Sol-gel preparation of Ag-doped MgO nanoparticles

Ceramics International 43 (2017) 1066–1072

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Sol-gel preparation of Ag-doped MgO nanoparticles with high efficiency for bacterial inactivation ⁎

Yuncheng Caia, Dan Wua, Xiwei Zhua, Wei Wanga, , Fatang Tana, Jianguo Chena, Xueliang Qiaoa, Xiaolin Qiub a b

State Key Laboratory of Material Processing and Die & Mould Technology, Huazhong University of Science and Technology, Wuhan 430074, China Nanomaterials Research Centre, Nanchang Institute of Technology, Nanchang 330013, China

A R T I C L E I N F O

A BS T RAC T

Keywords: Magnesium oxide Ag doping Sol-gel preparation Nanoparticle Bacterial inactivation

Herein, Ag-doped magnesium oxide (MgO) nanoparticles were prepared by a citric acid-assist sol-gel method. It is evidenced that the size of MgO particles decreases after Ag doping and a small amount of Ag is doped into MgO crystal. The bacterial inactivation of as-prepared Ag-doped MgO against Escherichia coli (E. coli) suggests that Ag doping can greatly enhance the antibacterial activity of MgO nanoparticles and 1% Ag-doped MgO inactivates effectively 7-log bacterial cells within 20 min. The releases of metal ions (Ag+ and Mg2+) from Agdoped MgO are at a very low level, which would not play the leading role in bacterial inactivation. The mechanism for the improvement of antibacterial activity of Ag-doped MgO is concluded as three aspects. Firstly, Ag doping can inhibit the grain growth of MgO nanoparticles, resulting in smaller size of MgO particles. Secondly, when Ag+ is doped into MgO matrix, more oxygen vacancies will be generated to keep an overall neutral charge. Thirdly, Ag-doped MgO has a relatively low electron-transfer resistance, which can accelerate the electron transfer within MgO crystal, in favour of the single-electron reduction of adsorbed oxygen. All these would substantially enhance ROS production and the contact interaction between bacterial cells and nanoparticles. Therefore, Ag doping can markedly promote the antibacterial activity of MgO nanoparticles.

1. Introduction Currently, MgO nanoparticles have drawn considerable attention due to their great promising applications as catalyst, adsorbent and bactericide [1–10]. As inorganic antibacterial agents, MgO nanoparticles have numerous prospects in applications due to their abundant source of raw materials, high thermal stability, low biological toxicity and biodegradability [11–13]. More importantly, MgO nanoparticles have wide-spectrum bactericidal property towards both Gram-positive and Gram-negative bacteria [7], and can even inactivate several kinds of cancer cells [14]. However, the antibacterial activity of MgO nanoparticles is rather limited, which hampers the extensive application of MgO nanoparticles as bactericide. Therefore, a plenty of efforts have been made to improve the antibacterial activity of MgO nanoparticles. Composite with other antibacterial agents or doping with metal elements are believed to be effective methods. Stoimenov et al. demonstrated that the composites of MgO nanoparticles and halogens (Cl2, Br2) show very effective antibacterial activity against Grampositive and Gram-negative bacteria as well as spores [15]. However, halogens are of high toxicity to human body and environment. Jin et al.

⁎

revealed a synergistic effect of MgO in combination with nisin induced the distortion and damage of cell membrane of E. coli [16]. Our previous work suggested that lithium doping could enhance the antibacterial activity of MgO nanoparticles, due to the enhancement of oxygen vacancy concentration and basicity of MgO nanoparticles, favouring the generation and stabilization of active oxygen [17]. Cui et al. proved that Cu-doped MgO exhibits better antibacterial activity than pure MgO owing to the increase of defect concentration and copper content [18]. Unfortunately, these studies do not put forward a way to significantly promote the antibacterial activity of MgO nanoparticles, and few work has systematically illuminated the mechanism for the improvement of antibacterial activity of MgO nanoparticles. Silver (Ag) and its derivatives show wide-spectrum and highefficiency bactericidal activity towards a great variety of microorganisms [19,20]. Although numerous Ag products have been commercially used as bactericides, there is still a great risk involved with widespread utilization to humans and the environment [21]. Recently, we prepared Ag-loaded MgO nanocomposites by loading synthesized Ag nanoparticles on MgO nanoparticles, and the as-prepared Ag-loaded MgO nanocomposites show better antibacterial activity than MgO and Ag

Corresponding author. E-mail address: [email protected] (W. Wang).

http://dx.doi.org/10.1016/j.ceramint.2016.10.041 Received 28 July 2016; Received in revised form 26 September 2016; Accepted 6 October 2016 Available online 07 October 2016 0272-8842/ © 2016 Elsevier Ltd and Techna Group S.r.l. All rights reserved.


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out on a Kratos AXIS Ultra DLD-600W X-ray photoelectron spectrometer (Shimadzu Co., Japan). Monochromatic Al Kα radiation was used as excitation source, and binding energy (BE) was referred to carbon (C) 1s line at 284.6 eV.

counterparts [22]. However, the synthetic process is relatively complex, and the loading efficiency of Ag decreased rapidly along with the increase of Ag amount. Besides, Ag loading would occupy the active sites on the surface of MgO and thus inhibit the adsorption of oxygen. To our knowledge, few work focused on the preparation and antibacterial property of Ag-doped MgO nanoparticles. When Ag is doped into MgO lattice, Ag atom will occupy substitutional site rather than interstitial site since the radius of Ag+(0.126 nm) is larger than that of Mg2+(0.066 nm). Accordingly, oxygen vacancy will be generated to favour the structure reorganization and keep an overall neutral charge after Mg2+ in MgO crystal is replaced by Ag+. The defect reaction equation can be expressed as follows:

2.4. Antibacterial test The antibacterial activity of as-prepared samples was evaluated by inactivating a model bacterium of E. coli ATCC25922. The detailed procedure was described as follows: 5 mg of as-prepared sample was added into 100 mL sterilized saline solution (0.9 wt%) containing ~107 CFU/mL (colony forming units per millilitre) bacterial cells. Then the mixture was stirred with a magnetic stirring apparatus. At certain interval, an aliquot of the mixture was pipetted out and serially diluted with sterilized saline. Subsequently, 0.1 mL of the diluted mixture was uniformly spread on agar plate and incubated at 37 °C for 24 h. The colonies formed on agar plates were counted to calculate the number of survived bacteria. The above experiments were conducted in triplicates to get an average number of bacteria with error bar. The partition experiments were proceeded similarly as the above process except that the bacterial cells and as-prepared samples were parted by using semipermeable membrane (MWCO 1000, Spectrumlabs, USA) and anion exchange membrane (MA-3475, AKT, USA).

2MgO Ag2 O ⎯⎯⎯⎯⎯⎯⎯⎯⎯→ 2Ag′Mg +V∙∙ O +OO The generated defects can accelerate the reactive oxygen species (ROS) production, further improving the corresponding antibacterial activity of oxides [23,24]. Moreover, Ag doping will lead to the decrease in particle size because Ag dopant has a negative effect on the grain growth of metal oxides [25,26]. Thus, Ag doping makes it possible to obtain MgO nanoparticles with smaller particle size, leading to the stronger the contact interaction between MgO particles and bacterial cells. Therefore, Ag-doped MgO nanoparticles are expected to exhibit excellent antibacterial activity in comparison with pure MgO nanoparticles. In present work, Ag-doped MgO nanoparticles were prepared by a sol-gel method. The antibacterial activity of Ag-doped MgO nanoparticles was evaluated by the bacterial inactivation against Escherichia coli (E. coli, ATCC25922). The influence of Ag doping on the morphology and the antibacterial activity of as-prepared samples was discussed. Additionally, the antibacterial mechanism of Ag-doped MgO nanoparticles was further investigated and discussed.

2.5. Release of silver and magnesium ions To investigate the leakage of silver and magnesium ions, 5 mg of Ag-doped MgO sample was suspended in 100 mL saline solution under continuous stirring. At certain intervals, 5 mL of suspension was collected and filtered through a membrane filter with pore size of 0.22 µm. The concentrations of Ag/Mg ions in filtrate were measured on a 4100 microwave plasma-atomic emission spectrophotometer (MP-AES, Agilent Technologies, USA).

2. Materials and method 2.6. Detection of ROS 2.1. Materials The generation of superoxide radical (·O2−) could be detected using nitro blue tetrazolium (NBT) as a probe which shows a maximum absorbance at 259 nm [27–29]. The detection process was described in detail as follows, 5 mg of Ag-doped MgO sample was suspended in 100 mL saline containing NBT (2.5×10−4 M) under a 300 W Xe lamp irradiation. At certain intervals, 3 mL of suspension was taken out and filtered to separate the sample. The absorbance of obtained filtrate was measured with a UV–vis spectrophotometer at the wavelength of 259 nm. The generation of superoxide radical was quantitatively determined by analysing the decrease of the concentration of NBT. The generated ·O2− would react with H+ to produce H2O2, which can be measured by titration method with the KMnO4 solution [30,31]. 0.10 g of Ag-doped MgO sample was suspended in 20 mL of distilled water and kept stirring for 40 min. Then the suspension was filtered and the pH value of the obtained filtrate was adjusted to 1 with 0.2 M H2SO4, subsequently titrated with freshly prepared 0.001 M KMnO4 solution.

Magnesium nitrate hexahydrate (Mg(NO3)2·6H2O) was purchased from Shanghai Experimental Reagent Co., Ltd (Shanghai, China). Citric acid monohydrate (C6H8O7·H2O) and silver nitrate (AgNO3) were supplied by Sinopharm Chemical Reagent Co., Ltd (Shanghai, China). All chemicals were of analytical grade and used as received. Double distilled (DI) water was used throughout the experiments. 2.2. Preparation of Ag-doped MgO nanoparticles Ag-doped MgO nanoparticles were prepared via a sol-gel method reported in previous work [22]. Firstly, (0.02-x) mol Mg(NO3)2·6H2O and x mol AgNO3 were dissolved in 20 mL DI water. After then a solution containing 0.02 mol C6H8O7·H2O was added into the above solution under stirring. The mixture was kept stirring in a water bath at 80 °C until a wet gel formed. Secondly, the wet gel was heated to 150 °C in an oven to get a fluffy dry gel. Finally, the dry gel was crushed down and calcined at 600 °C in air atmosphere to get Ag-doped MgO nanoparticles. Here, x was set as 0, 0.0001, 0.0002, 0.0004 and 0.0006, and the obtained samples were designated as pure MgO, 0.5% Ag-doped MgO, 1% Ag-doped MgO, 2% Ag-doped MgO and 3% Ag-doped MgO, respectively.

2.7. Electrochemical impedance spectroscopy (EIS) measurement Electrochemical impedance spectroscopy (EIS) measurements were performed using a CS350 electrochemical analyser (CorrTest, China) with a single-compartment three-electrode glass cell. Platinum foil and a saturated calomel electrode were used as a counter electrode and a reference electrode, respectively. As-prepared samples were used as working electrodes, and the working electrodes were prepared as follows: 0.1 g of as-prepared sample, 0.25 mL water and 0.03 g polyethylene glycol (PEG, molecular weight: 20,000) were mixed in an agate mortar and ground to obtain a slurry. Then the slurry was coated on a FTO glass (2 cm×1.5 cm) by doctor-blade method. Finally,

2.3. Characterization X-ray diffraction (XRD) patterns were recorded on a Philips X′Pert PRO diffractometer (PANalytical B.V., Holland) with Cu Kα radiation (λ=1.5406 Å). The morphologies of as-prepared samples were observed on a TECNAI G2 20 transmission electron microscope (TEM, FEI, Holland). X-ray photoelectron spectroscopic (XPS) analysis was carried 1067


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Ag content. When the silver content increases to 1%, the particle size decreases to the minimum and would not change any more with further increase of Ag content. According to the HRTEM image inserted in Fig. 2c, the interplanar spacing of 0238 nm matches with the (111) crystal plane of metallic Ag, while the lattice distance of 0.209 nm corresponds to the (200) plane of periclase MgO. The result further indicates the existences of metallic Ag and MgO phases in Ag-doped MgO samples, which is in accordance with the XRD analysis. XPS technique was conducted to investigate the chemical states of elements of 1% Ag-doped MgO. The wide-scan spectrum presented in Fig. 3a confirms the elemental signals from carbon (C), oxygen (O), magnesium (Mg) and silver (Ag) atoms in the sample. The C element is ascribed to absorbed carbon species. The high resolution spectrum of Ag 3d is shown in Fig. 3b, which can be deconvoluted into two couple of peaks. The bimodal peaks located at 374.6 eV (AgI) and 368.6 eV (AgIII) could be assigned as the Ag 3d5/2 and Ag 3d3/2 characteristics for metallic silver (Ag°), and another couple located at 373.9 eV (AgII) and 367.9 eV (AgIV) could be attributed to the Ag 3d5/2 and Ag 3d3/2 characteristics for Ag+(Ag-O) [36]. This result clearly reveals that Ag element exists in the forms of Ag° and Ag+ in the Ag-doped MgO sample. Compared with the O 1s spectrum of pure MgO (Fig. 3c) which could be divided into two sub-peaks at 532.30 eV (OI) and 531.15 eV (OII), the O 1s spectrum of 1% Ag-doped MgO (Fig. 3d) is composed of three sub-peaks at 532.29 eV (OI), 531.36 eV (OII) and 529.53 eV (OIII), respectively. The OI peak could be attributed to the adsorbed oxygen, while the OII peak is obviously related to the lattice oxygen of MgO [3,17,37]. Notably, OII peak slightly shifts to higher binding energy compared to pure MgO, which is probably assigned to the formation of Mg–O···Ag bond [38]. Moreover, The OIII sub-peak may be interpret as the formation Ag–O bond [39]. Besides, XPS quantitative analysis is proceeded to investigate the content of adsorbed oxygen. The ratio of OI to OII (OI/OII) is 0.951 for 1% Ag-doped MgO, which is much larger than that of pure MgO (0.496), which suggests that Ag doping can improve the adsorbed oxygen content.

the glass electrodes were calcined at 300 °C for 30 min. And a 0.1 M Na2SO4 aqueous solution was employed as the electrolyte solution. Impedance was measured at open circuit potential at the frequency ranging from 10 kHz to 10 MHz with an AC voltage magnitude of 10 mV. All the measurements were carried out at room temperature. 3. Results and discussion 3.1. Characterization of Ag-doped MgO nanoparticles Fig. 1a shows the XRD patterns of the precursors before calcination. Only a broad hump is observed for each precursor, indicating the amorphous nature of the precursors. It is noteworthy that a distinguishable diffraction peak at 2θ=29.9° can be observed for the precursor of 3% Ag-doped MgO, which is probably due to the existence of silver nitrate (JCPDS 1–0856). This result suggests that excess Ag dopants (3%) would disrupt the sol-gel system. After being calcined at 600 °C for 2 h, the amorphous precursors turn into crystallized compounds (Fig. 1b). Among all the products, the diffraction peaks at 2θ=36.9, 42.9, 62.2, 74.6 and 78.5° can be indexed to (111), (200), (220), (311) and (222) crystallographic plane of periclase MgO phase (JCPDS 87-0652), respectively. Notably, the intensity of the strongest diffraction peak (2θ=42.9°) decreases and the full width at half maximum (FWHM) increases when Ag is doped. This result demonstrates that Ag doping can affect the crystallization and grain growth of MgO. Meanwhile, the magnified XRD patterns of calcined samples (insert in Fig. 1b) suggest the strongest diffraction peak of MgO shifts to smaller angle when Ag is doped, indicating the increase of interplanar spacing of MgO [32,33]. This is a powerful evidence for the doping of Ag into the lattice of MgO. In addition to the diffraction peaks of MgO, all other diffraction peaks of the Ag-doped samples can be assigned to the metallic silver phase with face-centred cubic structure (JCPDS 87-0597), and no diffraction peak of silver-containing substance is detected. The results indicate that the Ag-doped MgO samples are composed of metallic Ag and MgO phases. Interestingly, metallic Ag phase exists even at low amount of dopant (0.5% Ag), which indicates that the solid solubility of Ag in MgO is very low. It can be attributed to the larger ionic radius of Ag+ compared to Mg2+ and the high-temperature calcination at 600 °C [34,35]. Fig. 2 shows the TEM images of pure MgO and Ag-doped MgO samples. It is clearly observed that the morphology of pure MgO particles is irregular shaped nanoplates with an average diameter of ca. 30 nm (Fig. 2a). However, the average particle size becomes smaller when Ag is doped. This is probably due to the inhibition of Ag doping towards the crystallization and crystal growth of MgO particles. Besides, the average particle size decreases along with an increase of

3.2. Antibacterial activity of Ag-doped MgO nanoparticles The antibacterial activity of as-prepared samples was examined against E. coli ATCC25922. Fig. 4 presents the plots of antibacterial efficiency of pure MgO and Ag-doped MgO samples. In the control experiment, the bacterial population keeps unaltered within 30 min, which suggests that bacterial cells would not be self-inactivated under the test condition. When employing pure MgO as an antibacterial agent, the bacterial cell density is reduced by only one order of magnitude (i.e. 1-log). However, the Ag-doped MgO samples exhibit much better antibacterial activities compared to pure MgO.

Fig. 1. XRD patterns of the precursors (a) and calcined products (b) of pure MgO and Ag-doped MgO.

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Fig. 2. TEM images of pure MgO (a), 0.5% Ag-doped MgO (b), 1% Ag-doped MgO (c) and 2% Ag-doped MgO (d).

much higher than that for pure MgO (4.85 ± 0.18 μM). These results further illustrate that more ROS would be generated for the Ag-doped MgO sample. EIS measurements are usually used to investigate the electrontransfer resistance. The Faradaic impedance spectra of pure MgO and 1% Ag-doped MgO are presented as Nyquist plots (Z” versus Z′) in Fig. 5b. The radius of the semicircles in Nyquist diagram represents the electron-transfer resistance at contact interface. It can be seen that the arc radius of 1% Ag-doped MgO is much smaller than that of pure MgO, suggesting a lower electron-transfer resistance. That means a more efficient electron transfer for 1% Ag-doped MgO, which is beneficial for the single-electron reduction of adsorbed oxygen to generate ROS. The contact interaction between bacterial cells and nanoparticles was also considered as one of the primary factors for the antibacterial property of MgO nanoparticles [8]. The partition experiments, which use semipermeable membrane and anion exchange membrane to part bacterial cells and as-prepared samples in the bacterial inactivation tests, were employed to explore the antibacterial mechanism of Agdoped MgO. As shown in Fig. 5c, nearly 1-log of bacterial cells will be inactivated by pure MgO, while 1% Ag-doped MgO can inactivate 5-log of E. coli cells within 2 h. It suggests that these two antibacterial agents

Surprisingly, 1% Ag-doped MgO shows the best antibacterial activity, which can inactivate 7-log bacterial cells within 20 min. When further increasing the Ag dopant, the antibacterial activity of 2% Ag-doped MgO decreases instead. It is assumed that the more formed Ag nanoparticles will occupy the defect sites on the surface of MgO particles and thus hinder the adsorption of oxygen to produce ROS. 3.3. Antibacterial mechanism of Ag-doped MgO Superoxide radical (·O2−) production was widely accepted as one of the main reasons for the antibacterial property of MgO nanoparticles [10,13,14,40,41]. The generation of ·O2− was quantitatively measured by the degradation of NBT. As shown in Fig. 5a, there is no decomposition of NBT itself, implying NBT is quite stable in the present system. However, when MgO or 1% Ag-doped MgO is added, there is an obvious decrease of NBT within 30 min, indicating the generation of ·O2−. Notably, more NBT would be degraded relatively for 1% Ag-doped MgO in comparison with pure MgO, which implies that more ·O2− would be produced for 1% Ag-doped MgO. Furthermore, the generated ·O2− will react with H+ to produce H2O2, which can be measured by KMnO4 titration method. It is found that the concentration of produced H2O2 for 1% Ag-doped MgO (10.55 ± 0.36 μM) is 1069


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Fig. 3. XPS survey spectrum for 1% Ag-doped MgO (a) and high resolution spectra of Ag 3d for 1% Ag-doped MgO (b), O 1s for pure MgO (c), and O 1s for 1% Ag-doped MgO (d).

interaction is also one of the mechanisms of Ag-doped MgO, as well as ROS generation. It was reported that the release of some metal ions from materials would also show toxicity towards bacterial cells [18,19,42]. Hence, the releases of metal ions from Ag-doped MgO were also investigated in this work. As shown in Fig. 5d, the released Mg2+ from pure MgO and 1% Ag-doped MgO increases at initial stage and finally reaches at a level of 4.61 and 4.41 μg/mL, respectively. The low concentrations of Mg2+ would not result in any significant toxicity to E. coli cells [7,8,13,42]. Significantly, an extremely low concentration of Ag+(0.03 μg/mL) is detected for 1% Ag-doped MgO, which is much smaller than the reported minimum inhibitory concentration (MIC) of Ag+(0.50 μg/mL) [43]. Obviously, the release of Mg2+ and Ag+ from Ag-doped MgO does not play the leading role in bacterial inactivation. According to the above results, Ag doping results in the improvement of ROS production and further superior antibacterial activity. Firstly, MgO particle size becomes smaller when Ag is doped. Ag-doped MgO with smaller particles has higher specific surface area and higher concentration of surface defects. Secondly, when a small amount of Ag is doped into MgO crystal, part Mg2+ would be substituted by Ag+. To keep an overall neutral charge, oxygen vacancy will be generated accordingly [44]. Thirdly, Ag doping could make the electron-transfer resistance of MgO nanoparticles decrease, and accelerate the transfer of electron to the surface to generate ·O2− by single-electron reduction of adsorbed oxygen on oxygen vacancy. In brief, the enhancement of ROS production and the contact interaction between nanoparticles and E. coli bacterial cells lead to the promotion of antibacterial activity of Ag-doped MgO nanoparticles.

Fig. 4. Bacterial inactivation of pure MgO and Ag-doped MgO samples.

can function without direct interaction with bacterial cells, and thus confirming the importance of ROS. Since ROS is predominantly responsible for two bacterial inactivation systems, the superior antibacterial activity of 1% Ag-doped MgO could be ascribed to the higher concentration of ROS induced by Ag doping. Notably, compared with the non-partition experiments (Fig. 4), the bacterial inactivation efficiencies of 1% Ag-doped MgO and pure MgO are lower in partition experiments. This result indirectly demonstrates that the contact 1070


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Fig. 5. Transformation percentage of NBT concentration (a), Nyquist plots (b), bacterial inactivation in partition experiments (c), and leakages of metal ions (d) for pure MgO and 1% Ag-doped MgO.

4. Conclusion

& Technology.

In this work, Ag-doped MgO nanoparticles were prepared by a citric acid-assist sol-gel method. Compared with pure MgO, Ag-doped MgO samples exhibit smaller particle size and higher concentration of surface defects. XRD and XPS studies prove that Ag-doped MgO samples are composed of metallic Ag and MgO phases, and a small amount of Ag is doped into MgO crystal. The antibacterial activity tests reveal that the Ag-doped MgO samples show much stronger antibacterial activity than pure MgO, and 1% Ag-doped MgO can inactivate effectively 7-log bacterial cells within 20 min. The antibacterial mechanism of Ag-doped MgO nanoparticles is mainly attributed to the ROS production and contact interaction between nanoparticles and bacterial cells, while the release of Mg2+ and Ag+ ions almost makes no contribution to the bacterial inactivation. On the one hand, Ag doping can result in smaller particle size and more surface defects, facilitating the adsorption of oxygen on the surface of nanoparticles. On the other hand, Ag doping will decrease the resistance of electron transfer, in favour of one-electron reduction of adsorbed oxygen to generate more amounts of ·O2−.

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Acknowledgement The authors gratefully acknowledge the support from the National Natural Science Foundation of China (No. 50902054) and the Fundamental Research Funds for the Central Universities (2014TS025). The authors also acknowledge the technical support from Analytical and Testing Center of Huazhong University of Science 1071


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