Treatment of Coliphage MS2 with Palladium-Modified Nitrogen-Doped

Jul 2, 2008 - Tao Yu , Wen-li Hu , Lixia Jia , Xin Tan , Juanru Huang , and Xiang ... Jingtao Zhang , Yang Liu , Qi Li , Xiaoping Zhang , and Jian Ku ...
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Environ. Sci. Technol. 2008, 42, 6148–6153

Treatment of Coliphage MS2 with Palladium-Modified Nitrogen-Doped Titanium Oxide Photocatalyst Illuminated by Visible Light Q I L I , †,§ M A R T I N A . P A G E , ‡,§ B E N I T O J . M A R I Ñ A S , ‡,§ A N D J I A N K U S H A N G * ,†,§ Department of Materials Science and Engineering, Department of Civil and Environmental Engineering, and Center of Advanced Materials for the Purification of Water with Systems; University of Illinois at Urbana-Champaign, Urbana, Illinois 61801

Received October 15, 2007. Revised manuscript received May 19, 2008. Accepted May 23, 2008.

A palladium-modified nitrogen-doped titanium oxide (TiON/ PdO) photocatalytic fiber was synthesized on a mesoporous activated carbon fiber template by a sol-gel process. Calcination of the coated fibers resulted in a macroporous interfiber structure and mesoporous photocatalyst coating. Atomic ratios of major photocatalyst constituents determined by X-ray photoelectron spectroscopy analyses were N/Ti ≈ 0.1 and Pd/ Ti ≈ 0.03. X-ray diffraction analyses revealed that the photocatalyst had an anatase structure and palladium additive was present as PdO. Triplicate batch experiments performed with MS2 phage (average initial concentration of 3 × 108 plaque forming units/mL) and TiON/PdO photocatalyst at a dose of 0.1 g/L under dark conditions revealed the occurrence of virus adsorption on the photocatalyst fibers at a rate that resulted in equilibrium within 1 h of contact time with corresponding virion removals of 95.4-96.7%. Subsequent illumination of the darkequilibrated samples with visible light (wavelengths greater than 400 nm and average intensity of 40 mW/cm2) resulted in additional virus removal of 94.5-98.2% within 1 h of additional contact time. By combining adsorption and visible-light photocatalysis, TiON/PdO fibers reached final virus removal rates of 99.75-99.94%. Spin trapping electron paramagnetic resonance (EPR) measurements confirmed the production of •OH radicals by TiON/PdO under visible light illumination, which provided indirect evidence about MS2 phage being potentially inactivated.

Introduction Pathogens continue to be the water contaminants with greatest detrimental impact on global human health, especially in developing countries. Drinking water quality control strategies in both developing and developed countries give higher priority to preventing waterborne disease outbreaks associated with pathogens compared to controlling associated long-term exposure to chemical disinfection byproduct * Corresponding author e-mail: [email protected]. † Department of Materials Science and Engineering. § Center of Advanced Materials for the Purification of Water with Systems. ‡ Department of Civil and Environmental Engineering. 6148

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(1). Thus, traditional water disinfection processes rely heavily on chemical disinfectants such as free chlorine, the most widely used drinking water disinfectant worldwide, despite the production of toxic disinfection byproduct (DBPs) resulting from reactions of free chlorine with disinfection byproduct precursors (DBPPs) present in both pristine and contaminated source waters. While emerging technologies such as ultraviolet (UV) light and microfiltration (MF) processes can be effective to control pathogens such as protozoan (oo)cysts without forming hazardous DBPs, these processes are generally less effective in controlling viral pathogens. There is a need for innovative processes that are more effective against the whole spectrum of waterborne pathogens, including viruses, before the industry can move away from the use of chemical oxidants, like free chlorine, for primary disinfection. The idea of enhancing or supplementing current disinfection processes through the use of photocatalytic materials offers one potential solution that beckons further research. Since the discovery of photoelectrochemical splitting of water on n-TiO2 electrodes by Fujishima and Honda (2) in 1972, semiconductor-based materials have been investigated extensively as photocatalysts on environmental control applications (1, 3–20) in the past several decades. In this process, highly reactive •OH radicals are produced to oxidize organic pollutants, disinfect microorganisms, and degrade hazardous DBPs and DBPPs. In these previous studies, TiO2 was used as the photocatalyst, but its photocatalytic capability requires activation by ultraviolet (UV) light (λ >400 nm), seriously limiting its solar efficiency (7). Since Asahi et al. (21) reported that nitrogen doping of n-TiO2 (TiON) extended the optical absorbance of TiO2 into the visible-light region, anionic nonmetal dopants, such as nitrogen (21, 29), carbon (30–38), sulfur (39, 44), or fluorine (45), have been explored for visible-light photocatalysis with improved stability, photocatalytic efficiency, and ease of the doping process (46, 47). Visible-light-induced photocatalysis allows the main part of the solar spectrum to be used to provide photocatalytic capability and therefore can highly increase the photocatalytic efficiency under sun light illumination and reduce the cost by eliminating the need for a UV light source. However, until now, only a few reports had been made on the bactericidal effect of anion-doped TiO2, which demonstrated the successful inactivation of model gram-positive Micrococcus lylae (44) and model gramnegative E. coli (48) under visible light illumination. To date, no photocatalytic inactivation of viruses under visible light illumination has been reported. In our recent work (49), we had developed a palladiummodified nitrogen-doped titanium oxide (TiON/PdO) nanoparticle photocatalyst by a sol-gel process, which demonstrated a superior photocatalytic activity to TiON when the Pd/Ti atomic ratio was 0.5%. In the present study, we combined the sol-gel process with a template technique to create a novel TiON/PdO photocatalytic fiber. The immobilization of photocatalytic TiON/PdO onto the fiber template removes the need of recycling photocatalysts in the powder form from aqueous environment. For the first time, a high degree of photocatalytic virus removal under visible light illumination was observed on this TiON/PdO photocatalytic fiber. With further development and investigation, this technology may offer a potentially DBP-free alternative for the primary control of viral pathogens in environmental applications. 10.1021/es7026086 CCC: $40.75

 2008 American Chemical Society

Published on Web 07/02/2008

FIGURE 2. X-ray diffraction patterns of TiON/PdO photocatalytic fiber.

FIGURE 1. XPS survey spectrum (a), and multiplex high-resolution scan over N 1s (b) and Pd 3d (c) spectral regions associated with TiON/PdO photocatalytic fiber, respectively.

Experimental Section Chemicals and Materials. Titanium tetraisopropoxide (TTIP, 97%, Sigma-Aldrich, St. Louis, MO), tetramethylammonium hydroxide (TMA, 25 wt% in methanol, Sigma-Aldrich, St. Louis, MO), and palladium acetylacetonate (Pd(acac)2, 99%, Sigma-Aldrich, St. Louis, MO) were used in this study as sources of titanium, nitrogen, and palladium, respectively. Ethyl alcohol (EtOH, 100%, AAPER Alcohol and Chemical Co., Shelbyville, KY) and dichloromethane (CH2Cl2, 99.6%, Sigma-Aldrich, St. Louis, MO) were used as solvents. Activated carbon glass fibers (ACGF), prepared in a nonwoven fabric form by a thermal activation process (50), were used as templates. Coliphage MS2, a nonpathogenic virus widely used as a model system for immunological studies, drug delivery, and gene delivery studies (51–54), was used for the virus

FIGURE 3. Low magnification (a), and high magnification (b) SEM images of TiON/PdO photocatalytic fiber, respectively. control assessment portion of this study. MS2 phase is an icosahedral-shaped virus with a diameter at ∼27.5 nm, and a well-characterized molecular structure (55, 56). TiON/PdO Fiber Fabrication. The TiON/PdO precursor solution was prepared at room temperature by the following sol-gel process. First, TMA was dissolved in EtOH at a mol ratio at 1:10. The solution was stirred magnetically for 5 min, and then TTIP was added into the solution at a TMA:TTIP molar ratio of 1:5. A proper amount of Pd(acac)2 was dissolved in CH2Cl2, and then added into the TMA/TTIP/EtOH mixture to achieve a target Pd:Ti molar ratio at 0.5%. After stirring for 5 min, a homogeneous TiON/PdO precursor solution was VOL. 42, NO. 16, 2008 / ENVIRONMENTAL SCIENCE & TECHNOLOGY

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TABLE 1. Results Obtained from Triplicate Experiments Performed to Assess the Inactivation Kinetics of MS2 Phage by Sequential Exposure to TiON/PdO fibers (0.1 g/L as photocatalyst) under Dark Followed by Visible Light (λ >400 nm) (light Turned on Immediately after Collection of Last Dark Sample), and a Control Experiment under Visible Light in the Absence of TiON/PdO Performed Otherwise under the Same Conditions (I = 40 mW/cm2, 1 mM Carbonate Buffer, pH 8.1-8.2, 23-26°C) light w/o TiON/PdO time (min)

0 30 60 120

Nt

1.90 × 108 1.62 × 108 1.47 × 108 1.37 × 108

TiON/PdO test 1 time (min)

Nt

0 1 10 60

5.00 × 108 1.48 × 108 5.70 × 107 2.30 × 107

1 2 5 10 30 60

1.80 × 107 1.50 × 107 1.00 × 107 2.87 × 106 1.40 × 106 1.27 × 106

obtained. The ACGF template was then soaked in the solution for 24 h. Upon removal from the precursor solution, the soaked template was quickly washed in EtOH before it was exposed to humidified ambient air to induce the hydrolysis of precursors. After further hydrolysis and drying, the template was calcinated in air at 450 °C for 3 h to produce fine crystallites of TiON/PdO on the fiber surface. Photocatalyst Characterization. The crystal structure of TiON/PdO fiber was analyzed by X-ray diffraction (XRD) using a Rigaku D-Max X-ray powder diffractometer (Rigaku Corporation, Tokyo, Japan) with Ni-filtered Cu ΚR (0.15418 nm) radiation at 45 kV and 20 mA. X-ray photoelectron spectroscopy (XPS) measurements were made using a Physical Electronics PHI 5400 X-ray photoelectron spectrometer (Perkin-Elmer Corporation, Eden Prairie, MN) with a Mg K anode (1253.6 eV photon energy, 15 kV, 300 W) at a takeoff angle of 45°. Multiplex XPS spectra of N 1s, O 1s, Ti 2p, and Pd 3d were recorded using band-pass energy of 35.75 eV and corresponding energy resolution of 1.2 eV. Atomic concentrations of these elements were obtained by comparing the peak areas of their spectra. The morphology of the fiber was examined by scanning electron microscopy (SEM) with a Hitachi S-4700 scanning electron microscope (Hitachi Ltd., Tokyo, Japan). Prior to imaging, the sample was sputtered with gold for 15 s using an Emitech K575 Sputter Coater (Emitech Ltd., Ashford Kent, UK). Virus Propagation and Viability Assessment. Coliphage MS2 (ATCC 15597-B1) and its bacterial host E. coli (ATCC 15597) were obtained from the American type culture collection (Manassas, VA). E. coli cells were grown and maintained using slants and Tryptic Soy Broth suspensions, and stored at 4 °C. Virus stocks were grown in E. coli suspensions and purified by sequential centrifugation, microfiltration (MF) and ultrafiltration (UF). Cell debris were removed by centrifugation at 230g, and the resulting supernatant was passed through a polyvinylidene fluoride (PVDF) MF membrane with nominal pore size of 0.45 µm. The resulting filtrate and a 1 mM phosphate buffer solution (PBS) volume approximately 1000 times that of the filtrate were passed through a PVDF ultrafiltration (UF) membrane with nominal molecular-weight cutoff of 30 kDa (HFM-100; Koch Membrane Systems, Wilmington, MA). The final concentrate retained by the UF membrane was diluted in 1 mM PBS to a final concentration of 1011 plaque-formingunits (pfu/mL). Viability was assessed by plaque assay with the soft agar overlay method to determine MS2 phage concentration (57). Photocatalytic Removal of Coliphage MS2. Photocatalytic 6150

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TiON/PdO test 2

TiON/PdO test 3

time (min)

Nt

time (min)

Nt

0 1 10 30 60

2.43 × 108 9.50 × 107 6.10 × 107 1.30 × 107 8.00 × 106

0 10 45 80

1.80 × 108 3.80 × 107 1.15 × 107 8.10 × 106

1 2 5 10 30 60

6.00 × 106 3.43 × 106 1.94 × 106 1.46 × 106 4.00 × 105 1.45 × 105

1 2 5 20 60 90

7.60 × 106 3.70 × 106 2.80 × 106 6.80 × 105 1.50 × 105 1.90 × 105

dark

light

experiments were conducted in a 50 mL, batch reactor placed under a collimated beam from a 1000 W xenon-arc lamp (Newport, Stratford, CT). The light source was equipped with a liquid filter (H2O), a long pass (λ 400 nm) filter, and a neutral density filter (10% T). The average intensity at the surface of the suspension was I ) 40 mW/cm2, measured using a radiant power meter (Newport, Irvine, CA). Temperature and pH, measured before and after each experiment, were within the ranges of 23-26 °C and 8.1-8.2, respectively. Mixing was achieved by magnetic stirring with minimal vortex formation, and it was done carefully to avoid contact between the magnetic stirrer and the TiON/PdO fiber sample. In a dark room, TiON/PdO fibers were preconditioned by washing in distilled, deionized (DDI) water. After preconditioning, they were immersed into 1 mM carbonate buffer solution (CBS) in the reactor and stirred in the dark for at least 3 h. Triplicate dark control experiments were performed prior to the photocatalysis experiment to assess the adsorption taking place prior to photocatalysis, allowing better resolution of the photocatalysis phenomenon itself. The dark control experiments were performed by adding a predetermined volume of MS2 phage stock into this reactor to obtain an initial MS2 phage suspension concentration of (3 ( 2) × 108 plaque forming units (pfu)/mL, and a photocatalyst mass (as TiON/PdO) concentration of 0.1 g/L. Sample volumes of 1 mL were withdrawn at various contact times (up to 60-80 min) and quenched in 0.1% sodium thiosulfate solution prior to viability measurement. Upon completion of the dark control experiments, the reactors were uncovered and placed in the collimated beam apparatus to assess the photocatalytic disinfection effect. Again, samples were withdrawn at increasing time intervals (up to 60-90 min) and processed as described for the dark control. A light-only experiment without photocatalyst addition was also conducted as control test. Spin Trapping EPR Measurements. Spin trapping electron paramagnetic resonance (EPR) measurements were conducted to verify the formation of reactive radicals by TiON/PdO photocatalytic powders both under visible light illumination and in the dark. The spin trapping chemical used in this study was R-(4-pyridyl N-oxide)-N-tert-butylnitrone (POBN, 99%, Sigma-Aldrich, St. Louis, MO). Prior to the measurements with TiON/PdO, a Fenton reaction was first conducted for comparison and calibration of the instrumentation. TiON/PdO powders were dispersed in double deionized water inside Petri dishes before adding the electron trapping chemicals. A stock solution containing 100 mM POBN and 95% ethanol was added into the TiON/PdO

FIGURE 4. Survival ratios of MS2 virus vs treatment time with only visible light (>400 nm) illumination ((), TiON/PdO photocatalytic fiber in dark environment (O∆∇), and TiON/PdO photocatalytic fiber under visible light (>400 nm) illumination after corresponding dark control (b21). The MS2 virus suspension had an initial concentration of (3 ( 2) × 108 pfu/ml, and the photocatalyst dose was at 0.1 g/L as TiON/PdO. The solution was 1 mM carbonate buffer (pH 8.1-8.2, 23-26 °C).

FIGURE 5. EPR spectra of TiON/PdO samples tested with POBN under different experimental conditions. dispersion to reach a final concentration of POBN at 10 mM and ethanol at 170 mM. EPR spectra were collected on a Eline Century Series EPR spectrometer (Varian E-109-12, Varian, Inc., Palo Alto, CA) working in the X-band mode at 9.51 GHz, center field 3390 G, and 10.00 dB power.

Results and Discussion Composition of TiON/PdO Fiber. XPS investigation was first conducted to determine the composition of the fiber sample. Figure 1a shows the representative XPS survey spectrum, which confirms the presence of Ti, O, N, and Pd in the fiber sample. A C 1s peak was also observed in the XPS survey spectrum. Multiplex high-resolution scans over Ti 2p, O 1s, N 1s, and Pd 3d spectral regions were conducted to determine the relative element composition ratio. Figure 1b demonstrates the XPS high-resolution scan over N 1s. N 1s has the peak position at ∼397 eV, which suggests that some O atoms were substituted by N atoms in the fiber sample. The N/Ti atomic ratio was determined to be ∼0.1. In a previous study, the surface and inner XPS ratios of sol-gel TiON were found to be very similar (57). Figure 1c presents the XPS highresolution scan over Pd 3d. It shows that the binding energy of Pd 3d5/2 is ∼336.20 eV, which can be attributed to PdO species. For this reason, the fiber sample has been referred to as TiON/PdO fiber. The Pd/Ti atomic ratio was determined

to be ∼0.03, which was approximately six times that in the sol-gel precursor solution. As demonstrated in our previous work (49), PdO stays outside of the TiON lattice in the sol-gel TiON/PdO nanoparticles and tends to remain on the surface. As a surface characterization technique, XPS can only determine the surface composition ratio within a very shallow depth, which would provide a higher Pd/Ti atomic ratio than that in the precursor solution. Crystal Structure of TiON/PdO Fiber. Figure 2 shows the X-ray diffraction (XRD) pattern of our TiON/PdO fiber sample, which can be assigned to an anatase structure without rutile phase. A very weak peak corresponding to PdO (101) was observed in the XRD pattern, which suggests that Pd additive exists as PdO at a very small quantity and is not incorporated into the anatase structure. This observation is in accordance with the present XPS result and the previous work on TiON/ PdO nanoparticles (49). Morphology of TiON/PdO Fiber. Figure 3 shows SEM images of the TiON/PdO fibers under different magnifications. At the low magnification (Figure 3a), a nonwoven fiber network is observed, which reflects the ACGF template structure. On the individual glass fiber, a thin layer of TiON/ PdO photocatalyst was immobilized. High magnification SEM image of the TiON/PdO fiber surface (Figure 3b) shows that the TiON/PdO photocatalytic layer has a mesoporous structure, and the average particle size is several nanometers. Thus, the TiON/PdO fiber network has a combination of macroporous (from ACGF template matrix) and mesoporous (from coated photocatalytic layer) structures. This dual porous structure is beneficial for achieving relatively high disinfection efficiency because it provides access to the entire photocatalyst contact area for virions and other contaminants present in water. We could not observe individual PdO nanoparticles on the fiber surface because of the low palladium additive concentration. Photocatalytic Removal of Coliphage MS2. The TiON/ PdO fibers reduced the concentration of viable MS2 phage in synthetic carbonate buffer solution. The absolute (Nt) and normalized (Nt/N0) concentrations of viable viruses as a function of exposure time are presented in Table 1 and Figure 4, respectively. Prior to experiments with the photocatalyst fibers, a light-only control was performed to demonstrate that visible light by itself had little effect on virus viability over the time course of the experiments. Characterizing the photocatalytic effect imparted by the TiON/PdO fibers required prior assessment of virus removal by the fibers in the absence of light. To clearly distinguish the removal due only to the photocatalytic effect, the viruses were first equilibrated with the TiON/PdO fibers in the dark (Figure 4, open symbols). Under these conditions, a 95.4-96.7% reduction in viable virus concentration in the bulk solution was observed. The rate of virus removal decreased over time until reaching equilibrium in approximately one hour. Following dark equilibration, the same reactor was exposed to visible light to determine the additional removal induced by irradiating the material. No additional viruses were added prior to light exposure. Therefore, the initial virus concentration in the bulk solution was approximately 5% of that prior to the dark control. A clear enhancement in the virus removal rate was observed upon irradiation. However, as in the dark control, the rate of virus removal decreased with time, yielding final additional removals ranging from 94.5-98.2%. The tailing phenomenon is currently under investigation and is important in understanding the photocatalytic mechanism. •OH Radical Formation. To verify the formation of •OH radicals by TiON/PdO under visible light illumination, spin trapping EPR measurements were conducted on TiON/PdO sol-gel powders both under visible light illumination and in VOL. 42, NO. 16, 2008 / ENVIRONMENTAL SCIENCE & TECHNOLOGY

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the dark. Figure 5 presents the EPR spectra of TiON/PdO samples in interaction with POBN under different experimental conditions. In the dark environment, no POBN-•OH adduct signals were observed, thus supporting that the observed MS2 removal in the dark could be attributed to the adsorption of MS2 onto the dual porous fiber structure. In contrast, characteristic triple-peak POBN-•OH adduct signals were observed under visible light illumination, which revealed that •OH radicals were produced by TiON/PdO under visible light illumination. The intensity of POBN-•OH adduct signals increased with increasing illumination time, revealing the continuous production of •OH radicals. The •OH radicals are known to react unselectively with most constituents present in aqueous solution including the various chemical constituents of viruses thus providing indirect evidence for MS2 inactivation upon visible light illumination. Thus, the tailing phenomenon observed may have been due to fouling of the photoactive sites by removed virions, which would prevent other viruses from reaching the surface and reacting with surface radicals or electronholes. In our previous study, palladium additive demonstrated efficacy as a charge trapping center to trap electrons in TiON/ PdO photocatalytic material system under the proper additive concentration, which will significantly decrease the recombination of electron and hole pairs and improve the photocatalytic efficiency under visible light illumination (49). The results of this study indicate that TiON/PdO can remove viruses from water under dark conditions and that illuminating this material enhances the extent of virus removal. With further development, it is hoped that this novel material could be applied in a heterogeneous disinfection approach to selectively remove viruses from the bulk solution and inactivate them in a confined space on the surface. Such an approach might yield fewer disinfection byproducts than traditional approaches in which chemical oxidants react homogeneously within the bulk solution. If photochemical reactions on the surface would inactivate the viruses after sorption and return them to the bulk phase, in situ regeneration may be possible. However, further research is needed to develop such a system. Future efforts will focus on elucidating the regeneration potential of the material, enhancing photochemical reactions on its surface, characterizing its performance in natural waters, elucidating its selectivity for viruses, determining the true fate of the viruses, and elucidating the cause(s) of the tailing phenomenon observed in this study. Reactor design will also be an important aspect to consider. Because the rate of the virus removal observed under illumination was comparable to that observed for the dark control, the photocatalyzed removal mechanism might be mass transfer limited. If so, the virus removal rate could be increased with appropriate improvements in reactor configuration, such as passing the solution through an irradiated network of fibers.

Acknowledgments We thank Prof. J. Economy in the Department of Materials Science and Engineering, University of Illinois at UrbanaChampaign for providing the ACGF template, and Prof. Mark J. Nilges in the Illinois EPR Research Center, University of Illinois at Urbana-Champaign, for assistance on EPR measurements. Support for this study was provided by the Center of Advanced Materials for the Purification of Water with Systems (WaterCAMPWS), under National Science Foundation Project Agreement Number CTS-0120978. XPS, XRD, and SEM measurements were carried out at the Frederick Seitz Materials Research Laboratory, University of Illinois at Urbana-Champaign, which is partially supported by the U.S. Department of Energy under grant DEFG02-91ER45439. 6152

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