Photocatalytic water disinfection under the artificial solar light by fructose-modified TiO2

Accepted Manuscript Photocatalytic water disinfection under the artificial solar light by fructosemodified TiO2 Paulina Rokicka-Konieczna, Agata Markowska-Szczupak, Ewelina KusiakNejman, Antoni W. Morawski PII: DOI: Reference:

S1385-8947(19)30892-7 https://doi.org/10.1016/j.cej.2019.04.113 CEJ 21533

To appear in:

Chemical Engineering Journal

Received Date: Revised Date: Accepted Date:

30 December 2018 15 April 2019 16 April 2019

Please cite this article as: P. Rokicka-Konieczna, A. Markowska-Szczupak, E. Kusiak-Nejman, A.W. Morawski, Photocatalytic water disinfection under the artificial solar light by fructose-modified TiO2, Chemical Engineering Journal (2019), doi: https://doi.org/10.1016/j.cej.2019.04.113

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Photocatalytic water disinfection under the artificial solar light by fructose-modified TiO2 Paulina Rokicka-Konieczna*, Agata Markowska-Szczupak, Ewelina Kusiak-Nejman, Antoni W. Morawski West Pomeranian University of Technology, Szczecin, Faculty of Chemical Technology and Engineering, Institute of Inorganic Technology and Environment Engineering, Pułaskiego 10, 70-322 Szczecin, Poland *Corresponding author E-mail address: [email protected]

Highlights 

TiO2 was modified by hydrothermal method with fructose as a carbon source.



Antibacterial activity was enhanced both under UV-A and artificial solar light.

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Antibacterial activity of fructose-modified TiO2 depends mainly on carbon content.

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Modification increases the amount of surface -OH groups and the photocatalytic efficiency.

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The two-stage photocatalytic mechanism of bacteria destruction by •OH radicals was found.

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Abstract This study presents a simple method of titanium dioxide modification by carbon. Monosaccharide (fructose) was used as the carbon source. The pressure modification using fructose caused enhancement of antibacterial efficiency. It was found that prepared photocatalysts were capable of total Escherichia coli and Staphylococcus epidermidis inactivation under the UV-A and artificial solar light, which was attributed to the changes of the surface characteristics, i.e. zeta potential. The best results were observed for the TiO2-F-1%-100 photocatalyst, containing 0.51 wt% of carbon with less negative zeta potential (-18.08 mV). The two-stage photocatalytic mechanism of bacteria destruction by •OH radicals was found. Obtained data suggest that fructose-modified photocatalysts may be useful in the development of alternative water disinfectants.

Keywords: photocatalysis, titanium dioxide, carbon modification, fructose, antibacterial activity

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1. Introduction Water is an essential compound for the development of all forms of life. Unfortunately, water is also the main route of microorganism transmission, including pathogenic bacteria. Due to their negative impact on human health, the microbial quality of water engages more and more attention from the general public [1]. Numerous disinfection technologies characterized by varied efficacy are currently implemented for water treatment. Their applications are limited through several shortcomings such as the formation of unwanted by-products (e.g. chlorination) or high costs (e.g. ozonation) as well low efficiency against some of the water microorganisms (e.g. chlorination) [2], [3], [4]. For that reason, particular attention should be paid to the development of a more effective, safer and relatively inexpensive method for water disinfection. The promising methods seem to be Advanced Oxidation Processes (AOPs), which constitute a technology capable of degrading wide spectrum of non-easily removable organic contaminants and microbes [5], [6], [7]. Among the different AOPs systems, photocatalysis is one of the well-known [8], [9], [10]. In the photocatalysis system, different semiconductors have been applied but titanium dioxide is one of the most widely studied [11]. Unfortunately, TiO2 can be activated only under UV-A irradiation (λ= 315-400 nm) [10], [12]. Therefore, many researchers have been focusing on the activation of titanium dioxide under solar irradiation [13], [14], [15], [16]. In order to enhance the photocatalytic activity of TiO2 under sunlight, many different ways of modification have been applied, i.e. doping with metal/non-metal elements [17], [18], sensitizing of TiO2 with dyes [19], coupled of TiO2 with other semiconductors [20] or polymers [21] and carbon-based material such as graphene [22], [23]. On the basis of the literature reviews, it has been shown that carbon modification of titania resulted in a significant enhancement of photoactivity under solar irradiation [24], [25]. One of the carbon

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sources can be saccharides- inexpensive and nontoxic carbon precursors. Many authors reported that photocatalyst formed through modification by saccharides (glucose or sucrose) demonstrated better photocatalytic activity (than commercial TiO2) under visible light irradiation. The improvement of photocatalytic activity of glucose-modified TiO2 materials was observed while decomposition: toluene [26], rhodamine B [27], [28], reactive red [29] and even olive mill [30], caffeic acid [31] or pharmaceuticals like carbamazepine and diclofenac [32]. Organic pollutants that have been reported to be removed by saccharosemodified photocatalysts include, i.e. methylene blue [33] or methyl orange [34]. Our previous studies have also shown that glucose-modified TiO2 presented good biocidal effectiveness against bacteria [35], [36]. However, according to our best knowledge, there is a lack of information concerning the antimicrobial properties of photocatalysts modified with fructose. Fructose and glucose are both monosaccharides with the same chemical composition but a different molecular structure. As mentioned above modification of TiO2 by glucose was promising, thus, in this study, we wanted to check the influence of fructose monosaccharide on antibacterial properties of hydrothermally modified TiO2. There are a number of methods of TiO2 modification [14]. According to Byrappa and Adschiri [37] and Rao et al. [38] hydrothermal method is one of the most promising and frequently applied techniques to produce the nanomaterials [37], [38]. Moreover, hydrothermal synthesis is relatively inexpensive and environmentally friendly that allows generating nanomaterials without hazardous wastes and by-products [38], [39]. It has been shown that hydrothermal modification of TiO2 led to obtaining photocatalysts with improved photocatalytic activity. Ho et al. [40] found that S-doped TiO2 prepared by low-temperature (180°C) hydrothermal treatment of TiS2 powder in HCl solution presented much higher photocatalytic activity than photocatalyst obtained by the traditional high-temperature thermal annealing method. Ren et al. [27] and Dong et al. [26] prepared a visible-light-active TiO2-C

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photocatalyst by a hydrothermal method at 160°C with glucose as carbon source. In both cases obtained TiO2-C presented higher photocatalytic activity on the degradation of rhodamine B [27] or toluene [26] than the unmodified counterparts and commercial P25 photocatalyst. In turn, Li et al. [41] showed that carbon-doped TiO2 could be successfully prepared by the hydrothermal process at 130°C. According to literature, our paper is the first report of hydrothermally modified TiO2 by fructose at low temperature (100°C). The aim of this work was to investigate the antibacterial properties of photocatalysts obtained by monosaccharide fructose modification and gain more knowledge into the role of carbon-modified TiO2 in microbial inactivation mechanisms. The antibacterial properties of photocatalysts have been evaluated against Escherichia coli and Staphylococcus epidermidis. Gram-negative Escherichia coli is commonly used as a specific indicator of water faecal contamination and considered as biological drinking water indicator for public protection [42]. Staphylococcus epidermidis is a Gram-positive bacteria that is common of the human skin and mucous membrane microflora [43]. Recent studies have shown that S. epidermidis might colonize water allocated to human consumption [44] as well as water in swimming pools [45], [46]. 2. Experimental 2.1. Materials and reagents The intermediate product taken directly from the production line of titanium white from the Grupa Azoty Zakłady Chemiczne "Police" S.A. (Poland) was used as the crude material. The product contains 2.1 wt% of residual sulphur (from post-production sulphuric acid). In order to remove the residual sulfuric acid, the titanium white slurry was washed with 25% of ammonia aqueous solution (Firma Chempur, Poland) and further with distilled water. This material was adjusted to reach near-neutral pH. Then the prepared sample was dried at

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105°C for 24 h and use as starting material. The D-fructose (C6H12O6) used as a carbon source was purchased from Firma Chempur (Poland). 2.2. Preparation of carbon-modified photocatalysts Carbon-modified photocatalysts were obtained in a pressure reactor BHL-800 (Berghof, Germany). 4 g of starting material was mixed with 5 mL of fructose solution in various concentration: 1, 5 and 10 wt% in distilled water. Next, the suspension was transferred to a pressure reactor and heated at 100°C for 4 h under autogenic pressure (approx. 1.6 bar). After that, the reactor was cooled down to room temperature (25°C). In the end, obtained samples were dried for 24 h at 105°C to remove residual water. Starting material was fabricated in the same way but without fructose solution. This sample was used as a control material (denoted as TiO2-100). Commercial carbon-modified TiO2 KRONOClean 7000 (KRONOS Worldwide, Inc., USA) was used as a reference sample. 2.3. Structural characterization The crystalline phase and crystal structure of obtained photocatalysts were identified by means of XRD analysis (PANalytical Empyrean X-ray diffractometer, UK) using Cu Kα radiation (λ=0.154056 nm). The SBET surface area of tested samples was measured by an N2 adsorption-desorption method on a Quadrasorb SI analyzer (Quantachrome Instruments, USA). The micropores volume (Vmicro) was determined by applying the DubininRadushkevich equation using adsorption branches of the measured isotherm. The total pore volume (Vtotal) was calculated on the basis of the adsorbed N2 after finishing pore condensation at a relative pressure p/p₀ = 0.99. Mesopore volume (Vmeso) was determined from the difference between Vtotal and Vmicro. Total carbon content in examined samples was calculated using CN 628 elemental analyzer (LECO Corporation, USA). FTIR/DR spectra of photocatalysts were recorded using FTIR 4200 spectrometer (Jasco International Co. Ltd., Japan) equipped with DR accessory of Harrick Scientific Products Inc. (USA). The

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morphology of photocatalysts and bacteria cells were evaluated by Hitachi SU8020 UltraHigh Resolution Field Emission Scanning Electron Microscope (Hitachi Group, Japan). The zeta potential was determined using ZetaSizer NanoSeries ZS (Malvern Panalytical Ltd., UK). The UV–Vis/DR spectra were recorded in the range of 250–800 nm using a V-650 UV–VIS spectrophotometer (JASCO International Co. Ltd., Japan) equipped with an integrating sphere accessory for studying DR spectra. As the standard sample BaSO4 (purity 98%, Avantor Performance Materials Poland S.A.) was used. 2.4. Determination of •OH radicals. The analysis of hydroxyl radicals formation on the photocatalysts surface under UV-A and artificial solar light (ASL) irradiation was performed by fluorescence technique with terephthalic acid (Acros Organics B.V.B.A, Belgium). The fluorescence product of terephthalic acid hydroxylation, 2-hydroxyterephthalic acid (2-HTA), was detected as an emission peak at the maximum wavelength of 420 nm, with the excitation wavelength of 314 nm. 0.02 g of tested photocatalyst was suspended in a solution of terephthalic acid with the initial concentration of 0.083 g/L. Next, the suspension was exposed to UV-A or artificial solar light for 90 min. Sampling was performed in every 10 min. Suspension (after filtration through 0.45 μm membrane filter) was analyzed on a Hitachi F-2500 fluorescence spectrophotometer (Hitachi Group, Japan). 2.5. Antibacterial tests The antibacterial properties of obtained photocatalysts were evaluated against gramnegative Escherichia coli K12 (ATCC 25922) and gram-positive Staphylococcus epidermidis (ATCC 49461). Before the experiment, E. coli and S. epidermidis bacteria were inoculated into Enriched Broth (Biomaxima S.A., Poland) and Brain Heart Infusion Broth (Biomaxima S.A., Poland), respectively, and were cultured at 37ºC for 24 h. The bacteria cells were harvested by centrifugation at 4000 rpm for 10 min and then washed twice with sterile saline

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solution (0.9% NaCl) and in order to remove broth residues. Finally, the initial microorganisms concentration approx. 1.5 × 107 CFU/mL was calculated by reference to a calibration curve (presented in Supplementary Materials as Figs. SM1) established according to quantitative spectrometric measurements (absorbance versus live cell concentration). All glassware used in antibacterial tests were washed with distilled water and then thermal sterilized at 150°C for 8 h. The experiments were performed in 25 mL glass beaker used as a simple reactor (reactor scheme was presented in Supplementary Materials as Fig. SM2). 2 mL of the bacterial suspension (1.5 × 107 CFU/mL) was added into the reactor containing 18 mL of saline solution (0.9%) and 0.1 g/L of the appropriate photocatalyst. Optimum dosage of photocatalyst (0.1 g/L) and bacteria concentration (approx. 1.5×106 CFU/mL) were determined based on previous works [36], [47]. The reaction suspension was illuminated with artificial solar light for 90 min. The distance between the solution and the light source was fixed at approx. 30 cm. For the evaluation of the number of microorganisms the standard plate count technique was used. The method is one of the most frequently applied in microbiological research and can provide valuable and highly relevant information. The reaction suspension was continuously stirred to ensure homogeneity. 1 mL of the suspension was collected in every 15 min. Next serial tenfold dilutions according to Lister method were appropriately performed. 0.25 mL of diluted suspension was spread over the surface of Plate Count Agar (BioMaxima S.A., Poland) for E. coli or Brain Heart Infusion Agar (Biomaxima S.A., Poland) for S. epidermidis and then incubated at 37°C for 24 h. After incubation, the number of viable colonies was counted and depicted as log CFU/mL. The control experiments in the dark and for the pristine saline solution were also performed. All experiments were repeated 3 times to obtain reliable results and presented as the mean standard deviation. The photocatalytic experiments were carried out under UV-A and artificial solar light (named as ASL)

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irradiation. The employed UV-A light source comprised of four bulbs 20 W each, Phillips Hapro Summer Glow (Royal Phillips, Netherlands) with the radiation intensity of 28.3 W/m2 in the spectral range from 300 to 2800 nm and 39.1 W/m2 in the spectral range from 280 to 380 nm. The artificial solar light source was 300 W light bulb (OSRAM Ultra Vitalux, Poland) with the radiation intensity of 9.0 W/m2 in the spectral range from 300 to 2800 nm and 258.1 W/m2 in the spectral range from 280 to 380 nm. The emission spectra were measured by using Ocean Optics USB 4000 spectrometer (Ocean Optics Inc. USA) and presented in Supplementary Materials as Fig. SM3. 2.6. Kinetics of the photocatalytic disinfection In this work, we studied the disinfection kinetics of E. coli and S. epidermidis using TiO2 photocatalysts. Four classical disinfection models were checked: Chick–Watson model (Eq. (1)), modified Chick-Watson model (Eq. (2)) Hom model (Eq. (3)) and modified Hom model (Eq. (4)). The equations are expressed as follows [48], [49]:

log

( ) =‒ 𝑘𝑡 𝐶 𝐶0

(1)

where: C represents the bacteria concentration [CFU/mL] at time t [min], C0 is the initial bacteria concentration [CFU/mL] and k is the photocatalytic destruction kinetic rate constant.

log

( ) =‒ 𝑘 [1 ‒ exp ( ‒ 𝑘 𝑡)] 𝐶 𝐶0

1

(2)

2

where: the kinetic rate constant k has divided into two parameters expression, i.e., k1 and k2. log

( ) =‒ 𝑘𝑡 𝐶 𝐶0

ℎ

(3)

where: h is a second parameter.

log

( ) = ‒ 𝑘 [1 ‒ exp ( ‒ 𝑘 𝑡] 𝐶 𝐶0

1

2

𝑘3

(4)

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where: k2 and k3 are model parameters of the modified Hom model [50]. Analysis of obtained results was conducted using Statistica 13.3. 2.7. CO2 evolution The possible decomposition products of bacteria mineralization were examined on the basis of CO2 evolution. The amount of generated CO2 was analyzed by gas chromatography. A gas chromatograph GC SRI 8610C (SRI Instruments, USA) was used with a thermal conductivity detector. A stainless steel column packed with Poropak Q (Agilent Technologies, Inc., CA, USA) was used for separation at 40°C with hydrogen as a carrier gas at a flow rate of 30 mL/min. The experiments were carried out similarly to those described in chapter 2.5., in exceptional that instead of a glass beaker the glass tubes (20 mL) sealed with a silicone stopper were used. For CO2 determination, a portion of the gas phase (0.5 mL) of the reaction suspension was collected by a syringe (Hamilton, USA) in every 30 min. The gas sample was injected into the GC system with simultaneous integration of peaks using the Peak Simple 3 software (SRI Instruments, USA). The calibration curve and reactor schemes were presented in Supplementary Materials (Figs. SM4 and SM5, respectively). 2.8. Photocatalysts stability in the simultaneous process The experiments were carried out similarly to those described in chapter 2.5. After each cycle 1 mL of the suspension was collected to estimation the number of viable colonies. At the same time and new portion of E. coli suspension was added. The concentration of bacteria and photocatalyst in the reaction solution at the beginning of each next cycle amounted 1.5 ×106 CFU/mL and 0.1 g/L, respectively.

3. Results and discussion 3.1. Photocatalysts characterization

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Fig. 1 showed the XRD patterns of TiO2-100, fructose-modified TiO2 and commercial KRONOClean 7000 photocatalysts. It was shown that obtained photocatalysts consisted mainly of anatase phase (peaks located at 25.3°, 37.6°, 47.8°, 53.7°, 54.8°, 62.6°, 70.2° and 75.0°) with a small amount of rutile phase (peak located at 27.1°). It was clear that the rutile phase (approx. 2%) resulted from rutile nuclei added in the production process. The diffractograms of carbon-modified photocatalysts did not show any differences compared to the diffractogram of TiO2-100 were due to the low temperature of modification (100°C). Commercial KRONOClean 7000 consisted only of anatase phase, which was in accordance with data obtained from the manufacturer. The physicochemical properties of photocatalysts were presented in Table 1. In Figure 2 the SEM images of tested photocatalysts were presented. It can be observed that the morphology of all photocatalysts was quite homogenous. The TiO2 particles were formed agglomerates. The average size of anatase crystallites of tested photocatalysts was calculated according to the Scherrer's equation [51]. The mean crystallites sizes of tested photocatalysts were from 11 to 12 nm (Table 1). As was shown, carbon modification conducted at low temperature had no significant effect on the particles size. The N2 adsorption-desorption isotherms of examined samples were shown in Fig. 3. The BET specific surface area (SBET), total pore volume (Vtotal), micro (Vmicro) and mesopores volume (Vmeso) as derived from nitrogen adsorption-desorption measurement were presented in Table 2. It was shown that the specific surface area for fructose-modified TiO2 was in a range of 222-267 m2/g. Obtained photocatalysts were mesoporous materials with a small number of micropores. It was noted that the increase of the fructose concentration (in the solution which was used for modification) resulted in a decrease of the SBET surface area and mesopores volume of tested photocatalysts. This was in accordance with our previous studies

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[36]. It was found that a decrease in specific surface area with increasing of carbon precursor content might be associated with the covering anatase crystallites by uniform and a thin layer of sugar. That was also evidenced by slight differences in the average crystallite size of the anatase phase (Table 1). The presence of carbon was also confirmed by elemental analysis of carbon. It was noted that the increase of carbon resulted in a decrease in specific surface area. The carbon content in carbon-modified photocatalysts was from 0.51 to 4.16 wt%. Commercial KRONOClean 70000 contained 0.96 wt% of carbon. FTIR/DRS spectra (Fig. 4) of TiO2-100, carbon-modified TiO2 and KRONOClean 7000 were carried out in order to identify the functional groups on the surface of the photocatalysts. A broad band in the region of 3700-2800 cm-1 was assigned to O–H stretching vibration [52]. Another band located around 1621 cm-1 corresponded to the molecular water bending mode [53]. It can be observed that peaks located at 3700-2800 cm-1 and 1621 cm-1 presented higher intensity after fructose modification in comparison to TiO2-100. This indicated that hydroxyl groups from fructose could bond to the TiO2 surface [54]. A similar result was obtained by Dong et al. [26] who prepared carbon-doped TiO2 nanomaterials by hydrothermal method at 160°C with monosaccharide glucose as a carbon source. According to the literature [55], the strong band at 960 cm-1 corresponded to the self-absorption of titanium (Ti4+). Comparing FTIR/DR spectra with fructose spectrum and data presented in the literature [56], [57] it was found that region located between 700 and 1500 cm-1 presented absorbance bands that were characteristic for saccharide. The band at 1418 cm−1 is a combination of O–H bending of the C–OH group and C–H bending. The peak at 1053 cm-1 corresponded to the C–O stretch in the C–OH group in the carbohydrate structure. A narrow band located around 923 cm-1 was assigned to the C–H bending of the carbohydrate [57]. According to Wiercigroch et al. [58] bands that were found at 976 cm-1, 874 cm−1, 782 cm-1 and 624 cm-1 came from fructose. In case of commercial KRONOClean 7000, a peak at 1580

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cm−1 was attributed to the asymmetric and symmetric stretching vibrations of an aryl carboxylate group. The band at 1330 cm−1 was assigned to the C–O stretching vibrations [59]. The D-fructose modification changed zeta potential from -24.13 mV (TiO2-100) to 18.08 mV (for TiO2-F-1%-100). Additionally, it was noted that with an increase in carbon content in photocatalysts the zeta potential values were more negative. As was reported by Jafari et al. [60] carbon modification caused changes in surface charge via CH3 and HO–CH groups. The presence of these groups (derived from fructose) on the surface of examined photocatalysts was confirmed by FTIR-DRS analysis (Fig. 4). The impact of carbon modification on the zeta potential of photocatalysts was confirmed also by research carried out by Janus et al. [61]. Authors stated that the modification of TiO2 by alcohol (ethanol) led to obtaining C-TiO2 materials characterized by much less negative zeta potential. Fig. 5 presented the UV–Vis/DR spectra of TiO2-100, carbon-modified TiO2 and KRONOClean 7000. TiO2-100 showed high absorption in the UV region and did not show absorption in the visible range. It was observed that carbon modification caused a significant increase in light absorption in the visible region. Moreover, the intensity of visible light absorption increased with the increase in carbon content (Fig 5). These changes can be assigned to the colour change after the modification from white for TiO2-100 and TiO2-F-1%-100 to beige and lightbrown for TiO2-F-5%-100 and TiO2-F-10%-100, respectively. The highest absorption in the visible light region was observed for the photocatalyst contained 4.16 wt% of carbon (TiO2-F10%-100). In Fig. 6 the generation of hydroxyl radicals under UV-A and ASL irradiation was presented. It was noted that after carbon modification studied nanomaterials are characterized by the high fluorescence intensity of 2-hydroxyterephthalic acid. It indicated that modified

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photocatalysts generated more hydroxyl radicals in comparison with unmodified TiO2-100 and commercial KRONOClean 7000. 3.2. Microbial inactivation by fructose-modified TiO2 In the first stage of the study, the control experiments without light activation were conducted. As was shown in Fig. 7 no significant changes in the bacteria number were observed. The survival curves of E. coli (Fig. 7a) and S. epidermidis (Fig. 7b) showed that more than 95% of the cells were alive after 90 minutes incubation in darkness. These results of control experiments indicated that TiO2-100, carbon-modified TiO2 and KRONOClean 7000 did not present bactericidal activity against E. coli and S. epidermidis. In Figs 8 and 9, the results obtained in experiments conducted under UV-A and artificial solar light were presented. As it has been shown fructose-modified TiO2 photocatalysts presented better antibacterial properties in comparison with unmodified TiO2 and commercial KRONOClean 7000 both under UV-A and ASL irradiation. The highest antibacterial activity was observed for TiO2-F-1%-100, which was obtained by modification with 1% of fructose solution. The total bacteria inactivation rate was achieved after 55 min (E. coli) and 60 min (S. epidermidis) of UV-A irradiation. In the case of an experiment performed under ASL irradiation, 100% of the initial bacterial cells were inactivated after 70 min (E. coli) and 75 min (S. epidermidis) respectively. The other pictures of plates with bacteria cells were presented in Supplementary Materials (as Figs. SM6 and SM7). For commercial KRONOClean 7000 no live bacteria cells were found after 80 and 85 min (for E. coli and S. epidermidis respectively) under UV-A irradiation. Under ASL irradiation, the complete disinfection of E. coli and S. epidermidis was achieved after 90 min.

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It should be noted that the antibacterial properties of fructose-modified TiO2 can be closely associated with carbon presence on the photocatalysts surface. The most active sample - TiO2-F-1%-100 contained the lowest amount of carbon (0.51 wt%). The results obtained in these investigations are in excellent agreement with our previous study of the antibacterial properties of photocatalysts modified by monosaccharide - glucose [35], [36] or alcohols [62] as a carbon source. According to Wanag et al. [35] a large amount of carbon in the photocatalysts influence on the deterioration of photocatalytic properties by blocking of the active sites on the TiO2 surface. Zhang et al. [63] reported that high carbon content in TiO2 carbon nanoparticles reducing the photocatalytic activity what was attributed to increased absorbance and scattering of photons through excess carbon in the photosystem. Li et al. [64] observed that the excess of glucose leads to excessive carbon on Bi2WO6 photocatalysts surface. As a result the photocatalyst surface was coated with a thick and dense carbon layer, which prevented light absorption and finally reduce the photoactivity. To better understand the inactivation process of bacterial cells the interaction of the E. coli and exemplary photocatalyst (TiO2-F-1%-100) were examined using scanning electron microscopy (SEM). In Fig. 10 the SEM images of E. coli (10a and 10b) or S. epidermidis (10c and 10d) on TiO2-F-1%-100 sample before and after photocatalytic process were shown. Before the photocatalytic process, the bacterial cells displayed a regular shape and average sizes. Subsequent SEM images have shown that bacterial cells morphology was clearly changed after the photocatalytic process due to the degradation of bacterial cells. After 75 min of radiation, it was difficult to found complete E. coli and S. epidermidis cells. The E. coli (Fig 10b) and S. epidermidis (Fig. 10d) cell walls were damaged and bacteria lost its typical morphology due to the release of the cytoplasmic contents. 3.3. Kinetics of the photocatalytic disinfection

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Fig. 11 have shown the results of the photocatalytic inactivation of E. coli and S. epidermidis in experiments performed with tested photocatalysts. As it can be observed that three different regions can be identified in the plot: a smooth decay at the beginning of the reaction, generally called “shoulder”, next to a log-linear inactivation region that covers most part of the reaction. In the end, the deceleration of the process, usually called “tail” was shown. In order to find a best-fit model for the experimental results concerning the E. coli and S. epidermidis inactivation, four classical disinfection models were used (Chick-Watson, modified Chick-Watson, Hom and modified Hom model). On the basis of the analysis of kinetic parameters, the Hom kinetic model was found to fit best. In Fig 12. kinetic modelling curves for E. coli and S. epidermidis for modified Hom kinetic model are presented. The similar results were found by Marugan et al. [48] and Wang et al. [49]. The kinetic models, rate constants for disinfection models and correlation coefficients (R2) were presented in Supplementary Materials (as SM8-10). 3.4. Bacteria mineralization It has been shown that the photocatalytic process not only inactivates but also causes the decomposition of bacterial cells structures. There are reports that the photocatalytic process has been capable of complete mineralization of cells structure, including nucleic acids to CO2 and water [65]. To study the mineralization of bacterial cells the evolution of carbon dioxide during artificial solar light irradiation was examined, for comparison control experiment in the dark was also performed. Additionally, blank tests (saline solution + tested photocatalyst powder) were also carried out in order to check how photocatalysts contribute to the production of CO2. Firstly, the blank test did not show any significant changes in the amount of CO2 evolved from photocatalysts suspension (Fig. 13). This indicates that all tested photocatalysts did not contribute to the production of CO2. The CO2 evolution from bacterial suspension incubated in the dark was presented in Fig 14. No changes in the amount of CO2

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evolved from E. coli and S. epidermidis suspensions incubated in darkness were observed. It indicated that the mineralization process did not occur. The quantity of evolved CO2 during the photocatalytic process conducted with fructose- modified photocatalysts under UV-A and ASL irradiation were shown in Figs 15 and 16. The activity under UV-A and ASL irradiation of all carbon-modified TiO2 was higher in comparison with TiO2-100. The amount of evolved CO2 increased gradually during the photocatalytic process. As it was shown the highest evolution of carbon dioxide (degree of bacteria mineralization) was achieved in an experiment performed with TiO2-F-1%-100. Both for suspension containing E. coli as well as for S. epidermidis, the quantity of evolved CO2 for TiO2-F-1%-100 was from approx. 3 times (for ASL irradiation) to 5 times higher (for UV-A irradiation) than that for starting TiO2 and commercial carbon modified KRONOClean 7000. It can be also observed, that with the increase of carbon content in C-TiO2 the amount of evolved CO2 decreased. As previously mentioned, the presence of too high carbon content in the photocatalyst reduced the photocatalytic activity. The study of the bacteria mineralization during the photocatalytic process was also examined by Sun et al. [66]. The author investigated the mineralization of E. coli in the presence of a TiO2-Fe2O3 showed that rapid mineralization of bacterial cells was caused mainly by a large number of highly reactive •OH radicals generated during the photocatalytic process [66]. In our study, the highest CO2 evolution (degree of bacteria mineralization) was observed for TiO2-F-1%-100 which was also characterized by the highest amount of •OH radicals generated from the surface. 3.5. Photostability An important factor to evaluate photocatalytic property is also the stability of a photocatalyst. There were concerns that fructose which was used as carbon source might be washed out from TiO2 surface or its derivatives were decomposed during the photocatalytic

17

process. Therefore, the photocatalytic stability of exemplary photocatalysts (TiO2-F-1%-100) using repeated experiments were examined. As was presented in Fig. 17 after 3 continuous cycles of photocatalytic reaction TiO2F-1%-100 still presented good antibacterial properties, showing complete inactivation of E. coli and S. epidermidis after 75 and 80 min of ASL irradiation, respectively. In the fourth cycle bacteria inactivation was slightly slower. After six cycles the photocatalyst was still active and inactivates all bacteria in suspension although much longer time was required for completing the treatment - complete bacteria inactivation were achieved after 110 min (E. coli) and 115 min (S. epidermidis) of ASL irradiation. The decrease in activity following four and more cycles might be attributed to bacteria cell deposition of photocatalysts surface. In general, the mineralization process is much slower than bacteria inactivation. Hence, the inactivated but still no decomposed bacteria cell could block the surface of TiO2 hindered the absorption of UV photons and as a result time needed for total bacteria inactivation should be extended. It can be also mentioned that in some study photocatalysts were separated, washed, dried and reused for the next runs [67]. In our research the photocatalyst was not washed or regenerated in any way. 3.6. The importance of contact between bacteria and titanium dioxide Many studies demonstrated that good biocidal activity of TiO2 is associated with close contact between the bacteria cells and the photocatalyst surface [68], [69]. An important role in the interaction between photocatalyst and bacteria cells played zeta potential of TiO2. Bacterial cell surfaces possess characteristic functional groups on cell walls and cell membranes (e.g. phosphoric, carboxylic, hydroxyl and amine groups) [70]. The presence of functional groups affected the electrostatic behaviour of the cells among others bacterial adhesion to the surface of photocatalysts agglomerates [71], [72]. Consequently, the negatively-charged bacterial cells (E. coli ζ= –44.2 mV and S. epidermidis ζ= –42.3 mV) had

18

better contact with the positive or less negative photocatalysts surface through the electrostatic attraction. In this case, it was found that the TiO2-F-1%-100 had less negative zeta potential (-18.08 mV) what provided a stronger affinity, thus better contact between bacteria cells and photocatalyst surface. However, in our study, it was found that KRONOClean 7000 characterized by the least negative zeta potential (-17.71 mV) showed the lowest antibacterial activity. There is no satisfactory explanation of this phenomenon. This appears to be to another preparation method, carbon source and content (0.96 wt%) that influenced the amount of •OH formed on the surface of the photocatalyst. 3.6. The mechanism of bacteria destruction The fundamental mechanism of titanium dioxide photocatalytic killing process remains largely unknown. There are still many questions over which process and how to lead to the death of microorganism subjected to the photocatalytic process. Therefore, it was also attempted to determine the mechanism of bacteria destruction and mineralization by the fructose-modified TiO2. In order to better understand the mechanisms photocatalytic bacteria destruction, the data for the combination of CO2 evolution, •OH radical formation and E. coli inactivation in experiments performed with TiO2-F-1%-100 were compiled and presented in Fig. 18. On the basis of the obtained results, the two-step mechanism of bacteria destruction in the presence of photocatalyst was proposed. The first stage was relatively short and included bacteria cell wall (plus outer membrane of gram-negative bacteria) and inactivation with selectively lineal •OH radicals formation [73]. The small amount of CO2 evolution indicates the only simple sugars such as pentoses, hexoses, heptoses or amino sugars and uronic acids composing outer membrane (O-antigen in gram-negative bacteria) or cell wall (gram-positive bacteria) were decomposed. Most likely in this phase bacteria could trigger some self-repair and self-defence mechanisms and are resistant to •OH radicals attack [74]. Therefore, in the

19

first minutes of the photocatalytic process, no significant changes in the bacteria number were observed. From about 30 minutes of the photocatalytic process, gradual bacteria inactivation was observed. The self-defence mechanisms were no longer to protect bacteria against •OH radicals. Since •OH could not migrate from the surface of photocatalyst the following hypothesis was put forward. Hydroxyl radicals disrupt transports through protein channels and through lipid bilayer domains. Over the past few years, the several beta-barrel proteins in cellular membrane that act as a pore through nutrient molecules were identified [75]. It is well known that porins composition depends on the species of bacteria. Generally, porins are primarily involved in passively transporting hydrophilic and some hydrophobic molecules but less than 600 Daltons in size [75]. Additionally, porins can regulate permeability and prevent lysis by limiting the entry of e.g. detergents into the bacterial cells. It cannot be excluded that changes in the shape of bacteria observed by SEM technique are caused by a decrease in cell turgor. Porins disruption caused also the uncontrolled leakage of intracellular components and progressive disintegration of the cell. It was confirmed inter alia by images observed at 75 min (Fig 10). This mechanism was approached by various angels. Ren et al. [76] assumed that bacterial death is caused by K+ leakage from E. coli cells, whereas Chen et al. [77] emphasized lipid peroxidation of outer and cytoplasmic membranes. Loss of enzymatic activity during the photocatalytic process is also taken into consideration [36]. At 70 min when no more viability was observed started the second stage of bacteria destruction – mineralization. Hydroxyl radicals attacked cell wall membranes and cause graduated oxidation of more complicated polymers such as liposaccharides (LPS), peptidoglycans, teichoic acids, proteins etc. Results presented in this work were only an initial stage on the way to complete bacteria cell mineralization. The time necessary for complete bacteria mineralization was much longer than for their inactivation. According to Jacoby et al. [65]

20

time needed for total mineralization of E. coli on TiO2-coated glass was about 75 hours. Therefore, further research will be undertaken in order to better understanding of the process. Conclusions New titania photocatalysts were prepared by D-fructose modification a low temperature. Carbon modification caused the enhancement of antibacterial activity and prepared photocatalysts were capable of total Escherichia coli and Staphylococcus epidermidis inactivation under UV-A and artificial solar light. The highest antibacterial properties presented TiO2-F-1%-100 containing 0.51 wt% of carbon. Obtained results indicate that the bacteria destruction process began from cell wall towards intracellular components. The two-stage photocatalytic mechanism of bacteria destruction by •OH radicals was proposed. Although bacterial mineralization needs much time obtained results suggested that photocatalytic process conducted with TiO2-F-1%-100 can be used in future water cleanup processes.

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oxidation,

Water

Res.

41

(4)

(2007)

842–852.

https://doi.org/10.1016/j.watres.2006.11.033

31

Fig. 1. XRD patterns of the tested samples.

32

Fig. 2. SEM images of tested photocatalysts: a) KRONOClean 7000, b) TiO2-100, c) TiO2-F1%-100, d) TiO2-F-5%-100, e) TiO2-F-10%-100.

33

Fig. 3. N2 adsorption-desorption isotherms for tested photocatalysts: a) KRONOClean 7000 and TiO2-100, b) fructose modified samples.

Fig. 4. FTIR/DR spectra of tested samples.

34

Fig. 5. UV-Vis/DR spectra of tested samples.

Fig. 6. The amount of generated 2-hydroxyterephthalic acid (fluorescence intensity) during 90 min of a) UV-A and b) ASL irradiation.

Fig. 7. Inactivation of a) E. coli and b) S. epidermidis in the presence of tested samples without radiation. 35

Fig. 8. Inactivation of E. coli in the presence of tested samples: a) under UV-A and b) under artificial solar light irradiation.

Fig. 9. Inactivation of S. epiderdmidis in the presence of tested samples: a) under UV-A and b) under artificial solar light irradiation.

36

Fig. 10. SEM images of bacteria: E. coli: a) before, b) after 75 min of and S. epidermidis: c) before, d) after 75 min in the presence of TiO2-F-1%-100 under ASL irradiation.

37

Fig. 11. Photocatalytic inactivation of 1.5 x 106 CFU/mL of bacteria under UV-A or ASL irradiation: a) E. coli (UV-A), b) E. coli (ASL), c) S. epidermidis (UV-A), d) S. epidermidis (ASL).

Figure 12. Fitting of the modified Hom kinetic model to experimental data of the photocatalytic inactivation of bacteria in suspension with tested photocatalysts under UV-A or

38

ASL irradiation: a) E. coli (UV-A), b) E. coli (ASL), c) S. epidermidis (UV-A), d) S. epidermidis (ASL).

Fig. 13. CO2 photocatalytic evolution during blank experiments performed with tested photocatalysts a) in the dark and under b) UV-A or c) ASL irradiation.

Fig. 14. CO2 photocatalytic evolution during a) E. coli and b) S. epidermidis cells decomposition in the dark in the presence of the tested sample.

39

Fig. 15. CO2 photocatalytic evolution during E. coli cells decomposition under a) UV-A and b) artificial solar light irradiation in the presence of the tested sample.

Fig. 16. CO2 photocatalytic evolution during S. epidermidis cells decomposition under a) UV-A and b) artificial solar light irradiation in the presence of the tested sample.

Fig. 17. Degradation efficiency of a) E. coli and b) S. epidermidis with TiO2-F-1%-100 photocatalyst in different recycle runs under ASL irradiation. 40

Fig. 18. Summary of the data for CO2 evolution, •OH radical formation and E. coli inactivation in experiments performed with TiO2-F-1%-100 under ASL irradiation.

Table 1. Physicochemical properties of studied photocatalysts. TiO2 crystalline phase Sample code

participation [%]

Crystallite size [nm]

Carbon content

Zeta potential

(wt%)

ζ [mV]

Anatase

Rutile

Anatase

Rutile

KRONOClean 7000

100

-

11.0

-

0.96

-17.71

TiO2-100

98.1

1.9

12.0

52.8

-

-24.13

TiO2-F-1%-100

97.6

2.4

11.4

29.1

0.51

-18.08

TiO2-F-5%-100

98.0

2.0

11.4

33.8

2.22

-21.52

TiO2-F-10%-100

97.6

2.4

11.2

33.8

4.16

-23.41

41

Table 2. Structural parameters of the studied photocatalysts. Sample code

SBET [m2/g]

Vtotal [cm3/g]

Vmicro [cm3/g]

Vmezo [cm3/g]

KRONOClean 7000

242

0.33

0.09

0.24

TiO2-100

266

0.46

0.09

0.37

TiO2-F-1%-100

267

0.42

0.09

0.33

TiO2-F-5%-100

242

0.41

0.09

0.32

TiO2-F-10%-100

222

0.37

0.08

0.29

Photocatalytic water disinfection under the artificial solar light by fructosemodified TiO2 Paulina Rokicka-Konieczna*, Agata Markowska-Szczupak, Ewelina Kusiak-Nejman, Antoni W. Morawski

42

West Pomeranian University of Technology, Szczecin, Faculty of Chemical Technology and Engineering, Institute of Inorganic Technology and Environment Engineering, Pułaskiego 10, 70-322 Szczecin, Poland



TiO2 was modified by hydrothermal method with fructose as a carbon source.



Antibacterial activity was enhanced both under UV-A and artificial solar light.



Antibacterial activity of fructose-modified TiO2 depends mainly on carbon content.



Modification increases the amount of surface -OH groups and the photocatalytic efficiency.



The two-stage photocatalytic mechanism of bacteria destruction by •OH radicals was found.

43