Recent Advances in Zinc Oxide Nanostructures with Antimicrobial Activities

Yuchao Li, Chengzhu Liao, Sie Chin Tjong, Yuchao Li, Chengzhu Liao, Sie Chin Tjong

Abstract

This article reviews the recent developments in the synthesis, antibacterial activity, and visible-light photocatalytic bacterial inactivation of nano-zinc oxide. Polycrystalline wurtzite ZnO nanostructures with a hexagonal lattice having different shapes can be synthesized by means of vapor-, liquid-, and solid-phase processing techniques. Among these, ZnO hierarchical nanostructures prepared from the liquid phase route are commonly used for antimicrobial activity. In particular, plant extract-mediated biosynthesis is a single step process for preparing nano-ZnO without using surfactants and toxic chemicals. The phytochemical molecules of natural plant extracts are attractive agents for reducing and stabilizing zinc ions of zinc salt precursors to form green ZnO nanostructures. The peel extracts of certain citrus fruits like grapefruits, lemons and oranges, acting as excellent chelating agents for zinc ions. Furthermore, phytochemicals of the plant extracts capped on ZnO nanomaterials are very effective for killing various bacterial strains, leading to low minimum inhibitory concentration (MIC) values. Bioactive phytocompounds from green ZnO also inhibit hemolysis of Staphylococcus aureus infected red blood cells and inflammatory activity of mammalian immune system. In general, three mechanisms have been adopted to explain bactericidal activity of ZnO nanomaterials, including direct contact killing, reactive oxygen species (ROS) production, and released zinc ion inactivation. These toxic effects lead to the destruction of bacterial membrane, denaturation of enzyme, inhibition of cellular respiration and deoxyribonucleic acid replication, causing leakage of the cytoplasmic content and eventual cell death. Meanwhile, antimicrobial activity of doped and modified ZnO nanomaterials under visible light can be attributed to photogeneration of ROS on their surfaces. Thus particular attention is paid to the design and synthesis of visible light-activated ZnO photocatalysts with antibacterial properties.

Keywords: antimicrobial activity; contact killing; free radicals; hemolysis; heterostructure; photocatalytic activity; phytocompounds; semiconducting oxide; synthesis; zinc ion.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

**Figure 1**
Antibacterial mechanisms of different nanoparticles (NPs) in fighting MDR bacteria. AuNPs: gold NPs, CuONPs: copper oxide NPs; AgNPs: silver NPs; Fe3O4NPs: iron oxide NPs, and ZnONPs: zinc oxide NPs. Reproduced from [16] under the terms of the Creative Commons Attribution License (CC BY).

**Figure 2**
Schematic representation showing versatile applications of ZnO nanoparticles in chemical, electronic, textile, pharmaceutical and cosmetic industries. Reproduced from [35] the terms of the Creative Commons Attribution License (CC BY).

**Figure 3**
(a) UV-visible spectra of pure ZnO, Mn-doped ZnO and Co-doped ZnO nanowires, and (b) Tauc plots of (αhv)2 versus hv for ZnO-based nanowires showing the reduction of bandgap energy through transition metal doping. (c) The generation of superoxide anion and hydroxyl radicals on ZnO nanowires under visible light due to the creation of midgap states in the bandgap by doping with Mn or Co. Reproduced from [108] under the terms of the Creative Commons Attribution License (CC BY).

**Figure 4**
Formation of superoxide anion and hydroxyl radicals on Mn-doped ZnO nanoparticles for degrading Orange II dye under solar light irradiation at different intervals of time. Reproduced from [109] with permission of Elsevier.

**Figure 5**
(A) Visible light induces localized surface plasmon resonance (LSPR) in AgNPs or AuNPs such that hot electrons are injected into the CB of ZnO for generating superoxide anion and hydroxyl radicals. (B) Under UV irradiation, photoexcited electrons are transferred from the CB of ZnO to AgNPs or AuNPs. VB = valence band, CB: conduction band, FMO: Fermi level of metal oxide, FM: Fermi level of metal, FEq: Fermi level of equilibrium, and M: Au and Ag. Reproduced from [127] with permission of the Royal Society of Chemistry.

**Figure 6**
The plots of Kubelka–Munk function vs photon energy for evaluating bandgap energy of (a) ZnO and Cu0.5Z, Cu1.5Z, Cu2.5Z and Cu5.0Z, and (b) NZ, Cu0.5NZ, Cu1.5NZ, Cu2.5NZ and Cu5.0NZ. (c) Optical absorbance of ZnO, Cu0.5Z, Cu1.5Z, Cu2.5Z, Cu5.0Z, NZ, Cu0.5NZ, Cu1.5NZ, Cu2.5NZ and Cu5.0NZ. Reproduced from [135] with permission of the Royal Society of Chemistry.

**Figure 7**
(a) UV-vis diffuse reflectance spectra, and (b) the plots of Kubelka–Munk function versus light energy for neat ZnO nanorod and RGO/ZnO nanocomposites. Reproduced from [172] with permission of the Royal Society of Chemistry.

**Figure 8**
Electron transfer from graphene sheet to the conduction band of ZnO under visible light for generating ROS. Reproduced from [173] with permission of Elsevier.

**Figure 9**
The transfer of photogenerated electron from the conduction band of ZnO to a single nanotube under UV irradiation. Reproduced from [175] with permission of Elsevier.

**Figure 10**
(a) Energy band alignments of type-I, type-II, and type-III heterojunctions. Reproduced from [186] with permission of Frontiers under the Creative Commons Attribution License. (b) The charge carrier transfer in CuO/ZnO photocatalyst under sunlight irradiation. Reproduced from [185] the terms of the Creative Commons Attribution License.

**Figure 11**
(a) Scanning electron microscope (SEM) image showing ZnO nanorods and nanobelts grown on the top (0001) and side surfaces of the ZnO microrods, respectively for 15 min. Inset: Magnified SEM image. (b) SEM image of ZnO nanorods and nanobelts after growing for 30 min at 1100 °C. Black arrows indicate nanobelts. Reproduced from [205] with permission of the American Chemical Society.

**Figure 12**
(a) SEM image of ZnO nanobelts. (b) Transmission electron micrograph of a helical nanobelt. Inset: structural model of ZnO nanobelt. Reproduced from [208] with permission of the American Chemical Society.

**Figure 13**
(A) SEM and (B) transmission electron microscope (TEM) images of ZnO nanoparticles (NPs) prepared by co-precipitation process using zinc acetate dihydrate and NaOH. Inset in (B) shows a high-magnified TEM image of hexagonal shaped ZnO NPs. Reproduced from [212] under a Creative Commons License.

**Figure 14**
(a) Proposed reaction mechanism between functional groups of grapefruit peel extract and zinc ions from zinc sulfate in forming zinc-ligand complex and ZnO NPs after drying in an oven at 150 °C. Reproduced from [217] under the Creative Commons Attribution License. (b) A schematic showing biosynthesis of ZnO nanoflowers (NFs) using Zn(NO3)2.6H2O and *sea buckthorn* (SBT) fruit extract. Reproduced from [220] under the terms of the Creative Commons Attribution License. (c) X-ray diffraction patterns showing the wurtzite structure of as-synthesized ZnO nanoparticles calcined at different temperatures. ZnO NPs are biosynthesized from Zn(NO3)2.6H2O and orange peel extract. (d) Fourier transform infrared spectra of orange peel extract and the as-synthesized ZnO NPs heat treated at different temperatures. Reproduced from [219] under the terms of the Creative Commons Attribution-NonCommercial 3.0 Unported License.

**Figure 15**
SEM images of top and cross-sectional views of ZnO nanorods formed on ZnO-seeded SiO2/Si substrate by immersing in zinc acetylacetonate hydrate and HMTA solution for (a) 0.5 h and (b) 2 h. Insets in left panels of (a,b): High-magnification plan-view SEM images. Right panels: cross-sectional SEM micrographs. Reproduced from [223] under the terms of the Creative Commons Attribution License (CC BY).

**Figure 16**
SEM images showing (a) top view and (b) 45° tilt view of ZnO nanorod arrays. Reproduced from [230] under the terms of the Creative Commons Attribution 4.0 International License.

**Figure 17**
The effect of growth time on morphological evolution of flower-like ZnO nanostructures in preheated aqueous Zn(NO3)2·6H2O and HMTA solutions: (a) 2 h, (b) 4 h, (c) 6 h, and (d) 24 h. Reproduced from [231] under the Creative Commons Attribution License.

**Figure 18**
Schematic displaying the evolution of ZnO nanorods and ZnO nanoflowers from [Zn(OH)4]2− growth units. Reproduced from [239] under the Creative Commons Attribution License.

**Figure 19**
Schematic representation of the synthesis of AgNPs/ZnO nanocomposite using arginine as a linker to immobilize AgNPs on ZnO nanorods. Reproduced from [235] under a Creative Commons Attribution 3.0 Unported License.

**Figure 20**
TEM images of (a) a single ZnO nanorod with uniformly dispersed AgNPs. (b) Side view of AgNPs/ZnO nanorod and immobilized AgNP at the tip of ZnO (inset). High-resolution TEM (HRTEM) images showing (c) a clear interface between AgNP and ZnO, (d) lattice fringes with characteristic d-spacing of ZnO, and (e) lattice fringes of AgNP. The corresponding electron diffraction patterns of ZnO (above panel) and AgNP (below panel) are also presented. Reproduced from [235] under a Creative Commons Attribution 3.0 Unported License.

**Figure 21**
Formation of GO-ZnO nanocomposites using solvothermal process. (a) Transmission electron micrograph showing dispersion of ZnO nanoparticles on graphene sheet. (b) HRTEM image showing the lattice fringes of ZnO nanoparticle. Reproduced from [242] with permission of the American Chemical Society.

**Figure 22**
(a) Three possible mechanisms responsible for bactericidal activity of ZnO NPs: (1) The generation of reactive oxygen species (ROS), (2) release of Zn2+ ions, and (3) direct attachment on bacterial cell membrane. Reproduced from [261] under the terms of the Creative Commons Attribution 4.0 International License. Schematics showing the cell wall structures of (b) Gram-positive and (c) Gram-negative bacteria. Reproduced from [266] under the terms of the Creative Commons Attribution License.

**Figure 23**
TEM images showing bare *D. radiodurans* cells (left panel), and internalization of ZnO NPs into bacterial cells (right panel). Reproduced from [276] under a Creative Commons Attribution 4.0 License.

**Figure 24**
Reduction in viability of *D. radiodurans* upon exposure to ZnO NPs for 3 h as determined by: (a) Colony count method, (b) 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide (MTT) assay, (c) propidium iodide (PI) uptake assay, and (d) ROS assay. The error bars are the standard deviation (n = 3); * denotes p < 0.05. Reproduced from [276] under a Creative Commons Attribution 4.0 International License.

**Figure 25**
(a) SEM images of *E. coli* with concentrations of 106, 107 and 108 CFU/mL upon exposure to ZnO nanoparticles of different doses (0.01, 0.1 and 1.0 mg/mL). Reproduced from [278] under a Creative Commons Attribution 4.0 International License. (b) SEM images of untreated *E. coli* cells (left panel) and ZnO NPs treated *E. coli* cells (right panel). Direct contact of ZnO NPs on bacterial membranes due to electrostatic interactions leads to membrane blebling, membrane damage, and membrane clumping as indicated by white arrows. Reproduced from [275] under a Creative Commons Attribution 4.0 International License. (c) Fluorescent 2,7-dichlorofluorescein (DCF) data showing the ROS level in *Pseudomonas aeruginosa* treated with ZnO NPs (5, 10, 25, 50 and 100 mg/mL) for 24 h. Reproduced from [29] under a Creative Commons Attribution License.

**Figure 26**
Growth inhibition zones for various bacterial strains exposed to green ZnO NPs of different concentrations. Oxytetracycline was used as a positive control. Reproduced from [31] under a Creative Commons Attribution License.

**Figure 27**
Effect of AgNPs/ZnO concentrations on the viability of (a) *E. coli*, (b) *S. aureus*, and (c) bacterial colony features cultured on agar plates. (d) Inhibition zone of AgNPs/ZnO nanocomposite (NC), ZnO NPs and Gentamicin. Gentamicin is an antibiotic specifically used for treating bacterial infections. OD in (a) denotes optical density. Reproduced from [282] under a Creative Commons Attribution 4.0 International License.

**Figure 28**
(a) Inactivation efficiency of *E. coli* treated with ZnO nanorod arrays of various lengths (0.5–4 μm) for 30 min under different conditions (dark, visible light, and UV irradiation). (b) Inactivation efficiency of *E. coli* treated with ZnO nanorod arrays of various lengths with different Al2O3 layer thicknesses for 30 min in the dark. The values are the average of triplicate measurements, and error bars denote the standard deviation. (c) Bactericidal mechanisms of ZnO nanorod arrays in the dark: membrane rupture due to the nanorod piercing (inset: SEM images) > ROS generation > released Zn2+ ions. Reproduced from [288] with permission of Elsevier.

**Figure 29**
Antibacterial efficacy of pristine ZnO and Cu-doped ZnO nanorods using shake flask method. Reproduced from [103] with permission of Springer.

**Figure 30**
(a) The growth of bacterial populations as expressed by the logarithm of the number of cells (N) versus time. The unit of N is given as the colony forming unit (CFU) per mL. Bactericidal activity of AgNPs/ZnO nanorods against *E. coli* tested at an initial bacterial concentration of 103 CFU/mL (triangle) and 105 CFU/mL (square) in both deionized water (continuous line) and phosphate buffer medium (dashed line), respectively. (b) Bactericidal activity of AgNPs/ZnO nanorods, pure ZnO nanorods, colloidal AgNPs and AgNPs/silica against E. coli tested at an initial bacterial concentration of 103 CFU/mL. Four independent tests were performed against E. coli, and the average values reported. Reproduced from [235] under a Creative Commons Attribution 3.0 Unported License.

**Figure 31**
(a) Disinfection performance of AgNPs/ZnO nanorods after reusing for 11 runs against *E. coli* (103 CFU/mL). (b) The corresponding released silver ions vs time profiles after every usage. (c) TEM image showing internalization of AgNP by *E. coli*. Reproduced from [235] under a Creative Commons Attribution 3.0 Unported License.

**Figure 32**
(a) ROS and (b) lactate dehydrogenase (LDH) levels of different Gram-negative bacteria strains treated with pure GO and GO/ZnO nanohybrid. Reproduced from [246] with permission of Springer Nature.

**Figure 33**
Growth curves of *E. coli* treated with (a) GO-1/ZnO and (b) GO-2/ZnO hybrids of different doses; (c) Zinc released from GO/ZnO composites; (d) Wrapping of graphene sheet around *E. coli* and released Zn2+ ions led to bacterial cell membrane damage. The experiments were performed in triplicates, and the results were given as mean ± standard deviation. Reproduced from [242] with permission of the American Chemical Society.

**Figure 34**
(a) SEM image showing morphology of Cu-doped ZnO nanorods; (b) Photocatalytic efficiency of ZnO NPs and Cu/ZnO nanorods against *E. coli* under simulated solar light irradiation; (c) Photocatalytic mechanism of Cu/ZnO nanorods under solar light. Reproduced from [298] with permission from Elsevier.

**Figure 35**
(a) Change in fluorescence intensity of green/red ratio of live/dead assay, (b) ROS and (c) MDA levels of *E.coli* treated with different Cu5/ZnO concentrations. The data were expressed as the mean ± SD (standard deviation) for three independent experiments (n = 3). p < 0.05 (*), 0.001 (**) and 0.0001 (***) were measured significant as compared to control. Reproduced from [102] with permission of the American Chemical Society.

**Figure 36**
Photoinactivation of *E. coli* treated with Cu5/ZnO (200 µg/mL) under solar light (SL). The plots of (a) OD600 and (b) CFU/mL as a function of time. The experiments were performed in triplicates and data were expressed as the mean ± SD. Reproduced from [102] with permission of the American Chemical Society.

**Figure 37**
(a) TEM image and (b) schematic illustration of the production of hydroxyl, superoxide anion and singlet oxygen radicals on 4% AuNPs/ZnO exposed to simulated sunlight. Fine grey circles in (a) are AuNPs; scale bar is 20 nm. (c) A bar graph showing *staphylococcus aureus* survival upon exposure to ZnO NPs and 4% AuNPs/AgNPs at doses of 0.05 and 0.1 mg/mL without (black column) and with simulated sunlight illumination for 10 min. Control 1 is bacteria exposed to neither NPs nor light. Control 2 denotes bacteria exposed to simulated sunlight for 10 min in the absence of NPs. All tests are conducted in triplicates and repeated at least twice to obtain reproducibility. Reproduced from [305] with permission of the American Chemical Society.

**Figure 38**
(a) Effect of Fe/ZnO NPs concentrations on solar-photocatalytic disinfection (PCD) kinetics of multidrug-resistant (MDR) *E. coli*. Control-1: bacteria exposed to Fe/ZnO NPs in the dark; Control-2: bacteria without Fe/ZnO NPs under solar irradiation. (b) Effect of different catalysts on the solar-PCD kinetics of *MDR E. coli* at a catalyst concentration of 500 mg/L. Initial MDR *E. coli* concentration = 1.2 × 107 CFU/mL, temperature = 35 ± 2 °C, pH = 6.5. Error bars indicate standard deviation of replicates (n = 3). Reproduced from [306] under a Creative Commons Attribution 4.0 International License.

**Figure 39**
Plots of (a) malondialdehyde (MDA) content vs time and (b) leakage of K+ ion vs time for MDR *E. coli* treated with Fe/ZnO NPs. Initial MDR *E. coli* concentration = 1.2 × 107 CFU/mL, Temperature = 35 ± 2 °C, pH = 6.5, [Fe/ZnO NPs] = 500 mg/L. Error bars indicate standard deviation of replicates (n = 3). Reproduced from [306] under a Creative Commons Attribution 4.0 International License.

**Figure 40**
Schematic view of visible-light photocatalytic bactericidal activity of Fe/ZnO NPs against *MDR E. coli*. Reproduced from [306] under a Creative Commons Attribution 4.0 International License.

**Figure 41**
Log reduction of *E. coli* treated with undoped ZnO SG, ZnO:TFA 1:1 and ZnO:TFA 1:2 under (A) the dark and (B) visible light conditions. (C) Bactericidal activity of those samples against *S. aureus* under visible light. All tests were conducted in triplicates. Reproduced from [310] with permission of Elsevier.

**Figure 42**
(a) SEM image showing ZnO nanorods decorated with CuO. (b) Survival rate vs visible light irradiation time curves of *E. coli* treated with CuO/ZnO membrane and ZnO membrane. Reproduced from [313] under the Creative Commons Attribution License.

**Figure 43**
(a) Visible-light photocatalytic inactivation efficiency of *E. coli* (1 × 107 CFU/ mL) treated with GO/ZnO composite, GO and ZnO; (b) H2O2 generation from GO/ZnO during the photocatalytic inactivation process under visible light. All the experiments and controls were conducted in triplicates. Reproduced from [173] with permisiion of Elsevier.

**Figure 44**
Hemolysis is caused by the binding or encapsulation of nanoparticles (NPs) in red blood cells (RBCs) leading to the generation of ROS, oxidative stress, and disturbed homeostasis as a result of osmotic shock and surface integrity problems. Reproduced from [320] with permission of Springer Nature.

**Figure 45**
(A) Hemolytic effect of ZnO NPs (<50 nm) of two different doses with and without albumin (4.5 μg dl−1) on erythrocytes for 24 h. # denotes significant difference at p ≤ 0.05 of the samples compared to control. (B) The effect of ZnO NPs (<50 nm; 200 μg/mL) and ZnO NPs with ferulic acid (FA) exposure on hemolysis in the presence of fetal bovine serum of different concentrations (3.125%, 6.25%, 12.5% and 25%) for 24 h. # denotes significant difference at p ≤ 0.05 of the samples compared to control. Reproduced from [323] under Creative Commons Attribution License.

**Figure 46**
Hemocompatibility assay results of human erythrocytes treated with (a) ZnO nanostrucuture (ZnONS) and (b) bovine α-lactalbumin (BLA) functionalized ZnONS of different concentrations. Trixton X 1% was employed as a control. All the data were expressed as mean ± standard deviation, n = 3. Reproduced from [326] with permission of Elsevier.

**Figure 47**
(a) The hemolytic activity of bulk ZnO, biosynthesized ZnO NPs and AgNPs/ZnO nanocomposite. Reproduced from [282] under the terms of Creative Commons License. (b) Percentage hemolysis of ZnO nanoparticles prepared by biosynthesis (green column) and co-precipitation (orange column). 0.1% Triton X-100 was employed as a positive control (PC). Reproduced from [328] with permission of Springer.

**Figure 48**
(a) SEM images showing lysis of RBCs by *S. aureus* and their inhibition by green ZnO NPs. Images from left to right: untreated RBCs, ZnO NPs treated RBCs, *S. aureus* infected RBCs, and RBCs co-cultured with *S. aureus* and ZnO NPs. (b) Inhibition of hemolysis in *S. aureus* infected RBCs by ZnO NPs. All data are expressed as the mean ± standard deviation. *** for p ≤ 0.001; ** for p ≤ 0.01. Reproduced from [332] under a Creative Commons License.

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Recent Advances in Zinc Oxide Nanostructures with Antimicrobial Activities

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