Next Article in Journal
Enhanced Optoelectronic Performance of Yellow Light-Emitting Diodes Grown on InGaN/GaN Pre-Well Structure
Next Article in Special Issue
Efficient Route for the Preparation of Composite Resin Incorporating Silver Nanoparticles with Enhanced Antibacterial Properties
Previous Article in Journal
Role Played by Edge-Defects in the Optical Properties of Armchair Graphene Nanoribbons
Previous Article in Special Issue
Plasmonic Gold Nanoisland Film for Bacterial Theranostics
 
 
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Palygorskite-Based Organic–Inorganic Hybrid Nanocomposite for Enhanced Antibacterial Activities

Key Laboratory of Clay Mineral Applied Research of Gansu Province, Center of Eco-Material and Green Chemistry, Lanzhou Institute of Chemical Physics, Chinese Academy of Sciences, Lanzhou 730000, China
*
Author to whom correspondence should be addressed.
Nanomaterials 2021, 11(12), 3230; https://doi.org/10.3390/nano11123230
Submission received: 31 October 2021 / Revised: 17 November 2021 / Accepted: 25 November 2021 / Published: 28 November 2021
(This article belongs to the Special Issue Antibacterial Applications of Nanomaterials)

Abstract

:
A synergistic antibacterial strategy is effective in enhancing the antibacterial efficacy of a single antibacterial material. Plant essential oils (PEOs) are safe antibacterial agents. However, some of their characteristics such as intense aroma, volatility, and poor thermal stability limit their antibacterial activity and applications. In this paper, five kinds of PEOs were incorporated onto ZnO/palygorskite (ZnO/PAL) nanoparticles by a simple adsorption process to form organic–inorganic nanocomposites (PEOs/ZnO/PAL) with excellent antibacterial properties. TEM and SEM analyses demonstrated that ZnO nanoparticles uniformly anchored onto the surface of rod-like PAL, and that the structure of ZnO/PAL maintained after the incorporation of ZnO nanoparticles and PEOs. It was found that carvacrol/ZnO/palygorskite (CAR/ZnO/PAL) exhibited higher antibacterial activities than other PEOs/ZnO/PAL nanocomposites, with minimum inhibitory concentration (MIC) values of 0.5 mg/mL and 1.5 mg/mL against Escherichia coli (E. coli) and Staphylococcus aureus (S. aureus), respectively. Moreover, the antibacterial efficiency of CAR/ZnO/PAL nanocomposites was superior to that of ZnO/PAL and pure CAR, demonstrating the synergistic effect that occurs in the combined system. PAL serving as a carrier for the combination of organic PEOs and ZnO nanoparticles is an effective strategy for enhanced, clay-based, organic–inorganic hybrid antibacterial nanocomposites.

Graphical Abstract

1. Introduction

Plant essential oils (PEOs) and their extracts have been examined for their effectiveness in food preservation [1,2,3,4,5]. PEOs as naturally occurring, biologically active agents have been shown to possess anti-inflammatory, antioxidant, antibacterial, and antifungal properties [6,7,8]. Recently, there has been a growing demand for natural PEOs in antibacterial applications owing to their safety and extensive sources such as plant leaves, barks, stems, roots, flowers, and fruits [9,10,11,12,13]. The good antibacterial activity of PEOs may be attributed to the hydrophobicity that could damage the bacterial cell membrane and cause the leakage of the internal contents of the cells [3,14,15,16]. Nevertheless, PEOs also suffer from the problems of volatility, tangy aromatic odor, and poor thermal stability, which would diminish their antibacterial activity as well as limit their practical applications [17,18]. A lot of research has demonstrated that PEO-based nanocomposites have been designed to overcome these issues. In addition, PEOs show more sensitivity toward Gram-positive bacteria than Gram-negative bacteria. Building microencapsulation or emulsion is a classical method of combining a variety of PEOs, while another effective strategy is to composite inorganic metal oxide with PEOs [19,20]. Furthermore, it is known that the complexes of various antibacterial components could obtain synergistic antibacterial effects, thus making it a feasible route for utilizing the advantages of various antibacterial factors.
Metal oxide such as ZnO, MgO, and TiO2 are all very efficient in inhibiting the growth of bacteria, and these antibacterial materials show better antibacterial properties against Gram-negative bacteria than Gram-positive bacteria [21,22,23,24,25]. Therefore, taking advantage of PEOs and metal oxide may be a facile approach to the building of synergistic antibacterial composites [3,6,26]. Among these metal oxides, ZnO exhibits excellent antibacterial activity toward foodborne pathogens such as Escherichia coli (E. coli) and Staphylococcus aureus (S. aureus) [21,22,27,28,29].
Interestingly, ZnO nanoparticles (NPs) can be loaded onto clay-based carriers, which could effectively avoid the agglomeration of ZnO NPs [30,31,32,33]. Palygorskite (PAL), as a naturally available one-dimensional nanomaterial, a special crystal structure, stacking mode, and nanometric dimension, endowing it with plentiful pores, a high aspect ratio, good ion-exchange capacity, and affluent surface groups [34,35,36]. PAL as a carrier could load inorganic NPs as well as immobilize organic molecules. Yang’s group and Osajima’s group have reported ZnO/PAL nanocomposites and found that the antibacterial properties of ZnO against E. coli could be improved through conducting nanocomposites [32,37]. In our previous work, ZnO/PAL were prepared in the presence of surfactants using an easy-to-operate hydrothermal method and chemical deposition [31,38]. Incorporating PEOs onto ZnO/PAL nanoparticles is expected to obtain highly efficient and broad-spectrum antibacterial materials.
In this paper, an ultrasonic-assisted dipping method was used to incorporate PEOs onto a ZnO-loaded PAL nanoparticles to build organic–inorganic nanocomposites with broad-spectrum antibacterial capabilities. PAL as a carrier can effectively immobilize PEOs and ZnO NPs, reducing the volatility of PEOs and showing synergistic antibacterial performance. The preparation parameters of ZnO/PAL such as the variety of alkaline, amount of PAL, reaction temperature, and time were optimized based on antibacterial properties. The antibacterial activities of PEOs/ZnO/PAL nanocomposites formed by different PEOs were evaluated, and the synergistic antibacterial effects and synthesis mechanism were also discussed.

2. Materials and Methods

2.1. Materials

PAL originated from the Huangnishan Mine and was provided by Huida Mineral Technology Co. Ltd., Huaian, China. It was crushed and purified by 2% H2SO4 solution at the solid/liquid ratio of 1:10 to remove the associated carbonates. The purified PAL was filtered by passing it through a 200-mesh sieve for further use. The chemical composition is as follows: SiO2, 57.39%; Al2O3, 8.41%; MgO, 12.21%; Fe2O3, 5.05%; Na2O, 2.03%; K2O, 0.9%; CaO, 1.35%, and the value of specific surface area was 209.3 m2/g. Zinc nitrate hexahydrate (Zn(NO3)2·6H2O, 99.0%), sodium hydroxide (NaOH, 96.0%), and ethanol were purchased from Tianjin Kermel Chemical Regent Co., Ltd., Tianjin, China). The PEOs of citral (97%, cis + trans), thymol (>99%), carvacrol (CAR, 99%), oregano oil (carvacrol 85%, thymol 6%), and cinnamaldehyde (98%) were bought from Shanghai Macklin Biochemical Co., Ltd. (Shanghai, China). The chemicals were directly used without further purification, and distilled water was used throughout the experiment.

2.2. Preparation of PEOs/ZnO/PAL

The PEOs were incorporated onto PAL and ZnO/PAL by a simple dipping method. In order to synthesize the PEOs/PAL nanocomposites, 2 g of purified PAL was added to a PEO ethanol solution (10%, w/v), and the mixture was ultrasonically dispersed for 30 min and shocked for 24 h with 160 r/min. The powder was subsequently collected by centrifugation and dried at 45 °C for 12 h in an oven. CAR/PAL nanocomposites with various concentrations of CAR (1%, 2.5%, 5%, 10%, 20%) were synthesized by the same process. ZnO/PAL nanoparticles were prepared by chemical deposition and calcination method (Hui et al., 2020; Huo et al., 2010); the preparation conditions and antibacterial activities of ZnO/PAL nanoparticles are shown in Table S1.

2.3. Characterization

The chemical composition of PAL was determined using a Minipal 4 X-ray fluorescence spectrometer (PANalytical, The Netherlands, Germany). Morphological evolution of the samples was observed using a field emission scanning electron microscopy (SEM, JSM-6701F, JEOL, Tokyo, Japan) and a transmission electron microscope (TEM, JEM-1200EX, JEOL, Tokyo, Japan). X-ray diffraction (XRD) patterns were acquired on an X’ Pert PRO diffractometer equipped with a Cu Kα radiation source, 40 mA, and 40 kV at a scanning rate of 0.02° per second. Fourier Transform infrared (FTIR) spectra were measured on a Nicolet NEXUS spectrometer (Thermo Fisher Scientific, Waltham, Massachusetts, America) in the range of 4000–400 cm−1 using potassium bromide pellets. Nitrogen adsorption–desorption isotherms were recorded using the Brunauer–Emmett–Teller analysis (BET, Micromeritics, Norcross, Georgia, America). Thermogravimetric analyses (TG) were performed on the simultaneous thermal analyzer (STA6000, PerkinElmer, America), operating from 30 °C to 800 °C, with a heating rate of 10 °C/min in a nitrogen atmosphere.

2.4. Antibacterial Assay

Antibacterial activities of the samples were evaluated by examining the minimum inhibitory concentration (MIC) value against Gram-negative E. coli (CVCC1524, C83698, O8: K91) and Gram-positive S. aureus (CVCC1885, C56005) bacteria [31], which were kindly provided by China Veterinary Culture Collection Center. Bacterial strains were isolated from the Luria–Bertani agar plate, and added into fresh Luria–Bertani broth separately for incubation at 37 °C in a shaking incubator, at a speed of 160 r/min for 12 h. The strains were inoculated into the fresh medium again and cultivated for 3 h in the logarithmic phase, at a volume ratio of 1:100 of bacteria liquid and fresh medium. Then, a certain amount of sample was mixed with 40 mL of the Macconkey medium, and 1 μL fresh bacteria liquid (108 CFU/mL) was put into the medium with three parallel dots at different locations, repeated on three parallel plates for each sample. The tested plates were kept in an incubator at 37 °C for 24 h. Positive control with the exclusion of antibacterial materials on an agar plate and a blank control with no samples and bacteria liquid dots were performed under the same cultivation conditions. The MIC value was reported as the lowest concentration to completely inhibit the growth of each bacterial strain being tested.

3. Results and Discussion

3.1. Possible Formation Mechanism of PEOs/ZnO/PAL

PEOs such as citral, thymol, CAR, oregano oil, and cinnamaldehyde were selected as natural antibacterial factors. These PEOs are all small molecules with active groups such as the phenolic hydroxyly group, carbonyl group, and aldehyde group (Figure 1a), and favor adsorption onto the surface of PAL and ZnO/PAL through hydrogen bonding and weak electrostatic interaction, or by entering into the nanopores of PAL. Two steps for loading ZnO NPs and PEOs onto PAL are shown in Figure 1b. The electrostatic interaction between PAL with a negative charge and Zn2+ with a positive charge could make them self-assemble together in an aqueous solution. When Zn2+ was introduced into the reaction mixture, it assembled on the PAL surface spontaneously and uniformly. By adjusting the pH of the solution, the sheet-like Zn(OH)2 appeared and finally transformed into ZnO/PAL after calcination. For- PEOs/ZnO/PAL nanocomposites, PEO molecules were incorporated onto ZnO/PAL via a simple dipping method. PEOs with the phenolic hydroxyly group, carbonyl group, and aldehyde group could be connected with Si–OH groups on the outer surface of ZnO/PAL by hydrogen-bond interaction. In these PEOs/ZnO/PAL composites, PEOs play a vital role in enhancing the antibacterial activities of inorganic ZnO/PAL nanoparticles. Small CAR molecules displayed better antibacterial activities toward two model bacteria than other PEOs; therefore, the following work was conducted to obtain the reasonable concentrations of CAR, as shown in Figure 1b.

3.2. FTIR

In the spectrum of PAL shown in Figure 2a, the bands at 3550 cm−1, 3430 cm−1, and 1636 cm−1 are related to the stretching vibration of the coordinated water, the stretching vibration, and the antisymmetric stretching vibration of zeolitic water and adsorption water [39], while the characteristic absorption bands at 1020 cm−1 and 476 cm−1 were attributed to the stretching vibration of Si–O–Si and δSi–O, respectively [35,40,41]. In the case of PEOs/ZnO/PAL, the band at 3740 cm–1 disappeared and shifted to lower wavelengths, and a broad band appeared from 3700 cm–1 to 3400 cm–1 (Figure 2a), which indicated that the interactions between ZnO/PAL and PEOs had occurred, and that the new absorption peaks that appeared at 1660 cm−1 corresponded to the C=C or benzene ring stretching vibrations of the PEOs. The FTIR spectra of PAL containing different amounts of CAR are shown in Figure S1 and Figure 2b, the antisymmetric stretching vibration absorption bands of the CH3 group and the CH2 group were located at 2968 cm–1 and 2856 cm–1, respectively, and the symmetric stretching vibration absorption band of the CH3 group was found at 2870 cm–1 [42]. Moreover, the absorption bands at 1400–1600 cm−1, 1186 cm−1, and 800–900 cm−1 can be ascribed to the aromatic C=C stretching vibration, aromatic O–H stretching vibrations peak, and aromatic C–H bending, respectively [43].

3.3. XRD Patterns

XRD patterns of PAL, ZnO/PAL, and CAR/ZnO/PAL are shown in Figure 3. The diffraction peaks at 2θ of 8.4°, 13.7°, 16.3°, 19.8°, 19.9°, and 34.4° correspond to (110), (200), (130), (040), (310), and (102) planes of PAL, respectively [31,35,40]. It is worth noting that 2θ = 26.7° shows a characteristic peak for quartz [40], and the diffraction peaks of ZnO/PAL were located at 2θ = 31.7°, 34.4°, 36.3°, 47.6°, 56.6°, 62.9°, 66.5°, 67.9°, and 69.1°, which corresponded to (100), (002), (101), (102), (110), (103), (200), (112), and (201) of a wurtzite ZnO [21]. After the incorporation of CAR, the CAR/ZnO/PAL nanocomposites displayed a similar XRD pattern to that of ZnO/PAL, and there was an obvious change in the intensity of the diffraction peaks for PAL, which may be due to the weak interface interaction of the PEOs with ZnO/PAL.

3.4. TG Curves

The weight loss of PAL, ZnO/PAL, and CAR/ZnO/PAL was also demonstrated by the TG curves, as shown in Figure 4, where the weight loss of PAL could be divided into four steps [44]. The first step is below 100 °C, owing to the loss of superficially adsorbed water and most of the zeolitic H2O. In the second step, the residual zeolitic H2O and the first half of the structural water molecules were removed from 100 °C to 250 °C. In the third step, the loss of the residual first half of the structural water and the second half of the structural water were removed from 500 °C to 550 °C, and the removal of the second half of the structural water and the hydroxyl groups was observed in the last region at about 550–800 °C. In terms of ZnO/PAL, the weight loss is lower in comparison with PAL; in addition, it can be seen that the temperature increased to 300 °C, the CAR molecules began decomposition with the growing temperature. There are four stages of weight loss for the CAR/ZnO/PAL nanocomposites, which corresponding to the weight loss of PAL, as shown in the insert image of Figure 4. CAR molecules escaped from the surface of PAL when the temperature was at 105 °C. The maximum decomposition temperature was 315 °C, which could have been caused by the small CAR molecules that loaded onto PAL. The total weight loss of CAR/ZnO/PAL was 8.2%.

3.5. SEM and TEM

Figure 5 shows the SEM images of PAL, ZnO/PAL, and CAR/ZnO/PAL; it can be seen that PAL exhibits a rod-like morphology (Figure 5a), and ZnO NPs anchored uniformly onto the surface of PAL (Figure 5b). Moreover, after the incorporation of the CAR molecules, the morphology of ZnO/PAL nanocomposites had no clear change, but the nanorods had become loose due to the active CAR molecules adsorbed on the surface of ZnO/PAL through the hydrogen bond interaction (Figure 5c); the interfacial repulsion between the CAR molecules caused the CAR/ZnO/PAL nanocomposites to become looser. TEM was carried out to further investigate the changes in the microstructures of CAR/ZnO/PAL. As shown in Figure 6, the length of the rod-like PAL typically varies from 0.5 μm to 1.5 μm, with a diameter from 20 nm to 70 nm (Figure 6a). Meanwhile, it can be clearly observed that a number of ZnO NPs with a diameter of about 40 nm were incorporated onto the surface of rod-like PAL (Figure 6b). The morphology of ZnO/PAL was maintained after combining with the CAR molecules, confirming that ZnO NPs were loaded tightly onto the surface of PAL (Figure 6c). Moreover, compared to the previous work of mechanical milling, the dipping method is more favorable for the loading of small CAR molecules onto PAL or ZnO/PAL, and the rod-like structures are kept very well during the process; in contrast, the structure is easy to damage using the mechanical milling method [45].

3.6. BET Analysis

As shown in Table 1, the microporous surface area (Smicro) of the CAR/ZnO/PAL nanocomposites were disappeared when the CAR molecules incorporated on PAL. The Smicro, Sext, and Vtotal of the CAR/ZnO/PAL nanocomposites extremely decreased with the increasing concentrations of CAR. The specific surface area of PAL was 125 m2/g, but it decreased to 27 m2/g for PAL/ZnO, and decreased from 25 m2/g to 9 m2/g for the CAR/ZnO/PAL nanocomposites with growing concentrations of CAR. The extra surface area (Sext) also decreased with the addition of CAR. It may be due to the existence of ZnO NPs or small CAR molecules on the surface or channel of PAL, which set a big barrier for N2 molecules entering into the nanopore structure [45]. With the increasing amount of CAR, SBET and Sext obviously decreased, showing that CAR molecules could be adsorbed onto the surface of ZnO/PAL or enter into the nanopores of PAL due to the hydrogen bond interaction between the phenolic hydroxyl group of CAR and the silanol group of PAL.

3.7. Antibacterial Evaluation

E. coli and S. aureus were chosen to evaluate the antibacterial activities of the samples, including PAL, PEOs/PAL, ZnO/PAL, and PEOs/ZnO/PAL. The MIC value was defined as the lowest concentration (mg/mL) of the tested sample preventing the visible growth of a microorganism under defined conditions. The MIC results of PAL are shown in Figures S2 and S3, which were more than 50 mg/mL toward E. coli and S. aureus. As a control, PAL did not show obvious antibacterial activities against Gram-negative E. coli and Gram-positive S. aureus, and there were also no visible differences in the MIC results with different amounts of PAL toward the two model bacteria. It can be clearly observed that the microbial colony of the bacteria disappeared with the treatment of ZnO/PAL (Figure 7), which indicated that ZnO/PAL exhibited good antibacterial activities against E. coli and S. aureus; the MIC values toward E. coli and S. aureus were 1.5 mg/mL and 2.5 mg/mL, respectively.
Five kinds of PEOs were selected to be combined with ZnO/PAL in order to enhance the broad-spectrum antibacterial activities, as shown in Figure 8 (E. coli) and Figure 9 (S. aureus). The bacteria colonies of E. coli and S. aureus disappeared clearly upon contact with the PEOs/ZnO/PAL nanocomposites. In particular, five kinds of PEOs combined with ZnO/PAL nanoparticles had different antibacterial properties against the ´Gram-negative and Gram-positive bacteria. The CAR/ZnO/PAL nanocomposites and oregano oil/ZnO/PAL nanocomposites displayed better antibacterial properties toward E. coli than other PEOs/ZnO/PAL nanocomposites (Figure 8), while the CAR/ZnO/PAL nanocomposites also exhibited higher antibacterial efficacy against S. aureus (Figure 9) from among the PEOs/ZnO/PAL nanocomposites. The differences can be attributed to the distinct composition of the cell membrane and the cell wall as well as the functional groups present in different kinds of PEOs and the synergistic effects induced by the interactions of PEOs and ZnO/PAL nanoparticles [6,38,46]. The MIC value of the CAR/ZnO/PAL nanocomposites against E. coli and S. aureus reached 0.5 mg/mL and 1.5 mg/mL, respectively (Table S2).
Meanwhile, the antibacterial activities of the orange oil/ZnO/PAL nanocomposites against E. coli were the same as those of the CAR/ZnO/PAL nanocomposites due to the fact that CAR was the main component of orange oil. The antibacterial action of CAR on bacteria occurs via the change in cell membrane permeability, which results in the depletion of the intracellular ATP pool, ultimately leading to cell death [47,48]. In order to determine the superior concentration of CAR among the CAR/ZnO/PAL nanocomposites, the MIC value of the CAR/ZnO/PAL nanocomposites prepared with different concentrations of CAR against E. coli is shown in Figure 10, and the MIC evaluation of PAL with different concentrations of CAR is shown in Figure S4. It can be seen that when the concentration of CAR was maintained at 10%, the CAR/ZnO/PAL nanocomposites reached their best antibacterial activity. When the concentration of CAR further increased to 20%, the antibacterial activities did not increase, which was possibly caused by the effective amounts loaded onto ZnO/PAL. The antibacterial performance of the CAR/ZnO/PAL nanocomposites was attributed to the synergistic antibacterial effect, which can be described as follows. The nanoparticles and reactive oxygen species generated by ZnO such as superoxide, singlet oxygen, and hydroxyl radicals could damage the structural integrity of bacteria [49,50]. Meanwhile, the slow release of CAR molecules from the nanocomposites can disturb the formation of nucleic acids, protein, or cell wall synthesis [47,49,51]. Therefore, the effects of physical damage combined with the chemical adsorption and bactericidal function would create broad-spectrum antibacterial effects. In particular, when compared with the previous antibacterial materials prepared with a PAL carrier, the antibacterial activities of the CAR/ZnO/PAL nanocomposites were superior to those of single ZnO/PAL nanoparticles (1.5 mg/mL) and CAR/PAL hybrid materials (2 mg/mL) toward Gram-negative E. coli [31,43].

4. Conclusions

A series of organic–inorganic antibacterial nanocomposites with broad-spectrum antibacterial effects were prepared based on natural PEOs and ZnO/PAL nanoparticles using a dipping method with ultrasonic processing. ZnO nanoparticles with a diameter of 40 nm uniformly anchored onto the surface of rod-like PAL. TG analysis indicated the effective loading content of CAR at 8.2%. The antibacterial activities did not increase when the concentration of CAR further increased to 20%. The obtained PEOs/ZnO/PAL nanocomposites exhibited synergistic antibacterial activities against E. coli and S. aureus. Among these nanocomposites, the CAR/ZnO/PAL nanocomposites exhibited better antibacterial efficacy than other PEOs/ZnO/PAL nanocomposites, with MIC values of 0.5 mg/mL and 1.5 mg/mL toward E. coli and S. aureus, respectively. This study provides a feasible route for the preparation of broad-spectrum antibacterial materials with PEOs and inorganic antibacterial carriers.

Supplementary Materials

The following are available online at https://www.mdpi.com/article/10.3390/nano11123230/s1, Figure S1: FTIR spectra of PAL containing (a) 0%, (b) 1%, (c) 2.5%, (d) 5%, (e) 10%, (f) 20% of CAR, Figure S2: (a) Blank control, (b) positive control of E. coli, E. coli treated by PAL with different concentrations (c) 50 mg/mL, (d) 20 mg/mL, (e) 10 mg/mL, (f) 1 mg/mL, Figure S3: (a) Blank control, (b) positive control of S. aureus, S. aureus treated by PAL with different concentrations (c) 50 mg/mL, (d) 20 mg/mL, (e) 10 mg/mL, (f) 1 mg/mL, Figure S4: (a) Blank control, (b) positive control, MIC evaluation of PAL containing (c) 1%, (d) 2.5%, (e) 5%, (f)10%, (g) 20% of CAR, Table S1: Effects of preparation parameters on antibacterial activities of ZnO/PAL against E. coli, Table S2: The MIC values of PEOs/ZnO/PAL nanocomposites against E. coli and S. aureus, Table S3: The MIC values of PAL and ZnO/PAL at different concentrations of CAR against E. coli.

Author Contributions

A.H. conducted the experiment and wrote the original draft, F.Y. and R.Y. characterized and evaluated the material properties, and Y.K. and A.W. designed the experiment and revised the paper. All authors have read and agreed to the published version of the manuscript.

Funding

This work was funded by the Major Projects of the Natural Science Foundation of Gansu, China (18JR4RA001), the Natural Science Foundation of Gansu, China (21JR7RA079), and the Regional Key Project of the Science and Technology Service of the Chinese Academy of Sciences (KFJ-STS-QYZX-086).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Gyawali, R.; Ibrahim, S.A. Natural products as antimicrobial agents. Food Control 2014, 46, 412–429. [Google Scholar] [CrossRef]
  2. Hu, W.; Li, C.Z.; Dai, J.M.; Cui, H.Y.; Lin, L. Antibacterial activity and mechanism of Litsea cubeba essential oil against methicillin-resistant Staphylococcus aureus (MRSA). Ind. Crop. Prod. 2019, 130, 34–41. [Google Scholar] [CrossRef]
  3. Jayasena, D.D.; Jo, C. Essential oils as potential antimicrobial agents in meat and meat products: A review. Trends Food Sci. Tech. 2013, 34, 96–108. [Google Scholar] [CrossRef]
  4. Moon, S.H.; Waite-Cusic, J.; Huang, E. Control of Salmonella in chicken meat using a combination of a commercial bacteriophage and plant-based essential oils. Food Control 2020, 110, 106984. [Google Scholar] [CrossRef]
  5. Ni, Z.J.; Wang, X.; Shen, Y.; Thakur, K.; Han, J.Z.; Zhang, J.G.; Hu, F.; Wei, Z.J. Recent updates on the chemistry, bioactivities, mode of action, and industrial applications of plant essential oils. Trends Food Sci. Tech. 2021, 110, 78–89. [Google Scholar] [CrossRef]
  6. Calo, J.R.; Crandall, P.G.; O’Bryan, C.A.; Ricke, S.C. Essential oils as antimicrobials in food systems: A review. Food Control 2015, 54, 111–119. [Google Scholar] [CrossRef]
  7. He, F.; Wang, W.; Wu, M.C.; Fang, Y.P.; Wang, S.Z.; Yang, Y.; Ye, C.; Xiang, F. Antioxidant and antibacterial activities of essential oil from Atractylodes lancea rhizomes. Ind. Crop. Prod. 2020, 153, 112552. [Google Scholar] [CrossRef]
  8. Karpiński, T.M. Essential oils of lamiaceae family plants as antifungals. Biomolecules 2020, 10, 103. [Google Scholar] [CrossRef] [Green Version]
  9. Erasto, P.; Bojase-Moleta, G.; Majinda, R.R.T. Antimicrobial and antioxidant flavonoids from the root wood of Bolusanthus speciosus. Phytochemistry 2004, 65, 875–880. [Google Scholar] [CrossRef]
  10. Rahman, M.M.; Gray, A.I. Antimicrobial constituents from the stem bark of Feronia limonia. Phytochemistry 2002, 59, 73–77. [Google Scholar] [CrossRef]
  11. Reyes-Jurado, F.; Navarro-Cruz, A.R.; Ochoa-Velasco, C.E.; Palou, E.; López-Malo, A.; Ávila-Sosa, R. Essential oils in vapor phase as alternative antimicrobials: A review. Crit. Rev. Food Sci. 2019, 60, 1641–1650. [Google Scholar] [CrossRef]
  12. Wang, F.W.; You, H.Q.; Guo, Y.H.; Wei, Y.K.; Xia, P.G.; Yang, Z.Q.; Ren, M.; Guo, H.; Han, R.L.; Yang, D.F. Essential oils from three kinds of fingered citrons and their antibacterial activities. Ind. Crop. Prod. 2020, 147, 112172. [Google Scholar] [CrossRef]
  13. Zhu, X.F.; Zhang, H.X.; Lo, R. Phenolic compounds from the leaf extract of artichoke (leaf extract of artichoke (Cynara scolymus L.) and their antimicrobial activities. J. Agric. Food Chem. 2004, 52, 7272–7278. [Google Scholar] [CrossRef]
  14. Bajpai, V.K.; Baek, K.H.; Kang, S.C. Control of Salmonella in foods by using essential oils: A review. Food Res. Int. 2012, 45, 722–734. [Google Scholar] [CrossRef]
  15. Cui, H.Y.; Zhang, C.H.; Li, C.Z.; Lin, L. Antibacterial mechanism of oregano essential oil. Ind. Crop. Prod. 2019, 139, 111498. [Google Scholar] [CrossRef]
  16. Marchese, A.; Orhan, I.E.; Daglia, M.; Barbieri, R.; Di, L.A.; Nabavi, S.F.; Gortzi, O.; Izadi, M.; Nabavi, S.M. Antibacterial and antifungal activities of thymol: A brief review of the literature. Food Chem. 2016, 210, 402–414. [Google Scholar] [CrossRef]
  17. Chorianopoulos, N.; Kalpoutzakis, E.; Aligiannis, N.; Mitaku, S.; Nychas, G.J.; Haroutounian, S.A. Essential oils of Satureja, Origanum, and Thymus species: Chemical composition and antibacterial activities against foodborne pathogens. J. Agric. Food Chem. 2004, 52, 8261–8267. [Google Scholar] [CrossRef] [PubMed]
  18. Maggio, A.; Rosselli, S.; Bruno, M. Essential oils and pure volatile compounds as potential drugs in Alzheimer’s disease therapy: An updated review of the literature. Curr. Pharm. Des. 2016, 22, 4011–4027. [Google Scholar] [CrossRef]
  19. Akbari-Alavijeh, S.; Shaddel, R.; Jafari, S.M. Encapsulation of food bioactives and nutraceuticals by various chitosan-based nanocarriers. Food Hydrocoll. 2020, 105, 105774. [Google Scholar] [CrossRef]
  20. Moghimi, R.; Ghaderi, L.; Rafati, H.; Aliahmadi, A.; McClements, D.J. Superior antibacterial activity of nanoemulsion of Thymus daenensis essential oil against E. coli. Food Chem. 2016, 194, 410–415. [Google Scholar] [CrossRef]
  21. Hui, A.P.; Liu, J.L.; Ma, J.Z. Synthesis and morphology-dependent antimicrobial activity of cerium doped flower-shaped ZnO crystallites under visible light irradiation. Coll. Surf. A 2016, 506, 519–525. [Google Scholar] [CrossRef]
  22. Liu, J.L.; Shao, J.Z.; Wang, Y.h.; Li, J.Q.; Liu, H.; Wang, A.Q.; Hui, A.P.; Chen, S.W. Antimicrobial activity of zinc oxide-graphene quantum dot nanocomposites: Enhanced adsorption on bacterial cells by cationic capping polymers. ACS Sustain. Chem. Eng. 2019, 7, 16264–16273. [Google Scholar] [CrossRef]
  23. Raghunath, A.; Perumal, E. Metal oxide nanoparticles as antimicrobial agents: A promise for the future. Int. J. Antimicrob. Agents 2017, 49, 137–152. [Google Scholar] [CrossRef] [PubMed]
  24. Yan, Y.; Kuang, W.; Shi, L.; Ye, X.; Yang, Y.; Xie, X.; Tan, S. Carbon quantum dot-decorated TiO2 for fast and sustainable antibacterial properties under visible-light. J. Alloys Compd. 2019, 777, 234–243. [Google Scholar] [CrossRef]
  25. Zhu, X.W.; Wu, D.; Wang, W.; Tan, F.T.; Wong, P.K.; Wang, X.Y.; Qiu, X.L.; Qiao, X.L. Highly effective antibacterial activity and synergistic effect of Ag-MgO nanocomposite against Escherichia coli. J. Alloys Compd. 2016, 684, 282–290. [Google Scholar] [CrossRef]
  26. Bilia, A.R.; Guccione, C.; Isacchi, B.; Righeschi, C.; Firenzuoli, F.; Bergonzi, M.C. Essential oils loaded in nanosystems: A developing strategy a successful therapeutic approach. Evid-Based Complement Altern. Med. 2014, 2014, 651593. [Google Scholar] [CrossRef] [Green Version]
  27. Brayner, R.; Ferrari-Iliou, R.; Brivois, N.; Djediat, S.; Benedetti, M.F.; Fievet, F. Toxicological impact studies based on Escherichia coli bacteria in ultrafine ZnO nanoparticles colloidal medium. Nano Lett. 2006, 6, 866–870. [Google Scholar] [CrossRef]
  28. Jiang, Y.; Zhang, L.; Wen, D.; Ding, Y. Role of physical and chemical interactions in the antibacterial behavior of ZnO nanoparticles against E. coli. Mater. Sci. Eng. C 2016, 69, 1361–1366. [Google Scholar] [CrossRef]
  29. Applerot, G.; Lipovsky, A.; Dror, R.; Perkas, N.; Nitzan, Y.; Lubart, R.; Gedanken, A. Enhanced antibacterial activity of nanocrystalline ZnO due to increased ROS-mediated cell injury. Adv. Funct. Mater. 2009, 19, 842–852. [Google Scholar] [CrossRef]
  30. Alswat, A.A.; Ahmad, M.B.; Saleh, T.A.; Hussein, M.Z.B.; Ibrahim, N.A. Effect of zinc oxide amounts on the properties and antibacterial activities of zeolite/zinc oxide nanocomposite. Mater. Sci. Eng. C 2016, 68, 505–511. [Google Scholar] [CrossRef]
  31. Hui, A.P.; Dong, S.Q.; Kang, Y.R.; Zhou, Y.M.; Wang, A.Q. Hydrothermal fabrication of spindle-shaped ZnO/palygorskite nanocomposites using nonionic surfactant for enhancement of antibacterial activity. Nanomaterials 2019, 9, 1453. [Google Scholar] [CrossRef] [Green Version]
  32. Huo, C.L.; Yang, H.M. Synthesis and characterization of ZnO/palygorskite. Appl. Clay Sci. 2010, 50, 362–366. [Google Scholar] [CrossRef]
  33. Leone, F.; Cataldo, R.; Mohamed, S.S.Y.; Manna, L.; Banchero, M.; Ronchetti, S.; Mandras, N.; Tullio, V.; Cavalli, R.; Onida, B. Nanostructured ZnO as multifunctional carrier for a green antibacterial drug delivery system-a feasibility study. Nanomaterials 2019, 9, 407. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  34. Dong, W.K.; Lu, Y.S.; Wang, W.B.; Zhang, M.M.; Jing, Y.M.; Wang, A.Q. A sustainable approach to fabricate new 1D and 2D nanomaterials from natural abundant palygorskite clay for antibacterial and adsorption. Chem. Eng. J. 2020, 382, 122984. [Google Scholar] [CrossRef]
  35. Tang, J.; Mu, B.; Zong, L.; Wang, A.Q. One-step synthesis of magnetic attapulgite/carbon supported NiFe-LDHs by hydrothermal process of spent bleaching earth for pollutants removal. J. Clean. Prod. 2018, 172, 673–685. [Google Scholar] [CrossRef]
  36. Zhang, R.Q.; Zhou, Y.M.; Jiang, X.Y.; Chen, Y.P.; Wen, C.; Liu, W.B.; Jiang, Y. Evaluation Of zinc-bearing palygorskite effects on growth performance, nutrient retention, meat quality, and zinc accumulation in blunt snout bream Megalobrama Amblycephala. Clays Clay Miner. 2018, 66, 274–285. [Google Scholar] [CrossRef]
  37. Rosendo, F.R.; Pinto, L.I.; de Lima, I.S.; Trigueiro, P.; Honório, L.M.D.C.; Fonseca, M.G.; Osajima, J.A. Antimicrobial efficacy of building material based on ZnO/palygorskite against Gram-negative and Gram-positive bacteria. Appl. Clay Sci. 2020, 188, 105499. [Google Scholar] [CrossRef]
  38. Hui, A.P.; Yan, R.; Wang, W.B.; Wang, Q.; Zhou, Y.M.; Wang, A.Q. Incorporation of quaternary ammonium chitooligosaccharides on ZnO/palygorskite nanocomposites for enhancing antibacterial activities. Carbohydr. Polym. 2020, 247, 116685. [Google Scholar] [CrossRef]
  39. Zhang, Y.; Wang, W.B.; Mu, B.; Wang, Q.; Wang, A.Q. Effect of grinding time on fabricating a stable methylene blue/palygorskite hybrid nanocomposite. Powder Technol. 2015, 280, 173–179. [Google Scholar] [CrossRef]
  40. Wang, X.W.; Mu, B.; Hui, A.P.; Wang, Q.; Wang, A.Q. Low-cost bismuth yellow hybrid pigments derived from attapulgite. Dye. Pigment. 2018, 149, 521–530. [Google Scholar] [CrossRef]
  41. Mu, B.; Kang, Y.R.; Wang, A.Q. Preparation of a polyelectrolyte-coated magnetic attapulgite composite for the adsorption of precious metals. J. Mater. Chem. A 2013, 1, 4804–4811. [Google Scholar] [CrossRef]
  42. Mcnab, A.I.; Mccue, A.J.; Dionisi, D.; Anderson, J.A. Quantification and qualification by in-situ FTIR of species formed on supported-cobalt catalysts during the Fischer-Tropsch reaction. J. Catal. 2017, 353, 286–294. [Google Scholar] [CrossRef]
  43. Zhong, H.Q.; Mu, B.; Yan, P.J.; Jing, Y.M.; Hui, A.P.; Wang, A.Q. A comparative study on surface/interface mechanism and antibacterial properties of different hybrid materials prepared with essential oils active ingredients and palygorskite. Coll. Surf. A 2021, 618, 126455. [Google Scholar] [CrossRef]
  44. Xu, J.X.; Wang, W.B.; Wang, A.Q. Stable formamide/palygorskite nanostructure hybrid material fortified by high-pressure homogenization. Powder Technol. 2017, 318, 1–7. [Google Scholar] [CrossRef]
  45. Zhong, H.Q.; Mu, B.; Zhang, M.M.; Hui, A.P.; Kang, Y.R.; Wang, A.Q. Preparation of effective carvacrol/attapulgite hybrid antibacterial materials by mechanical milling. J. Porous Mater. 2020, 27, 843–853. [Google Scholar] [CrossRef]
  46. Mao, C.Y.; Xiang, Y.M.; Liu, X.M.; Cui, Z.D.; Yang, X.J.; Wai, K.; Yeung, K.; Pan, H.B.; Wang, X.B.; Chu, P.K.; et al. Photo-inspired antibacterial activity and wound healing acceleration by hydrogel embedded with Ag/Ag@AgCl/ZnO nanostructures. ACS Nano 2017, 11, 9010–9021. [Google Scholar] [CrossRef]
  47. Kiskó, G.; Roller, S. Carvacrol and p-cymene inactivate Escherichia coli O157: H7 in apple juice. BMC Microbiol. 2005, 5, 36. [Google Scholar] [CrossRef] [Green Version]
  48. Peretto, G.; Du, W.X.; Avenabustillos, R.J.; Berrios, J.D.J.; Sambo, P.; Mchugh, T.H. Optimization of antimicrobial and physical properties of alginate coatings containing carvacrol and methyl cinnamate for strawberry application. J. Agric. Food Chem. 2014, 62, 984–990. [Google Scholar] [CrossRef] [PubMed]
  49. Liu, J.L.; Rojas-Andrade, M.D.; Chata, G.; Peng, Y.; Roseman, G.; Lu, J.E.; Millhauser, G.L.; Saltikov, C.; Chen, S.W. Photo-enhanced antibacterial activity of ZnO/graphene quantum dot nanocomposites. Nanoscale 2018, 10, 158–166. [Google Scholar] [CrossRef] [PubMed]
  50. Liu, J.L.; Wang, Y.H.; Shen, J.H.; Liu, H.; Li, J.Q.; Wang, A.Q.; Hui, A.P.; AkifMunira, H. Superoxide anion: Critical source of high performance antibacterial activity in Co-Doped ZnO QDs. Ceram. Int. 2020, 46, 15822–15830. [Google Scholar] [CrossRef]
  51. Sivropoulou, A.; Papanikolaou, E.; Nikolaou, C.; Kokkini, S.; Lanaras, T.; Arsenakis, M. Antimicrobial and cytotoxic activities of origanum essential oils. J. Agric. Food Chem. 1996, 44, 1202–1205. [Google Scholar] [CrossRef]
Figure 1. (a) Chemical structures of PEOs, (b) schematic illustration for the preparation of CAR/ZnO/PAL nanocomposites.
Figure 1. (a) Chemical structures of PEOs, (b) schematic illustration for the preparation of CAR/ZnO/PAL nanocomposites.
Nanomaterials 11 03230 g001
Figure 2. FTIR spectra of PEOs/ZnO/PAL (i) citral, (ii) thymol, (iii) CAR, (iv) oregano oil, (v) cinnamaldehyde, (a) and CAR/ZnO/PAL with different concentrations of CAR (b).
Figure 2. FTIR spectra of PEOs/ZnO/PAL (i) citral, (ii) thymol, (iii) CAR, (iv) oregano oil, (v) cinnamaldehyde, (a) and CAR/ZnO/PAL with different concentrations of CAR (b).
Nanomaterials 11 03230 g002
Figure 3. XRD pattern of PAL, ZnO/PAL, and CAR/ZnO/PAL.
Figure 3. XRD pattern of PAL, ZnO/PAL, and CAR/ZnO/PAL.
Nanomaterials 11 03230 g003
Figure 4. TG curves of PAL, ZnO/PAL, and CAR/ZnO/PAL.
Figure 4. TG curves of PAL, ZnO/PAL, and CAR/ZnO/PAL.
Nanomaterials 11 03230 g004
Figure 5. SEM images of (a) PAL, (b) ZnO/PAL, and (c) CAR/ZnO/PAL.
Figure 5. SEM images of (a) PAL, (b) ZnO/PAL, and (c) CAR/ZnO/PAL.
Nanomaterials 11 03230 g005
Figure 6. TEM images of (a) PAL, (b) ZnO/PAL, and (c) CAR/ZnO/PAL.
Figure 6. TEM images of (a) PAL, (b) ZnO/PAL, and (c) CAR/ZnO/PAL.
Nanomaterials 11 03230 g006
Figure 7. (a) Blank control, (b) positive control of E. coli, E. coli treated with ZnO/PAL nanoparticles at various concentrations of (c) 2.5 mg/mL, (d) 1.5 mg/mL, (e) 1 mg/mL, and (f) 0.5 mg/mL, (g) blank control, (h) positive control of S. aureus, S. aureus treated with ZnO/PAL nanoparticles at various concentrations of (i) 10 mg/mL, (j) 5 mg/mL, (k) 2.5 mg/mL, and (l) 1.5 mg/mL.
Figure 7. (a) Blank control, (b) positive control of E. coli, E. coli treated with ZnO/PAL nanoparticles at various concentrations of (c) 2.5 mg/mL, (d) 1.5 mg/mL, (e) 1 mg/mL, and (f) 0.5 mg/mL, (g) blank control, (h) positive control of S. aureus, S. aureus treated with ZnO/PAL nanoparticles at various concentrations of (i) 10 mg/mL, (j) 5 mg/mL, (k) 2.5 mg/mL, and (l) 1.5 mg/mL.
Nanomaterials 11 03230 g007
Figure 8. MIC value of PEOs/ZnO/PAL nanocomposites against E. coli.
Figure 8. MIC value of PEOs/ZnO/PAL nanocomposites against E. coli.
Nanomaterials 11 03230 g008
Figure 9. MIC value of PEOs/ZnO/PAL nanocomposites against S. aureus.
Figure 9. MIC value of PEOs/ZnO/PAL nanocomposites against S. aureus.
Nanomaterials 11 03230 g009
Figure 10. MIC evaluation of ZnO/PAL at different concentrations of CAR against E. coli.
Figure 10. MIC evaluation of ZnO/PAL at different concentrations of CAR against E. coli.
Nanomaterials 11 03230 g010
Table 1. SBET, Smicro, Sext, and Vtotal of PAL, ZnO/PAL, and ZnO/PAL at different concentrations of CAR.
Table 1. SBET, Smicro, Sext, and Vtotal of PAL, ZnO/PAL, and ZnO/PAL at different concentrations of CAR.
Concentrations
of CAR (%)
SBET (m2/g)Smicro (m2/g)Sext (m2/g)Vtotal (cm3/g)
125290.149
2.519210.133
515170.091
1013160.082
209110.034
PAL12581170.332
ZnO/PAL27330.158
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Hui, A.; Yang, F.; Yan, R.; Kang, Y.; Wang, A. Palygorskite-Based Organic–Inorganic Hybrid Nanocomposite for Enhanced Antibacterial Activities. Nanomaterials 2021, 11, 3230. https://doi.org/10.3390/nano11123230

AMA Style

Hui A, Yang F, Yan R, Kang Y, Wang A. Palygorskite-Based Organic–Inorganic Hybrid Nanocomposite for Enhanced Antibacterial Activities. Nanomaterials. 2021; 11(12):3230. https://doi.org/10.3390/nano11123230

Chicago/Turabian Style

Hui, Aiping, Fangfang Yang, Rui Yan, Yuru Kang, and Aiqin Wang. 2021. "Palygorskite-Based Organic–Inorganic Hybrid Nanocomposite for Enhanced Antibacterial Activities" Nanomaterials 11, no. 12: 3230. https://doi.org/10.3390/nano11123230

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop