<i>E. coli</i> Bacteriostatic Action Using TiO<sub>2</sub> Photocatalytic Reactions

Rojviroon, Thammasak; Sirivithayapakorn, Sanya

doi:https://doi.org/10.1155/2018/8474017

International Journal of Photoenergy

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Abstract Introduction Experimental Results and Discussion Conclusion Data Availability Conflicts of Interest Acknowledgments References Copyright Related Articles

Research Article | Open Access

Volume 2018 | Article ID 8474017 | https://doi.org/10.1155/2018/8474017

E. coli Bacteriostatic Action Using TiO₂ Photocatalytic Reactions

Thammasak Rojviroon¹and Sanya Sirivithayapakorn²

Academic Editor: Mohammad Al-Amin

Received12 Apr 2018

Accepted03 Jul 2018

Published07 Aug 2018

Abstract

This experimental research comparatively investigates the Escherichia coli (E. coli) bacterial inactivation of the TiO₂ photocatalytic thin films fabricated by the sol–gel dip-coating (SG) and low-temperature spray-coating (SP) techniques, with low-intensity (12 μW·cm⁻²) UVA-light-emitting diodes (UVA-LED) as the light source. The bacteriostatic experiments were undertaken using the nutrient broth (NB) and 0.85% NaCl with the initial E. coli concentrations of 10², 10⁴, 10⁶, and 10⁸ CFU·mL⁻¹. Moreover, the essential physical characteristics of the SG-TiO₂ and SP-TiO₂ photocatalytic thin films were determined prior to the experimental bacterial inactivation. The findings showed that both photocatalytic thin films possessed the ideal physical characteristics, especially the SP-TiO₂ thin film. In addition, the viable cell counts, the cell morphology, and the bioluminescence-based adenosine triphosphate (ATP) indicated that both SG-TiO₂ and SP-TiO₂ thin films under UVA could effectively inhibit the proliferation of the E. coli cells in both NB and 0.85% NaCl.

1. Introduction

The recent decades have witnessed a growing interest in the development of innovative antibacterial technologies against pathogens in the aquatic environment. The phenomenon is attributable to the drawbacks inherent in the existing technologies, including the implementation challenge, the high operation and maintenance costs, and the carcinogenic effects [1–3]. Moreover, the long-term use of antibiotics could cause the bacteria to become antibiotic-resistant and render the drugs less effective in controlling the spread of diseases [4, 5].

One such innovative antibacterial technology is the photocatalytic reactions in the presence of a semiconducting solid catalyst, which generate the free radicals, that is, hydroxyl radicals (^•OH) and superoxide radicals (^•O₂⁻), which are naturally strong oxidizing agents [6, 7]. In fact, the photocatalytic technology has been utilized in numerous applications, including deodorization, bacterial and viral disinfection, and air and water decontamination [8–11]. The technology is also easy to implement as it essentially requires an ultraviolet light source and a photocatalyst. The most commonly used photocatalyst is titanium dioxide (TiO₂) due to its high levels of photocatalytic activity, prolonged chemical stability, and low toxicity and production cost [12, 13].

Specifically, this experimental research comparatively investigates the TiO₂ photocatalytic thin films fabricated by the sol–gel dip-coating (SG) and low-temperature spray-coating (SP) techniques. In the experiment, the low-intensity UVA-light-emitting diodes (UVA-LED) were used as the light source because they are safer than UVB and UVC, easy to install, inexpensive, lightweight, and energy efficient [14, 15]. Prior to the experimental bacterial inactivation, the essential physical characteristics of the SG-TiO₂ and SP-TiO₂ photocatalytic thin films were determined, including the crystalline phase, bandgap energy, contact angle, morphology, adhesion, and acid-base corrosion resistance.

The experimental bacterial inactivation was carried out using the nutrient broth (NB) and 0.85% NaCl with the initial E. coli concentrations of 10², 10⁴, 10⁶, and 10⁸ CFU·mL⁻¹ treated with the SG- and SP-TiO₂ photocatalytic thin films and UVA. For comparison, the bacteriostatic activity testing was also conducted in the absence of UVA or the photocatalytic thin films (the control). The bacterial inactivation performance was determined by the viable cell count using the standard plate count (SPC) method and the bioluminescence-based adenosine triphosphate (ATP) test.

2. Experimental

2.1. Preparation of TiO₂ Thin Films

The photocatalytic thin films were fabricated using the sol–gel dip-coating (SG) and low-temperature spray-coating (SP) techniques, whereby the TiO₂ solution was coated onto borosilicate glass slides (40.0 × 85.0 × 0.3 mm) and petri dishes (100 mm in diameter × 15 mm in height). The SG- and SP-TiO₂ thin films on the borosilicate glass slides and the petri dishes were for determination of the physical properties and the E. coli bacteriostatic action, respectively.

The SG-TiO₂ thin film was prepared using the TiO₂ acid-catalyzed sol–gel dip-coating process [16]. The sol–gel solution was prepared using titanium isopropoxide (C₁₂H₂₈O₄Ti, TTIP) and isopropanol (C₃H₇OH) in a volume ratio of 1 : 15 under a pH of 2-3 in a container flushed with N₂ gas at room temperature. The TiO₂ sol–gel solution was then transferred to a container flushed with N₂ gas for dip-coating. In this research, the SG-TiO₂ thin film consisted of five layers of film independently thermally treated: 100°C for the bottom layer and 200, 250, 350, and 500°C for the second, third, fourth, and top layers, respectively.

The low-temperature SP-TiO₂ thin film was produced using the modified TiO₂ composite colloid technique [17]. In the preparation of the TiO₂ composite colloids, 0.01 g of anatase TiO₂ nanoparticles was dispersed in 100 mL of ethanol and polyethylene glycol (PEG) and continuously stirred with a magnetic stirrer at room temperature for 1 hour. The pH of the solution was then adjusted to a pH of 2-3. The colloid solution was then stirred for another 1 hour at room temperature in a container flushed with N₂ and left at room temperature for 24 hours.

The TiO₂ colloid-based photocatalyst was then sprayed onto the substrates (i.e., the glass slide and petri dish) in a proprietary spray-coating chamber (Figure 1). The spray-coating process was carried out at room temperature flushed with N₂. In this research, the SP-TiO₂ thin film was made up of five film layers individually treated at 80°C for 2 hours.

2.2. Physical Characteristics of the SG- and SP-TiO₂ Thin Films

In this research, the crystalline phase of both thin films was analyzed using a D8 Advance X-ray diffractometer (Bruker) under a Cu Kα radiation scan range of 10–80°. The bandgap energy was determined with a Helios Alpha UV-Vis spectrometer (Thermo Electron) with a wavelength range of 290–800 nm. The surface morphology of both SG- and SP-TiO₂ thin films was determined using an MFP-3D-BIO™ Atomic Force Microscope (AFM Asylum Research), and the contact angles were obtained by the sessile drop technique using an OCA series TBU90E instrument (DataPhysics). Specifically, the contact angles were the averages of five replications after reposing a 1 mL water droplet on the experimental thin films for 30 seconds.

The AFM images were analyzed by Gwyddion v.2.22 (http://gwyddion.net) for the grain size and the apparent surface area of the thin films. The adhesion between the thin film and the substrate (i.e., the glass slide) was evaluated in accordance with the ASTM D3359B-17 standard. The acid-base corrosion resistance of the experimental thin films was determined by dipping the coated substrates (i.e., the glass slides with the TiO₂ thin film) for 5 minutes independently in 1 M nitric acid and 1 M sodium hydroxide solution [12, 18]. Table 1 tabulates the physical characteristics of interest and the corresponding analysis techniques.

2.3. Photocatalytic Bacterial Inactivation

Gram-negative bacteria E. coli (strain TISTR 073) were used to evaluate the photocatalytic bacterial inactivation of both the SG- and SP-TiO₂ thin films. The stock E. coli in −80°C was inoculated into 10 mL brain heart infusion (BHI) broth and incubated at 37°C for 24 h. The product was then inoculated into 30 mL nutrient broth (NB) that contained 3 g beef extract, 5 g peptone, and 1000 mL distilled water and incubated at 37°C (i.e., the substrate enrichment condition) for the initial E. coli concentrations (N₀) of 10², 10⁴, 10⁶, and 10⁸ CFU·mL⁻¹ (E. coli in NB).

The procedure was repeated for another batch of the products with the E. coli concentrations of 10², 10⁴, 10⁶, and 10⁸ CFU·mL⁻¹ prior to centrifugation at 3000 rpm for 10 min at room temperature. The supernatant was discarded, and the subnatant (i.e., the E. coli cells) was harvested and washed three times with 0.85% NaCl. The bacterial cells were then resuspended in 30 mL 0.85% NaCl (i.e., the nonsubstrate enrichment condition) for the initial E. coli concentrations in 0.85% NaCl of 10², 10⁴, 10⁶, and 10⁸ CFU·mL⁻¹ (E. coli in 0.85% NaCl).

Afterward, 30 mL aliquots of the NB and 0.85% NaCl with the E. coli concentrations of 10², 10⁴, 10⁶, and 10⁸ CFU·mL⁻¹ were transferred to the petri dishes coated with the SG-TiO₂ or SP-TiO₂ thin film and placed under the UVA light source (warm white UVA-LED) in a photoreactor for 180 minutes (Figure 2). The electric power was controlled by a 12 V 3 A power supply AC-DC adapter. The average UVA intensity in the photoreactor was 12 μW·cm⁻² such that the energy falling onto the coating surface in an hour was about 1.2 W·h, measured by the UV Light Meter Model UV-340. In this experimental condition, the cool down was not necessary because the average temperature of the photoreactor increased slightly by 1–3°C. The samples were collected after 30, 60, 120, and 180 minutes to analyze the viable cells using the standard plate count (SPC) method. Prior to the viable cell count, a serial dilution was carried out by introducing 1 mL of each sample into 30 mL of 0.85% NaCl. Then 0.1 mL of the serial dilutions was transferred to the plate count agar (PCA) and incubated 24–48 hours at 37°C. The viable cells of E. coli were subsequently counted.

Moreover, the viable E. coli cells in NB and in 0.85% NaCl (with the initial bacterial concentrations of 10², 10⁴, 10⁶, and 10⁸ CFU·mL⁻¹) treated with the SG- and SP-TiO₂ thin films and UVA were verified against the viable cell counts of the control with the identical initial E. coli concentrations (i.e., those treated with the thin films in the absence of UVA (dark) and those treated with UVA without the thin films). Figure 3 illustrates the overall scheme of this experimental research.

To further verify the photocatalytic bacterial inactivation performance of both thin films, the ATP bioluminescence assay was carried out for the adenosine triphosphate (ATP). The viable E. coli cells were determined by the cellular ATP content using the Lumitester PD-20 (Kikkoman Biochemifa, Japan), based on the detection of light generated by the ATP-dependent enzymatic conversion. Specifically, D-luciferin in the ATP was transformed into oxyluciferin by luciferase whereby the light was generated. The quantity of light emission was measured by the Lumitester and the result expressed as the relative light unit (RLU). The ATP of the viable E. coli cells (in RLU) was the averages of five replications of the E. coli cells in NB and in 0.85% NaCl, given the initial bacterial concentrations of 10², 10⁴, 10⁶, and 10⁸ CFU·mL⁻¹, after 30, 60, 120, and 180 minutes.

3. Results and Discussion

3.1. Physical Characteristics of the Photocatalytic Thin Films

Figure 4 illustrates the X-ray diffraction (XRD) patterns of both experimental thin films, with the peak at the diffraction angle (2θ) of 25.0°. In addition, the analysis results revealed that only the anatase (101) phase (anatase TiO₂, ICSD code: 01-089-4921) was present (no rutile phase) in both thin films.

The bandgap energy () is calculated from the linear relationship of against with extrapolation to zero, which is referred to as the Tauc plot and can be expressed as [13, 19], where is Plank’s constant (eV), is the frequency of vibration, is the absorption coefficient, is a proportional constant, and is the bandgap energy (eV).

Figure 5 illustrates the Tauc plots of both experimental thin films, in which the dotted lines intercepted the x-axis (-intercept) at 3.19 and 3.22 eV for the SG-TiO₂ and SP-TiO₂ thin films, respectively. The findings indicated that the bandgap energies of both thin films were in the range of anatase TiO₂ [20, 21].

In Figure 6, the contact angles of the water droplet on the surface of the SG- and SP-TiO₂ thin films were 46.78° and 57.31°, indicating that both films were hydrophilic [22, 23]. Figures 7(a) and 7(b), respectively, depict the 2D and 3D AFM images of the SG- and SP-TiO₂ thin films, in which the TiO₂ particles were round and uniform and evenly distributed with the grain sizes of 35–90 nm and 25–80 nm for the SG- and SP-TiO₂ thin films. The root mean square (RMS) averages of the roughness of the SG- and SP-TiO₂ thin films were 1.75 and 0.88 nm, respectively, resulting in the smooth surface and elevated hydrophilicity, which in turn contributed to the reduced contact angle and increased polar interaction with the water droplet [24].

(a)

(b)

(a)

(b)

The hydrophilicity of both thin films transformed the oxidation state from Ti⁴⁺ to Ti³⁺, while the photogenerated holes oxidized the O²⁻ anions to O₂. The expulsion of oxygen anions from Ti³⁺ generated ^•OH and ^•O₂⁻ and produced holes which play a crucial role in the photocatalytic activity and bacterial inactivation. In fact, the hydrophilicity, as expressed by the contact angle, could be used to approximate the photocatalytic performance of the TiO₂ thin films [25–27].

In Table 2, the total apparent surface areas per total weight of catalyst of the SG- and SP-TiO₂ thin films were 2.27 and 2.53 m²·g⁻¹, respectively, indicating that the proposed low-temperature spray-coating (SP) technique increased the total apparent surface area. In addition, both thin films exhibited a good substrate adhesion, achieving the 4B classification. For the acid-base corrosion resistance, neither of the thin films showed visible damage, suggesting a high acid-base resistance.

Table 3 compares the physical characteristics of the SG- and SP-TiO₂ photocatalytic thin films with those of existing research studies using variable coating techniques. Unlike the other techniques whose curing temperatures were in the range of 250 to 500°C, the curing temperature of the SP-TiO₂ thin film of this research was only 80°C. Notably, the SP-TiO₂ thin film possessed the physical characteristics resembling those fabricated under the high temperature conditions. In addition, the low-temperature spray-coating technique requires smaller amounts of TiO₂ and is applicable to the substrates with low thermal resistance. The proposed spray-coating scheme could also be applied to materials with large surface areas at minimal costs and short fabrication time.

3.2. Photocatalytic Bacterial Inactivation

The photocatalytic bacterial inactivation experiments were performed with four initial E. coli concentrations in NB and 0.85% NaCl of approximately 10², 10⁴, 10⁶, and 10⁸ CFU·mL⁻¹. The SPC was used to quantify the viable cells under the substrate enrichment condition (in NB) and the nonsubstrate enrichment condition (in 0.85% NaCl). For comparison, this research also determined the viable cell counts of the control, given the same initial E. coli concentrations (i.e., those treated with the thin films in the absence of UVA (dark) and those treated with UVA without the thin films).

Table 4 compares the E. coli inactivation performance of the SG- and SP-TiO₂ photocatalytic thin films under the UVA light, given the initial bacterial concentrations in NB and 0.85% NaCl of 10², 10⁴, 10⁶, and 10⁸ CFU·mL⁻¹. The results revealed that the thin-film type (SG- or SP-TiO₂ thin film) had no significant impact on the bacterial inactivation performance. In addition, given the same E. coli concentration, the photocatalytic bacterial inactivation in 0.85% NaCl was higher than in NB because the 0.85% NaCl solution was unconducive to the bacterial proliferation. Nevertheless, both experimental thin films under the UVA light were effective in inhibiting the proliferation of the E. coli cells in NB (10², 10⁴, 10⁶, and 10⁸ CFU·mL⁻¹).

Figures 8(a) and 8(b) illustrate the photocatalytic bacterial inactivation of the SG-TiO₂ thin film under UVA (SG/NB/UVA and SG/NaCl/UVA) relative to that of the control (SG/NB/dark, NB/UVA, SG/NaCl/dark, and NaCl/UVA), given the initial E. coli concentrations in NB and 0.85% NaCl of 10², 10⁴, 10⁶, and 10⁸ CFU·mL⁻¹. Meanwhile, Figures 8(c) and 8(d) depict the bacteriostatic activity of the SP-TiO₂ thin film under UVA (SP/NB/UVA and SP/NaCl/UVA) vis-à-vis that of the control (SP/NB/dark, NB/UVA, SP/NaCl/dark, and NaCl/UVA), given the same initial E. coli concentrations.

(a)

(b)

(c)

(d)

Figure 8

The photocatalytic bacterial inactivation, given the initial E. coli concentrations in NB and 0.85% NaCl of 10², 10⁴, 10⁶, and 10⁸ CFU·mL⁻¹: (a) NB treated with SG-TiO₂ thin film and UVA relative to the control (SG/NB/dark and NB/UVA), (b) NaCl treated with SG-TiO₂ thin film and UVA relative to the control (SG/NaCl/dark and NaCl/UVA), (c) NB treated with SP-TiO₂ thin film and UVA relative to the control (SP/NB/dark and NB/UVA), and (d) NaCl treated with SP-TiO₂ thin film and UVA relative to the control (SP/NaCl/dark and NaCl/UVA).

The results revealed that both SG- and SP-TiO₂ thin films, with the UVA exposure, were able to inhibit the proliferation of E. coli under the substrate enrichment (NB) and nonsubstrate enrichment (0.85% NaCl) conditions. Specifically, in the absence of the UVA light or the photocatalytic thin films (SG/NB/dark, SG/NaCl/dark, SP/NB/dark, SP/NaCl/dark, NB/UVA, and NaCl/UVA), the E. coli growth was normal. On the other hand, with the UVA exposure and the thin films (SG/NB/UVA, SG/NaCl/UVA, SP/NB/UVA, and SP/NaCl/UVA), the bacterial abundance declined. The reduction in the E. coli cells indicated that both photocatalytic thin films, given the UVA exposure, could effectively inhibit the bacterial growth. In addition, the photocatalytic bacterial inactivation performance increased with the elongated UVA irradiation time.

The bacterial inactivation analysis revealed that neither TiO₂ nor UVA could independently inhibit the growth of E. coli. In fact, the concurrent deployment of the photocatalytic thin film (SG- or SP-TiO₂ thin film) and the UVA light source is imperative to induce the bacteriostatic activity of the E. coli cells. The results showed that both thin films were good enough to inhibit the growth of E. coli cells (bacteriostatic) but not kill them (bactericidal). Since this prepared photocatalyst can be applied onto different surfaces, there are potential applications for surfaces that are needed to control the proliferation of bacteria, such as a kitchen counter, inside surface of a refrigerator, and door knobs, in order to gain benefit through a more eco- and environment-friendly process when compared to the use of harmful chemicals.

Figure 8 indicates the abundance of ^•OH species [32, 33]. ^•OH is bacteriostatic or even bactericidal and is an oxidizing agent stronger than chlorine, hydrogen peroxide, or even ozone [18, 34–36]. ^•OH is generated as the holes in the valence band oxidize H₂O molecules to generate ^•OH for the oxidation pathway and O₂ captures the electrons in the conduction band to produce ^•O₂⁻ and subsequently generate ^•OH for the reduction pathway [32, 33]. The high photocatalytic bacteriostatic action was attributable to the oxidation of E. coli by ^•OH and ^•O₂⁻. In Figure 8, the reaction kinetics of photocatalytic bacterial inactivation under a UVA-LED light can be described by pseudo first-order kinetics, and the highest kinetics constants for E. coli concentrations in NB and 0.85% NaCl of 10² CFU·mL⁻¹ were 4.5 × 10⁻³ and 5.8 × 10⁻³ min⁻¹ for the SG-TiO₂ thin film, respectively, and were 4.1 × 10⁻³ and 6.0 × 10⁻³ min⁻¹ for the SP-TiO₂ thin film, respectively.

Moreover, the bacteriostatic activity was further verified with the FE-SEM images of the E. coli cells, in addition to the SPC method. Figures 9(a)–9(d) illustrate the morphology and structure of the E. coli cells in NB and 0.85% NaCl after 180 minutes (at termination) treated with the SG- and SP-TiO₂ thin films and UVA irradiation, given the initial bacterial concentration of 10⁴ CFU·mL⁻¹, vis-à-vis the control (Figure 9(e)). The FE-SEM images showed that, with the photocatalytic thin films and UVA, the outer cell membranes exhibited the deformation or even destruction (Figures 9(a)–9(d)).

(a) SG/NB/UVA

(b) SP/NB/UVA

(c) SG/NaCl/UVA

(d) SP/NaCl/UVA

(e) Control experiment with only UVA

In Figures 9(a)–9(d), the E. coli cells were mostly either irreversibly deformed or collapsed, with fissures and pits visible on the cell membrane, indicating the loss of integrity and viability of the E. coli cells, consistent with [37–40]. In fact, the bacterial inhibition performance of the SG-TiO₂ thin film, given the UVA exposure, resembles that of the SP-TiO₂ thin film. The similarity could be attributed to the similar total apparent surface areas of the SG-TiO₂ (2.27 m²·g⁻¹) and SP-TiO₂ (2.53 m²·g⁻¹) thin films.

In Figure 10, the ATP of the E. coli cells treated with the SG- and SP-TiO₂ thin films, with and without UVA, validated the SPC results and the bacteriostatic activity. Specifically, the ATP declined as the viable cells decreased, which subsequently led to the decline in the cellular metabolic rates and the eventual cell death.

(a) ATP of E. coli cells in the NB and 0.85% NaCl treated with the SG-TiO2 thin film and with or without UVA

(b) ATP of E. coli cells in the NB and 0.85% NaCl treated with the SP-TiO2 thin film and with or without UVA

In short, the concurrent use of the SG- or SP-TiO₂ thin film and UVA could effectively inhibit the proliferation of the E. coli cells in both NB and 0.85% NaCl. However, the elevated initial E. coli concentrations in NB and 0.85% NaCl lowered the photocatalytic bacterial inactivation performance, due to the restricted active photocatalytic surface site [41–43] and the subsequently lower ^•OH and ^•O₂⁻ [9, 44, 45].

4. Conclusion

The aim of this experimental research is to comparatively examine the E. coli bacterial inactivation of the SG-TiO₂ and SP-TiO₂ photocatalytic thin films under the low-intensity UVA light source. The bacteriostatic experiments were undertaken using the NB and 0.85% NaCl with the initial E. coli concentrations of 10², 10⁴, 10⁶, and 10⁸ CFU·mL⁻¹. The bacteriostatic activity assessments were also carried out without UVA or the photocatalytic thin films (the control). The experimental results revealed that both SG-TiO₂ and SP-TiO₂ photocatalytic thin films possessed the ideal physical characteristics, especially the SP-TiO₂ thin film given its lower fabrication temperature (80°C), subsequent lower energy demand, minimal TiO₂ requirement, and applicability to large surface area objects. In addition, both photocatalytic thin films could effectively inhibit the proliferation of E. coli under the low-intensity UVA irradiation, as evidenced by the lower viable cell counts. The bacterial inactivation performance was further verified by the FE-SEM images of deformed E. coli cells and the ATP measurement. Nevertheless, the E. coli inactivation efficiencies declined as the initial bacterial concentration increased due to the restricted active photocatalytic surface site and the subsequently lower ^•OH and ^•O₂⁻.

Data Availability

The data used to support the findings of this study are available from the corresponding author upon request.

Conflicts of Interest

The authors declare that they have no conflicts of interest.

Acknowledgments

The authors would like to express their deep gratitude to the Thailand Research Fund for TRF Grant for New Researcher (2014): TRG 57802545, and to Rajamangala University of Technology Thanyaburi for the technical assistance.

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Copyright © 2018 Thammasak Rojviroon and Sanya Sirivithayapakorn. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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International Journal of Photoenergy

E. coli Bacteriostatic Action Using TiO2 Photocatalytic Reactions

Abstract

1. Introduction

2. Experimental

2.1. Preparation of TiO2 Thin Films

2.2. Physical Characteristics of the SG- and SP-TiO2 Thin Films

2.3. Photocatalytic Bacterial Inactivation

3. Results and Discussion

3.1. Physical Characteristics of the Photocatalytic Thin Films

3.2. Photocatalytic Bacterial Inactivation

4. Conclusion

Data Availability

Conflicts of Interest

Acknowledgments

References

Copyright

E. coli Bacteriostatic Action Using TiO₂ Photocatalytic Reactions

2.1. Preparation of TiO₂ Thin Films

2.2. Physical Characteristics of the SG- and SP-TiO₂ Thin Films