Preparation and Antibiofilm Properties of Zinc Oxide/Porous Anodic Alumina Composite Films
The PAA (porous anodic alumina) films were prepared by two-step anodic oxidation after different times, and then the ZnO/PAA composite films were prepared by sol-gel method on their surface. Meanwhile, the ZnO/PAA composite films were characterized by X-ray diffraction (XRD), thermogravimetric/differential thermal analyzer (TG/DTA), Fourier transform infrared spectrometer (FT-IR), scanning electron microscopy (SEM), transmission electron microscopy (TEM), selected area electron diffraction (SAED), and water contact angle (CA). The antibiofilm properties of ZnO/PAA composite films on Shewanella putrefaciens were measured simultaneously. The results show that the micromorphologies of PAA and ZnO/PAA composite films are affected by second anodization time. ZnO is a hexagonal wurtzite structure, and ZnO particles with a diameter of 10–30 nm attach to the inner or outer surfaces of PAA. After being modified by Si69, the ZnO films translate from hydrophilia to hydrophobicity. The ZnO/PAA film with the optimal antibiofilm properties is prepared on the PAA surface by two-step anodization for 40 min. The adherence of Shewanella putrefaciens is restrained by its super-hydrophobicity, and the growth of biofilm bacteria is inhibited by its abundant ZnO particles.
KeywordsPAA/ZnO Composite film Antibiofilm Shewanella putrefaciens
Water contact angle
Fourier transform infrared spectrometer
Porous anodic alumina
Selected area electron diffraction
Scanning electron microscopy
Transmission electron microscopy
Thermogravimetric/differential thermal analyze
As we know, the bacteria can adhere to solid surfaces and form a slippery biofilm in appropriate environments . Usually, the bacteria biofilms stick firmly to the surfaces of materials, such as stainless steel , rubber , glass , and polystyrene . Biofilm would result in equipment corrosion  and food contamination , leading to huge economic losses. Many studies have indicated that biofilm adhesion is affected by the properties of material surface, such as roughness [8, 9, 10, 11], microstructure [12, 13], hydrophilia [14, 15, 16, 17], and antibiotic constituents [18, 19, 20]. Bohinc et al.  pointed out that the bacterial adherence would increase with the surface roughness of the glass. Singh et al.  demonstrated that high surface roughness can improve protein adsorption and accelerate the bacterial adhesion and biofilm formation. Bonsaglia et al. found that Listeria monocytogenes adhered to hydrophilic surfaces (e.g., stainless steel and glass) better than to hydrophobic ones (e.g., polystyrene) . Other studies also proved that hydrophobic surface was not good for biofilm adhesion [16, 17]. Some studies have shown that antibiotic constituents could inhibit biofilm formation [18, 19, 20]. Three hundred four Cu-bearing stainless steel surfaces have great antibacterial and antibiofilm properties, taking advantage of the antimicrobial activity of Cu element . In short, the surface properties are crucial to the antibiofilm properties of the materials.
Aluminum materials have been widely used, and porous anodic alumina (PAA) has drawn more attention in the fields of light electrical function, catalytic function, and sensing function in recent years [21, 22, 23, 24], and its antimicrobial activity was reported. Ferraz et al.  reported that PAA can induce the adhering activation of monocytes/macrophages due to their matrix phase and nanoporosity.
In addition, zinc oxide (ZnO) thin films have been studied as an excellent material for antibacterial and antifungus. The adherence of Pseudomonas aeruginosa to ZnO films with nanorod surface structures was weaker than that of glass and sputtered ZnO, and more P. aeruginosa are killed in the ZnO films . Meanwhile, one research pointed out that ZnO-coated surfaces dramatically restricted biofilm formation, and the generation of hydroxyl radicals played a key role in antibiofilm activity but not the existence of zinc ions . Furthermore, ZnO composite films can be used in many fields to restrict biofilm formation and will have good application prospects in aquatic product preservation . ZnO is hydrophilic, while hydrophobic films are good at restraining biofilm adhesion. Thus, it is necessary to improve the hydrophobic properties of ZnO film.
Aquatic products are very perishable due to their microbial spoilage . Under aerobic storage conditions, Pseudomonas spp. and Shewanella putrefaciens are known as dominant spoilage organisms . Shewanella putrefaciens has psychrotrophic nature and can reduce trimethylamine-N-oxide to trimethylamine . So, Shewanella putrefaciens will be used as the indicator bacteria in this paper.
The microstructures of ZnO films would be different due to their PAA base, and then the antibiofilm properties would be affected. In this work, ZnO films were prepared on PAA with different morphology and modified to improve the hydrophobicity. The antibiofilm properties of Shewanella putrefaciens of the ZnO/PAA composite films were studied. The results provide potential value for the applications in food packaging, food processing equipment, and the other antibacterial functional material fields.
Materials and Methods
All the reagents used in this study were analytically pure. The de-ionized and sterile water was used to prepare solutions with conductivity lower than 0.5 mS/cm. Shewanella putrefaciens ATCC8071 was purchased from American Type Culture Collection. Aluminum foils of 0.3 mm thickness with aluminum purity over 99.99% were purchased from Shengshida Metal materials Co., Ltd. (China).
Preparation of ZnO/PAA Composite Films
Preparation of Porous Anodic Alumina (PAA) Films
A high purity aluminum foil was cut into small dimension of 10 × 30 mm2 and was polished with polishing paste of 50 nm silica by a polisher (WV80, Positec Machinery Co., Ltd., China) and was ultrasonic degreased in acetone at 53 kHz, 280 W for 15 min (SK8210HP, Kudos Ultrasonic Instruments Co. Ltd., Shanghai). Then, the foils were washed two times both with ethanol and water, respectively. The pretreated aluminum foils were used as the anode, the equal-area graphite sheet as the cathode, and the 0.3 mol/L oxalic acid solution as the electrolyte. The first anodization was under the conditions of 30 °C and 40 V for 90 min. After that, the aluminum sheets were immersed in the mixed solution of 6.0 wt% H3PO4 and 1.8 wt% H2CrO4 at 60 °C for 4 h to remove the alumina layers. The second anodization was then performed under the same conditions but for 0, 40, 60, and 80 min, respectively. The porous anodic alumina (PAA) films with a different port model were obtained.
Preparation of ZnO/PAA Composite Films
Firstly, the equal volume of 0.02 mol/L zinc acetate ethanol solution and 0.04 mol/L NaOH ethanol solution were mixed under rapid stirring at 70 °C for 5 min, and then the PAA films (aluminum foils) were immersed in the mixed solution under a vacuum degree of − 0.085 MPa. Afterwards, the solution was heated to boiling. After it became thin blue sol, the aluminum foils were taken out and rinsed with de-ionized water. Then, the samples were vacuum dried at − 0.085 MPa, 80 °C for 6 h, and the ZnO/PAA composite films were prepared after calcined at 480 °C for 2 h in air atmosphere. The zinc oxide powders were prepared simultaneously. Finally, the ZnO/PAA composite films and the powders were modified by 1.0 wt% Si69 ethanol solution at 65 °C for 2 h and then vacuum dried at − 0.085 MPa, 40 °C for 12 h.
Characterization of ZnO/PAA Composite Films
X-ray diffraction of the zinc oxide powders was performed using X-ray powder diffractometer (Rigaku Ultima IV, Rigaku, Japan) at a step of 0.02°and 2θ range of 10°–80° with CuKa radiation of 40 kV, 50 mA. The thermal changes and weight loss of the samples were analyzed by thermogravimetric/differential thermal analyzer (TG/DTA, Perkin Elmer Diamond). Fourier transform infrared (FT-IR) spectra were recorded with a Scimitar 2000 Near FT-IR Spectrometer (Agilent, American) in the range of 4000–400 cm−1. The surface micrographs of PAA films and ZnO/PAA composite films were imaged by field emission scanning electron microscopy (FESEM, S-4800, Hitachi, Japan). The nanoparticle morphologies shaved from the ZnO/PAA composite films are measured by field emission transmission electron microscopy (FETEM, Jem-2100F, JEOL, Japan), and the selected area electron diffraction (SAED, Jem-2100F, EOL, Japan) of the samples were examined. The water contact angles (CA) of the composite films (before/after modified) were measured by the sessile drop method at several different positions on each sample surface using 3.0-μL droplets of de-ionized water (SL200B, USA).
The Antibiofilm Properties of ZnO/PAA Composite Films
Cultivation of Shewanella putrefaciens Biofilm
The bacterium suspension of secondary activating Shewanella putrefaciens (OD595 ≈ 0.5) and alkaline peptone water (APW) of 3% (m/v) NaCl were mixed uniformity by the ratio of 1:200 (v/v). ZnO/PAA composite films (0.5 × 0.5 cm) were immersed in the diluted inoculums of 3 mL and incubated at 28 °C for a certain time. Under this condition, Shewanella putrefaciens grew well and showed strong proliferative ability.
Adhesion Assay of Shewanella putrefaciens Biofilms on ZnO/PAA Composite Films
After cultivating in bacterium suspension of Shewanella putrefaciens for a certain time, the ZnO/PAA composite films with biofilm were transferred to another sterile centrifuge tubes and washed three times with 1 mL of 0.85% (m/v) sterile NaCl solution to remove the free bacteria. The biofilm was stained with 1 mL of 0.2%w/w crystal violet for 15 min at room temperature and was washed three times with 1 mL of 0.85% (m/v) sterile NaCl solution to remove redundant crystal violet. Then, the stained biofilms were ultrasonically stripped in 33% (v/v) acetic acid of 200 μL at 53 kHz, 280 W for 10 min. The OD595 (optical density at 595 nm) of the above solution was recorded by a VICTOR™ X3 microplate reader (Perkin Elmer, America) in the 96-well microtiter plates. The results were shown as “averages ± standard deviations” of the thrice parallel experiment.
Total Bacterial Count Assay of Shewanella putrefaciens Biofilm on ZnO/PAA Composite Films
The ZnO/PAA composite films with biofilm were washed three times with sterile phosphate-buffered saline (PBS, pH 7.4; 137 mmol/L NaCl, 2.7 mmol/L KCl, 10 mmol/L Na2HPO4, and 1.8 mmol/L KH2PO4) to dislodge floating bacteria, and the stained biofilms were ultrasonically stripped in 10-mL sterile PBS at 53 KHz, 280 W for 10 min. Subsequently, the total bacterial count in the biofilms was measured by plate count method. With the thrice parallel experiment, the results were shown as “averages ± standard deviations,” and the colony growth curve of the biofilm bacteria was drawn.
The Micrographs Measurement of Shewanella putrefaciens Biofilms
After removal of the floating bacteria, the ZnO/PAA composite films with biofilm were immersed in 2.5% (w/v) glutaraldehyde at 4 °C for 4 h. Subsequently, the samples were dehydrated every 30 min with 50, 70, 80, and 90% (v/v) ethanol, respectively. After being dipped in the absolute ethyl alcohol for 1 h, the samples were naturally air dried on a clean bench. The surface micrographs of the samples were imaged by FESEM (S-4800, Hitachi, Japan) after gold sputter coated at 3 kV for 40 s.
The CLSM Measurement of Shewanella putrefaciens Biofilms
The ZnO/PAA composite films with biofilm were washed with phosphate-buffered saline (PBS, pH = 7.4) for three times to remove the floating bacteria, and the samples were stained in the dark for 15 min in the mixed solution of 0.01wt% acridine orange (AO, Sigma, America) and 0.1wt% propidium iodide (PI, Sigma, America). After that, the samples were washed three times with PBS to dislodge the redundant dyeing solution, and the excessive moisture was dislodged. Ten microliters of anti-fluorescence quenching sealing agents (Biosharp BL701A, China) was dropped on the biofilms, and the samples were stored at 4 °C without light. The proportions of alive and dead cells of the biofilms were observed using confocal laser scanning microscope (CLSM, TCS-SP5 II, Germany Leica Instrument Co., Ltd.) [31, 32].
Results and Discussion
Characterization of ZnO Films
XRD Characterization of the ZnO Powders Prepared by Sol-gel Process
Only bound water from Zn(CH3COO)2·2H2O is produced in the ethanol solution of Zn(CH3COO)2, and the hydrolyzation of CH3COO− is inhibited. Firstly, the Zn(CH3COO)2 is hydrolyzed and produced the intermediate product.
4Zn(CH3COO)2·2H2O → Zn4O(CH3COO)6 + 2CH3COOH + 3H2O(1)
In the heating process, the collosol is facilitated by the ethanol solution of NaOH, and the space steric effect of CH3COO− is of great importance for the stability of ZnO collosol. Meanwhile, the neutral reaction of CH3COOH with NaOH happens.
5Zn4O(CH3COO)6 + 22NaOH + 13H2O → 4Zn5(OH)8(CH3COO)2·2H2O + 22CH3COONa(2)
CH3COOH + NaOH→CH3COONa + H2O(3)
Spanhel and Anderson  indicated that the zinc oxide alcogels are formed from ZnO grains through aggregation and Ostwald Growth (aging). Then, the intermediate of Zn5(OH)8(CH3COO)2·2H2O is heated and decomposed into ZnO phase [36, 37]. Thus, the hexagonal wurtzite structure of ZnO is the basis of the dried gelatin before calcinations.
Zn5(OH)8(CH3COO)2·2H2O → 5ZnO + 2CH3COOH + 5H2O(4)
Hosono et al.  have confirm this reaction mechanism. The ethanol solution of Zn(CH3COO)2·2H2O turned colloidal products during heating at 60 °C, and XRD results show that the dry product of gelatin is a mixture of crystalline ZnO and Zn5(OH)8(CH3COO)2·2H2O. After refluxing for 48 h, the particles are transformed into the wurtzite ZnO.
FT-IR Characterization of the Unmodified/Modified Zinc Oxide Films
Micromorphologies Analysis of PAA Films
According to the theory of acidic field-assisted dissolution (AFAD) , in the anodization process, the oxide films of barrier layer became non-uniform, and the ridges are formed. At these points, the formation and development of the microporous are promoted by the aggravated AFAD. With the second anodization time prolonging, the ordered and through holes are formed gradually on the surface, and then the multilayer shell frames and ridges disappeared (Fig. 4b–d). The result is similar to Reddy’s, which prepared PAA via two-step anodization process in 0.3 mol/L oxalic acid .
Micromorphologies Analysis of ZnO Films
The above results show that the collosol particles easily enter into big holes and attach to the inner surface under vacuum condition; however, the collosol particles only attach to the skeletons of exterior surfaces of PAA with the small holes.
The lattice planes (100), (101), (102), (110), and (103) of hexagonal wurtzite structure ZnO are shown in SAED patterns (Fig. 6b, d), indicating that ZnO is a hexagonal wurtzite. The results are coincident with the XRD analysis.
Hydrophobicity-Hydrophilicity Characterization of the ZnO Film Surface
Water contact angle of the ZnO films prepared on PAA with different times of two-step anodization duration
Time of two-step anodization duration (min)
CA of the surface
Before modification (°)
After modification (°)
75.5 ± 0.3
125.5 ± 0.3
29.6 ± 0.3
149.8 ± 0.3
45.9 ± 0.3
107.1 ± 0.3
61.5 ± 0.3
99.3 ± 0.3
Before modification, the ZnO films are hydrophilic due to the surface hydroxyl groups on the ZnO particles. The hydrophilicity is the best due to its porous structure which prepared on PAA surface with two-step anodization duration of 40 min. For the other samples with two-step anodization duration of 60 and 80 min, the hydrophilies decreases gradually because of the low adhesive quantity of ZnO. For the sample with one-step anodization duration, the low hydrophily is due to its non-porous structure.
After modification, the ZnO films are translated into hydrophobic. According to FT-IR analysis, the triethoxysilylpropyl is grafted on the samples after –S–S– bonds of Si69 rupture. Meanwhile, it could be a result of its porous structure and more ZnO particles; the film has the highest hydrophobicity with two-step anodization duration of 40 min.
Characterization of Shewanella putrefaciens Biofilms
Chi et al.  reported that anodized aluminum has no antibacterial activity to Gram-negative bacteria(Escherichia coli and P. aeruginosa) and Gram-positive bacteria (Streptococcus faecalis and Staphylococcus aureus). However, ZnO has an excellent antibacterial and antibiofilm activity [25, 26, 27], and there is a positive correlation between antibacterial and antibiofilm activity [48, 49]. Furthermore, the antibacterial properties of ZnO are affected by its microstructure [50, 51]. In order to obtain an excellent antibiofilm activity surface, the ZnO films with different microstructure were prepared on PAA films with different times of second anodization duration, and the antibiofilm properties were measured.
The Adhesion of the Biofilms and Growth Curves of the Biofilm Bacteria
The formation and development of bacterial biofilm can be concluded in five stages: the reversible adhesion of bacteria to the surface initially; the conversion from the reversible adhesion to the irreversible adhesion; the initial formation of the biofilm; the development of the matured biofilm; and the degenerating of the biofilm and the bacteria return to planktonic state .
In addition, for the ZnO film prepared on the PAA surface with two-step anodization duration for 80 min, the adherence of the biofilm and the total amount of biofilm bacteria are both the highest among the four samples. However, for the ZnO film prepared on the PAA surface with two-step anodization duration for 40 min, the antibiofilm property is optimal. This could be because of the biofilm adherence that is inhibited by the highest hydrophobicity, and then less exopolysaccharides (EPS) and the other nutrient against the growth of biofilm bacterial. For the ZnO film prepared on the PAA surface with two-step anodization duration for 80 min, its hydrophily is good for the initial adherence of the biofilm, and less ZnO particles do not inhibit the growth of the biofilm bacteria. Meanwhile, more biofilm adhesive materials nourish the biofilm bacteria, and the biofilm bacteria multiply rapidly. Consistent with our research, the biofilm adherence is inhibited by the higher hydrophobicity of ZnO film in the initial stage of the biofilm formation . The adherence of biofilms is affected by the hydrophobic and hydrophilic properties of the materials [14, 53, 54]. Bonsaglia et al.  reported that L. monocytogenes adhere to the hydrophilic surface more easily than to the hydrophobic surface. Many studies found that the bacterial adhesion is reduced or inhibited by hydrophobic surface [47, 54]. Shaer et al.  indicated that the biofilm colonization on the functionalizing orthopedic hardware could be prevented by hydrophobic polycations. Chen et al.  also suggested that the biofilm could be inhibited by low surface free energy. The results matched those from us.
The Morphological Characteristics of Shewanella putrefaciens Biofilm
After cultivated for 2 h, there are less adhesive materials on the ZnO film prepared on PAA without two-step anodization (a) and with two-step anodization duration for 40 min (b), but more adhesive materials and a few bacteria on the other two (c, d). It is indicated that the anti-adhesive properties of the former two are better than the latter two, it is consistent with Fig. 7. After cultivated for 12 h, more and more EPS and bacteria are attached to ZnO films, signifying the rapid growth of the biofilm. At 24 h, the EPS films are thickened gradually and biofilm bacteria grew well, indicating mature biofilms. At 36 h, the deciduous EPS films and dead bacteria illustrate the biofilm degenerating stage.
According to the antibacterial mechanisms of dissolved metallic ions, the dissolved zinc ions are combined with active proteinase of bacteria, make proteinase lose its bioactivity, and damage its bacterial cells to death [34, 56]. Thus, the antibacterial properties of the former two (a, b) are superior to the latter two (c, d) due to their plentiful ZnO particles on the films. Xie  and Jones  also thought that the antibacterial abilities strengthened with the dosage increasing of ZnO particles. Meanwhile, the adhesive materials and bacteria on the sample (d) are all more than the others, according to the analysis of adhesion of Shewanella putrefaciens biofilm and colony growth curve of the biofilm bacteria (Fig. 7). Feng et al.  found that the hypha of Escherichia coli easily reached into the PAA pores with diameters of 50 and 100 nm, and the biofilm accumulated and adhered to the surface of PAA. However, there is no hypha of Shewanella putrefaciens could be observed in our study. It can be inferred that the optimal antibiofilm properties are ascribed to the lower hydrophobicity of ZnO film in the initial stage of the biofilm formation.
The CLSM Characteristics of the ZnO/PAA Composite Biofilms
In this work, the PAA films with different microstructures were prepared by two-step anodic oxidation first, and then the ZnO/PAA composite films are prepared by sol-gel. The ZnO films are hydrophilic due to the surface hydroxyl group on the ZnO particles. After being modified by Si69, the ZnO films translate to hydrophobicity because of its hydrophobic group. The antibiofilm properties of the ZnO films are affected by the hydrophobicity and amount of ZnO particles. The hydrophobicity inhibits the initial adherence of the biofilm and less EPS and the other nutrient against the growth of biofilm bacteria. So, the antibiofilm properties of the ZnO/PAA film are optimal which are prepared on the PAA surface with two-step anodization duration for 40 min because of its super-hydrophobicity and plenty of ZnO particles.
This study was supported by the National Key Research and Development Program “Key Techniques of Green Manufacturing of Preservatives and Antioxidants” (2016YFD0400805) and the National Natural Science Foundation of China (No. 31371858), Food Safety Key Laboratory of Liaoning Province and Engineering and Technology Research Center of Food Preservation, Processing, and Safety Control of Liaoning Province.
SX contributed to the concepts and design; experimental studies; data acquisition, analysis, and interpretation; manuscript preparation, editing, and revision; and manuscript’s final version approval. TS is the guarantor of integrity of the entire study and contributed to the study concepts and design; manuscript revision/review; and manuscript’s final version approval. QX is the guarantor of integrity of the entire study and contributed to the concepts and design of the study. CD, YD, and LW contributed to the experimental studies. QS revised the manuscript. All authors read and approved the final manuscript.
The authors declare that they have no competing interests.
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
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