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The Antibacterial Activity of Ta-doped ZnO Nanoparticles
© Guo et al. 2015
- Received: 12 May 2015
- Accepted: 10 August 2015
- Published: 21 August 2015
A novel photocatalyst of Ta-doped ZnO nanoparticles was prepared by a modified Pechini-type method. The antimicrobial study of Ta-doped ZnO nanoparticles on several bacteria of Gram-positive Bacillus subtilis (B. subtilis) and Staphylococcus aureus (S. aureus) and Gram-negative Escherichia coli (E. coli) and Pseudomonas aeruginosa (P. aeruginosa) were performed using a standard microbial method. The Ta-doping concentration effect on the minimum inhibitory concentration (MIC) of various bacteria under dark ambient has been evaluated. The photocatalytical inactivation of Ta-doped ZnO nanoparticles under visible light irradiation was examined. The MIC results indicate that the incorporation of Ta5+ ions into ZnO significantly improve the bacteriostasis effect of ZnO nanoparticles on E. coli, S. aureus, and B. subtilis in the absence of light. Compared to MIC results without light irradiation, Ta-doped ZnO and pure ZnO nanoparticles show much stronger bactericidal efficacy on P. aeruginosa, E. coli, and S. aureus under visible light illumination. The possible antimicrobial mechanisms in Ta-doped ZnO systems under visible light and dark conditions were also proposed. Ta-doped ZnO nanoparticles exhibit more effective bactericidal efficacy than pure ZnO in dark ambient, which can be attributed to the synergistic effect of enhanced surface bioactivity and increased electrostatic force due to the incorporation of Ta5+ ions into ZnO. Based on the antibacterial tests, 5 % Ta-doped ZnO is a more effective antimicrobial agent than pure ZnO.
- Ta-doped ZnO
- Photocatalytical inactivation
- Minimum inhibitory concentration
- Antibacterial activity
In recent years, ZnO has received increasing attention, owing to its unique optical, electrical, and chemical properties . Among these properties, degradation of pollutants catalyzed by ZnO has been studied widely so far [2–4]. Furthermore, ZnO appears to strongly resist microorganisms [5, 6]. Some work on the considerable antibacterial activity of bulk and nanosized ZnO materials has been reported [7–10].
Antibacterial agents are of relevance to a number of industrial sectors including environmental, water disposal, food, synthetic textiles, packaging, healthcare, medical care, as well as construction and decoration. They can be classified into two types, organic and inorganic ones. Most organic antibacterial agents are sensitive to temperature or pressure , while inorganic materials such as metal and metal oxide  have received more recognition over the past decade due to superior durability, less toxicity, greater selectivity, and heat resistance [13, 14]. TiO2 and ZnO semiconductors have been extensively studied as antimicrobial agents due to their photocatalytic activity under UV light [15, 16].
ZnO, as a semiconductor with a wide band gap (3.3 eV), is abundant in nature and environmentally friendly with low price. ZnO nanoparticles have been reported to exhibit strong antibacterial activities on a broad spectrum of bacteria [7–11]. A comparative study showed that for Bacillus subtilis and Escherichia coli, biocidal activity generally increased from SiO2 to TiO2 to ZnO . ZnO has higher bactericidal efficacy on B. subtilis than on E. coli . The minimum inhibitory concentration (MIC) was dependent on the ZnO particle size, ranging from 2000 to 12,500 ppm for B. subtilis and 50,000 to 100,000 ppm for E. coli . However, contradictory results have been reported on the impact of particle size on the antibacterial activity of ZnO [17, 18]. Up to now, the antibacterial mechanism of ZnO is still under investigation and not well understood . Several possible mechanisms, including the penetration of the cell envelope and disorganization of bacterial membrane , the photocatalytically generated reactive oxygen species (ROS) on oxide surface , and Zn2+ ion binding to the membranes of microorganisms , have been suggested.
ZnO has high UV absorption efficiency and good transparency to visible light. In order to improve its photocatalytic properties, some metal ions or doping nitrogen have been added into ZnO to narrow or split the band gap and enhance interfacial electron-transfer rate [21–23]. Some transition metal ions, e.g., Co2+ , Mn2+ , Ti4+ , La3+ , and Fe3+ , have been doped into ZnO. At present, most research focused on the influence of transition metal ions on the photocatalytic efficiency rather than the antimicrobial activity [22, 23].
Our group has first prepared Ta-doped ZnO nanopowders by a modified Pechini-type method and deeply investigated the photoinduced degradation of organic dye of methylene blue using Ta-doped ZnO with various Ta contents under visible light irradiation [28, 29]. In this work, we performed the antibacterial study of Ta-doped ZnO nanoparticles on several bacteria of Gram-positive Bacillus subtilis (B. subtilis) and Staphylococcus aureus (S. aureus) and Gram-negative Escherichia coli (E. coli) and Pseudomonas aeruginosa (P. aeruginosa) using a standard microbial method. The Ta concentration effect on the MIC of various bacteria has been evaluated. The antimicrobial activity of Ta-doped ZnO under visible light and dark conditions was examined and compared. The possible antimicrobial mechanism in Ta-doped ZnO systems was also proposed.
Preparation of Ta-doped ZnO Nanoparticles
A photocatalyst of Ta-doped ZnO with various Ta contents of 1, 3, and 5 % (mol. percentage) and pure ZnO was prepared by a modified Pechini-type method . All chemicals were analytical grade and used without further purification. Zinc nitrate Zn(NO3)2·6H2O and the water-soluble peroxo-citrato-tantalum were chosen as precursors of Zn and Ta, respectively. The synthesis of home-made water-soluble peroxo-citrato-tantalum has been described elsewhere in details . Deionized water was used as a dispersing agent in all the experiments.
Citric acid (CA) as chelating agent was dissolved into 50 ml water with 2.98 g Zn(NO3)2·6H2O (in 2:1 molar ratio with respect to the zinc nitrate). Ethylene glycol (EG) as cross-linking additive was added into the aqueous Ta precursor solution at the molar ratio of EG to CA of 5:1. As surfactant and catalyst, 1 g polyvinyl pyrrolidone (PVP, average mol. wt. 100,000) and 0.5 ml HNO3 were added to the mixture of solutions containing Zn and Ta, respectively. Hydroxypropyl cellulose (HPC, average mol. wt. 100 000, Aldrich) with a concentration 3.5 × 10−3 g/ml and 1 g acetylacetone were put into the above solution as steric dispersant and stabilizer, respectively. A colorless transparent sol was obtained and subsequently baked at 140 °C for 12 h for polyesterification. The resultant dark gray glassy resin finally underwent a two-step heat treatment to yield the final products: firstly, pyrolysis at 400 °C for 2 h and then annealing at 700 °C for 1 h in air.
In addition, control sample of Ta2O5 (99.5 wt %) powders was purchased from Shanghai Chemicals Corporation for control experiment.
Characterization of Ta-doped ZnO Nanoparticles
The structure of the particles was characterized by a powder X-ray diffraction (XRD) equipment (D/max2000, Rigaku) using Cu Ka radiation. The Ta-doping content was determined by inductively coupled plasma resonance (ICP, JY 38S, JY). The morphology and microstructure of nanoparticles were examined by scanning electron microscope (SEM, Philips XL-30, The Netherlands) and transmission electron microscope (TEM, Tecnai G2 F20, Philips). The surface chemical composition of the nanoparticles were investigated by X-ray photoelectron spectroscopy (XPS, Thermo Fisher K-Alpha) with standard Al Kα (1486.7 eV) X-ray source. The binding energy scale was calibrated using the energy position of the adventitious C 1s peak at 284.6 eV.
Bacterial Strains and Culture Conditions
For antibacterial experiments, Gram-positive B. subtilis and S. aureus and Gram-negative E. coli and P. Aeruginosa were four etiological agents of several infective diseases in humans, chosen as the target organism. E. coli (ATCC25922), S. aureus (ATCC6538), B. subtilis (CMCC63501), and P. aeruginosa (ATCC 27853) were purchased from Guangzhou Microbiology Research Center. All tubes and materials were sterilized in an autoclave before the experiments. Nutrient broth was used to culture E. coli, S. aureus, B. subtilis, and P. aeruginosa at 37 °C for 2 days on a rotary platform in an incubator. The liquid cultures were finally diluted to obtain bacterial cell concentration of approximately 107 colony-forming units (CFU)/ml for following antibacterial test.
Evaluation of Antibacterial Activity
The MIC of Ta-doped ZnO nanoparticles was measured by broth dilution test in dark condition. Phosphate buffered saline (PBS, 2.5 ml) and broth solution (2.5 ml) were added to the tubes containing the 107 CFU inoculation. Then, Ta-doped ZnO nanoparticles with various amounts of 100–1000 μg/ml were added into the tubes. The negative control tube did not contain any inoculum, and positive control tube was free of antibacterial agent. The tubes were incubated at 37 °C for 48 h on a rotary platform. The visual turbidity of the tubes was noted before and after incubation. The MIC was defined as the endpoint where no visible turbidity could be detected.
The antibacterial activity of Ta-doped ZnO nanoparticles was also evaluated under visible light illumination. The tube samples containing various bacteria were prepared as above. Based on the MIC results, the concentration of antibacterial agent suspensions in tubes was set to 160 μg/ml for B. subtilis and 100–200 μg/ml for E. coli, S. aureus, and P. aeruginosa, respectively. A 300-W Xe arc lamp (300W, Ushio) was located 15 cm away from the tubes, providing the visible light above 425 nm through a cut-off filter. After visible light irradiation for various durations of 0–240 min, the tubes were cultured for at 37 °C on a rotary platform. The cultivation time in an incubator was equal to the irradiation time. The growth curve was determined by measuring the time evolution of the optical density (OD) of the sample contained in a 10-mm optical path length quartz cuvette. The density of bacterial cells in the liquid cultures was estimated by OD measurements at 600 nm wavelength using a UV-vis-NIR spectrophotometer (UV-3600, Shimadzu) at a frequency of once every 20 min.
In order to make a comparative study, pure ZnO and Ta2O5 powders were also used as control samples for antibacterial test under visible light and dark ambient. The control tubes were prepared and incubated under the similar conditions.
To investigate the antibacterial behavior of Ta-doped ZnO nanoparticles, SEM were also used to examine the morphology of some bacteria samples with and without antimicrobial treatment under visible light and dark ambient.
Characterization of Ta-doped ZnO Nanoparticles
Antibacterial Test Results
MIC results of ZnO and Ta-doped ZnO with various Ta contents (unit: μg/ml)
1 % Ta-doped
3 % Ta-doped
5 % Ta-doped
Many bacteriological tests have shown that ZnO suspensions in the lower concentration range (0.01–1 mM, i.e., 0.8–80 μg/ml) exhibit less antimicrobial activity [31, 32]. Our MIC results also confirm this point. Fewer Zn2+ ions might act as nutrient-a supplement promoting the metabolic action of bacteria at trace concentrations. So, usually, ZnO are believed to be nontoxic, biosafe, and biocompatible and have been used in many applications in daily life, such as drug carriers, in cosmetics, and fillings in medical materials.
In addition, compared to MIC result under dark conditions, the visible light irradiation has a hardly significant influence on antibacterial activity of B. subtilis at 160 μg/ml concentration (see Fig. 3 d). For samples containing pure ZnO and 3 % Ta-doped ZnO nanoparticles, the gradually enhanced OD with time indicates the worse microbial control on B. subtilis, similar to the previous MIC results. Five percent Ta-doped ZnO nanoparticles show also similar antibacterial activity of B. subtilis under visible light and in the absence of light. The only exception is that 1 % Ta-doped ZnO nanoparticles exhibit slightly enhanced biocidal effect on B. subtilis. Maybe it is related to the fact that 1 % Ta-doped ZnO nanoparticles has optimal photocatalytical activity in Fig. 4 .
Although the anti-treatments of the bacteria with Ta-doped ZnO nanoparticles under dark and visible light ambient lead to considerable damage to cell membranes, compared to the MIC under dark ambient, the antibacterial effect is significantly enhanced in visible light. The anti-treatment on P. aeruginosa, E. coli, S. aureus, and B. subtilis for 10 min under visible light illumination by photocatalysis produces similar injury effect to that for 48 h in the absence of light by MIC in Fig. 6. Evidently, the antibacterial mechanism of ZnO and Ta-doped ZnO under visible light is different from under dark ambient.
Under visible light irradiation, an electron-hole pair forms, and then a conduction-band electron and a valence-band hole separate on the surface of Ta-doped ZnO (Eq. 1). The high oxidative potential of the holes can form very reactive hydroxyl groups through decomposing of water (Eq. 2). In the presence of the dissolved O2, electrons from the photoexcited Ta-doped ZnO produce superoxide anion radicals ·O2 − (Eq. 3), which subsequently could generate H2O2 by the intermediate HO2− and HO2· steps (Eqs. 4, 5). The free radicals ·O2 − and ·OH produced in the reactions can react with organic substance inside bacterial cells to produce bacterial toxins, leading to death of the bacteria. Especially, the generated H2O2 easily penetrates into the cell membrane and kills the bacteria .
The H2O2 content of different samples of 200 μg/ml at 0 and 40 min under visible light
1 % Ta
3 % Ta
5 % Ta
Recently, Yin group reported the photogenerated charge carriers and reactive oxygen species in ZnO/Au hybrid nanostructures with enhanced photocatalytic and antibacterial activity by electron spin resonance (ESR) spectroscopy . Maybe next, we may try ESR measurements to determine the generation of ROS and photoinduced charge carriers (electron or hole) of Ta-doped ZnO under visible light so as to better understand the antibacterial mechanism and clarify the correlation between charge carrier formation, generation of reactive intermediates, and antibacterial activity, especially, the role of individual ROS in antibacterial activity of photoexcited Ta-doped ZnO.
Our previous work shows the introduction of Ta5+ ions into ZnO can cause a series of changes in structure, morphology, and photocatalytical degradation of methylene blue, such as larger lattice parameter, smaller grain size, and more active defect sites and hydroxyl groups [28, 29]. Based on the antimicrobial study on Ta-doped ZnO nanoparticles, the incorporation of Ta5+ ions indeed improves the biological activity in dark ambient in most cases. The MIC results show that except the P. aeruginosa samples, the Ta-doping significantly enhances the bacteriostasis effect of ZnO nanoparticles on E. coli, S. aureus, and B. subtilis in the absence of light. Usually, ZnO particles directly adsorbed to the cell walls may inhibit bacterial growth by penetration of the cell envelope and disorganization of bacterial membrane. The cell wall rupture is related to the surface activity of ZnO in contact with the bacteria.
The XPS results of ZnO and 3 % Ta-doped ZnO before and after Ar-ion etching
3 % Ta-doped ZnO
3 % Ta-doped ZnO
Additionally, for various bacteria, the antibacterial action of Ta-doped ZnO nanoparticles under visible light and dark ambient shows some differences. Under dark environment, Ta-doped ZnO nanoparticles exhibit very weak bacteriostasis effect on P. aeruginosa, but in visible light irradiation, strong bactericidal efficacy on P. aeruginosa is observed. For B. subtilis, the action of the photocatalysis of Ta-doped ZnO seems to be limited. These phenomena might be related to various structures and functions of several bacteria. Further in-depth work is needed.
Above all, according to our antibacterial tests, 5 % Ta-doped ZnO is a more effective antimicrobial agent than pure ZnO.
In summary, novel photocatalyst of Ta-doped ZnO nanoparticles was prepared by a modified Pechini-type method. The antibacterial activity of Ta-doped ZnO nanoparticles on several bacteria of P. aeruginosa, S. aureus, E. coli, and B. subtilis were investigated using a standard microbial method. The Ta-doping concentration effect on MIC of various bacteria under dark ambient has been evaluated. The photocatalytical biocidal behavior of Ta-doped ZnO nanoparticles under visible light irradiation was also characterized. The MIC results indicate that the incorporation of Ta5+ ions into ZnO significantly improve the bacteriostasis effect of ZnO nanoparticles on E. coli, S. aureus, and B. subtilis in the absence of light. Compared to MIC results without light irradiation, Ta-doped ZnO and pure ZnO nanoparticles show much stronger bactericidal efficacy on P. aeruginosa, E. coli, and S. aureus under visible light illumination. The possible antibacterial mechanisms in Ta-doped ZnO systems under visible light and dark conditions have been proposed. Ta-doped ZnO nanoparticles exhibit more effective bactericidal efficacy than pure ZnO in dark ambient, which can be attributed to the synergistic effect of enhanced surface bioactivity and increased electrostatic force due to the incorporation of Ta5+ ions into ZnO. Based the antibacterial tests, 5 % Ta-doped ZnO is a more effective antimicrobial agent than pure ZnO.
This project is supported by the Natural Science Foundation of China (51202107), a grant from the State Key Program for Basic Research of China (2015CB921203 and 2011CB922104). Ai-Dong Li also thanks the support from Open Project of National Laboratory of Solid State Microstructures (M27001), PAPD in Jiangsu Province, and Doctoral Fund of Ministry of Education of China (20120091110049).
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