducing agent, which will produce silver nanoparticles loaded exclusively inside the tubes. Fig. 4A shows typical absorption spectra of bare HNTs and Agcoated ones. The absorption value, A, was calculated from the spectra of total transmittance, T, and reflectance, R, according to the following relation: A = 1-T-R, where the values of T and R were measured by using the clean quartz substrate as a reference sample. HNTs modified with silver NPs exhibit stronger absorption in the range from 350 to 800 nm than the bare HNTs. A pronounced absorption peak at 400 nm and a shoulder at 600 nm are clearly seen and marked with arrows in Fig. 4A. These features are evidences of the localized surface plasmon resonance in individual Ag NPs and their aggregates. [18–20] The absorption peak broadening in the longer wavelengths can be attributed to the emergence of collective modes, which can occur when silver NPs are not touching, but very close to each other. Another reason for the broadening is electronic states of the defects induced by the incorporated Ag NPs into the crystal lattice of HNTs, which destroy their aluminosilicate bonds. Note, the HNTs with smaller (5 nm) Ag NPs had stronger absorption in the long wavelength region and were visually darker than the samples with 9 nm-sized Ag. These optical losses will obviously decrease the electromagnetic field strength in HNTs-Ag nanocomposites. Fig. 4B shows dependences of the colony number of E. coli bacteria in Petri dishes with bare HNTs and Ag-decorated ones in darkness and under illumination. The colony number is divided to that in the reference group where HNTs were not added. While are the number of bacteria slightly reduced in the presence of bare HNTs, a strong suppression of the bacteria growth occurred for the samples of HNTs with Ag NPs. The illumination of HNTs resulted in an additional decrease of the bacteria number below 20% relative to the reference group. This fact indicates an effect of the plasmonic enhancement of electrical field by Ag NPs, which can stimulate the electrophoresis of the bacteria membrane and then its destruction (lysis). The role of plasmonic effect is confirmed by the results of in-vitro experiments with laser irradiation at 488 nm close to the main maximum of plasmonic resonance in Ag NPs (see Fig. 4A), which revealed nearly 2 times stronger suppression of the bacteria growth after illumination in the presence of HNTs coated with Ag NPs (blue bars in Fig. 4B). Note, the white light illumination of the concentrated (1 g/L) suspension of HNTs with Ag NPs resulted in weaker effect of the bacteria growth suppression relative to the non-illuminated samples (red bars in Fig. 4B). This effect can be explained by optical losses related to the defect states in the pre-

pared nanocomposites, which reduce the local electric fields nearby Ag nanoparticles. 4. Conclusions The nanocomposites based on halloysite nanotubes and silver nanoparticles with perfect crystalline structure and sizes ∼9 nm were prepared and characterized by different physical methods. The Ag NPs are immobilized over the external surfaces of HNTs and exhibit the plasmonic resonance in the visible spectral region. The experiments with E. coli in-vitro have confirmed that the prepared samples exhibited bactericidal properties and the bactericidal effect is stronger for the samples of HNTs with Ag NPs under blue light illumination that indicates a role of the plasmonic excitation of Ag NPs for their bioactive properties. Therefore, Ag-functionalized HNTs seem to be promising for antibacterial treatments of liquids and surfaces stimulated by visible light exposure. Acknowledgements The authors are grateful to Yu. M. Lvov and L. A. Osminkina for fruitful discussions and A. A. Eliseev for assistance in the optical experiments. S. Jana acknowledges the Department of Science and Technology (DST), New Delhi for the research grants (IFA12CH-60 and SR/NM/NS-18/2014). This work was also supported by the grant program of the Russian Science Foundation15-12-20021 and by Act 211 Government of the Russian Federation, contract no. 02.A03.21.0006. References [1] P.K. Jain, X. Huang, I.H. El-Sayed, M.A. El-Sayed, Noble metals on the nanoscale: optical and photothermal properties and some applications in imaging, sensing, biology, and medicine, Acc. Chem. Res. 42 (2008) 1578–1586. [2] E. Kelly, L.L. Coronado, The optical properties of metal nanoparticles: the influence of size, shape, and dielectric environment, J. Phys. Chem. B 107 (2003) 668–677. [3] A. Moran, B. Israela, Z. Meital, Gentamicin-loaded bioresorbable films for prevention of bacterial infections associated with orthopedic implants, J. Biomed. Mater. Res. Part A 83A (2007) 10–19. [4] M. Ramstedt, N. Cheng, O. Azzaroni, D. Mossialos, H.J. Mathieu, W.T.S. Huck, Synthesis and characterization of poly(3-sulfopropylmethacrylate) brushes for potential antibacterial applications, Langmuir 23 (2007) 3314–3321. [5] A. Kumar, P.K. Vemula, P.M. Ajayan, G. John, Silver-nanoparticle-embedded antimicrobial paints based on vegetable oil, Nat. Mater. 7 (2008) 236–241. [6] C. Wei, W.Y. Lin, Z. Zainal, N.E. Williams, K. Zhu, A.P. Kruzic, R.L. Smith, K. Rajeshwar, Bactericidal activity of TiO2 photocatalyst in aqueous media:

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