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Selective Inactivation of Bacteriophage in the Presence of Bacteria by Use of Ground Rh-Doped SrTiO3 Photocatalyst and Visible Light Yuichi Yamaguchi,†,‡ Sho Usuki,†,§ Yoshihiro Kanai,∥ Kenji Yamatoya,§ Norihiro Suzuki,† Ken-ichi Katsumata,† Chiaki Terashima,† Tomonori Suzuki,†,§ Akira Fujishima,† Hideki Sakai,†,‡ Akihiko Kudo,†,⊥ and Kazuya Nakata*,†,§ †

Photocatalysis International Research Center, Research Institute for Science and Technology, ‡Department of Pure and Applied Chemistry, Faculty of Science and Technology, §Department of Applied Biological Science, Faculty of Science and Technology, and ∥ Research Institute for Science and Technology, Tokyo University of Science, 2641 Yamazaki, Noda, Chiba 278-0022, Japan ⊥ Department of Applied Chemistry, Faculty of Science, Tokyo University of Science, 1-3 Kagurazaka, Shinjuku-ku, Tokyo 162-8601, Japan S Supporting Information *

ABSTRACT: Bacteriophage (denoted as phage) infection in the bacterial fermentation industry is a major problem, leading to the loss of fermented products such as alcohol and lactic acid. Currently, the prevention of phage infection is limited to biological approaches, which are difficult to apply in an industrial setting. Herein, we report an alternative chemical approach using ground Rh-doped SrTiO3 (denoted as g-STO:Rh) as a visible-light-driven photocatalyst. The g-STO:Rh showed selective inactivation of phage without bactericidal activity when irradiated with visible light (λ > 440 nm). After inactivation, the color of g-STO:Rh changed from gray to purple, suggesting that the Rh valence state partially changed from 3+ to 4+ induced by photocatalysis, as confirmed by diffuse reflectance spectroscopy. To study the effect of the Rh4+ ion on phage inactivation under visible-light irradiation, the survival rate of phage for gSTO:Rh was compared to that for ground Rh,Sb-codoped SrTiO3 (denoted as g-STO:Rh,Sb), where the change of Rh valence state from 3+ to 4+ is almost suppressed under visible-light irradiation due to charge compensation by the Sb5+ ion. Only gSTO:Rh effectively inactivated phage, which indicated that Rh4+ ion induced by photocatalysis particularly contributed to phage inactivation under visible-light irradiation. These results suggested that g-STO:Rh has potential as an antiphage material in bacterial fermentation. KEYWORDS: visible-light-driven photocatalyst, bacteriophage inactivation, ground Rh-doped SrTiO3, ball milling, Rh4+ ion

1. INTRODUCTION

Recently, as an alternative strategy, photocatalysis has gained much attention; this process uses materials that exhibit oxidative degradation for organic substances and inactivation of pathogens under light irradiation.22−24 TiO2 is widely used as an environmental purification material that shows high photocatalytic performance, which has been applied in air and water purification.25 The antibacterial performance of TiO2 has been well investigated in the literature so far.26−28 On the other hand, fewer studies have been documented the antiviral and antiphage activity of TiO2 compared to antibacterial performance.29−33 As methioned, TiO2 shows high photocatalytic performance, but it responds only to UV light, because of its wide gap.34 Since DNA and RNA of phage and bacteria are seriously

Probiotic organisms are essential for human life and are regularly employed in the fermentation industry, such as in the production of alcohol, lactic acid, and medicines.1−13 However, the dairy industry has faced increasing bacteriophage (denoted as phage) problems, notably phage infection, leading to losses of fermented products.1,2,14−18 Therefore, the development of facile and safe technologies that inactivate phage without damaging probiotic organisms is essential for the fermentation industry. To date, studies on addressing phage infection have employed microbiological approaches. Although genetically modified antiphage systems have been employed successfully,2,10,14,15 the practical application of such biological approaches is difficult because of the complex processes involved. Antiphage technology employing a physical approach (sonication) has been developed.19 However, it is also destructive to bacteria,20,21 making it difficult to inactivate phage selectively in the presence of bacteria. © XXXX American Chemical Society

Received: June 1, 2017 Accepted: August 30, 2017

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DOI: 10.1021/acsami.7b07786 ACS Appl. Mater. Interfaces XXXX, XXX, XXX−XXX

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ACS Applied Materials & Interfaces

(1.00 − 2a):a:a. The sample is denoted as g-STO:Rh(y%),Sb(y%), where y refers to the Rh and Sb doping percentages. 2.2. Characterization. Crystal structures of the prepared photocatalysts were determined by X-ray diffraction (Rigaku Ultima IV) using Cu Kα radiation. Diffuse reflectance spectra were obtained on a UV−visible spectrometer (Jasco V-670); reflection data were converted into absorbance values by the Kubelka−Munk formula. Nitrogen adsorption and desorption isotherms were measured at 77 K on a gas adsorption and desorption analyzer (MicrotracBEL Belsorpmax). Specific surface areas were determined by the Brunauer− Emmett−Teller method. 2.3. Photocatalytic Antiphage and Antibacterial Performance. Bacteriophage Qβ (NBRC20012) and Escherichia coli (IAM12119T) were used in our experiment as phage and bacteria, respectively. Qβ is easier to utilize in experimental systems than other phages because Qβ is quite simple and is the smallest of the known phages; it has capsids with T = 3 icosahedral morphology without an envelope.53 It is one of the best-studied bacteriophages, and extensive genetic and biochemical studies have been performed so far.53 Furthermore, Qβ is often used for evaluation of antiphage performance with photocatalysis.54 Therefore, we determined to use bacteriophage Qβ in our experiment. Phage was incubated in soft agar medium containing bacteria at 37 °C for 16 h, whereas bacteria were incubated in nutrient broth liquid medium at 37 °C for 16 h. The culture was centrifuged at 1100g for 10 min, followed by washing with sterile physiological saline solution (pH 7). After washing, the resulting pellet was resuspended in saline. For phage, the concentration was determined by testing infection of bacteria by the double-agar-layer plaque assay.55 The concentration of the phage suspension then was adjusted to 5.0 × 107 plaque-forming units (pfu)/mL with sterilized water. For bacteria, the suspension was adjusted to a concentration of 5.0 × 107 colony-forming units (cfu)/mL with sterilized water. The photocatalytic inactivation of phage and bacteria was tested as follows. In the case of phage, a photocatalyst (150 mg) was added to sterilized water (50 mL) and sonicated for 5 min, and then the solution of phage (5.0 × 107 pfu/mL) was added. For bacteria, a photocatalyst (150 mg) was added to sterilized water (45 mL) and sonicated for 5 min, and then the solution of bacteria (5.0 × 107 cfu/ mL) was added. The photocatalyst−phage or photocatalyst−bacteria suspensions were then irradiated at 110 mW/cm2 light intensity by a Xe lamp equipped with a Y-44 cutoff filter (λ < 440 nm). After irradiation, serial dilutions of the phage were mixed with bacteria and plated in a double-agar-layer plaque assay, while serial dilutions of the bacterial suspension were plated to nutrient agar. The resulting plates were cultivated at 37 °C for 1 day. The survival rate of phage and bacteria was determined by counting the plaques and colonies formed, respectively. Survival rate of pathogens in a mixed suspension of phage and bacteria was also examined as follows: photocatalyst (150 mg) was added to sterilized water (45 mL) and sonicated for 5 min, and then the solutions of phage and bacteria were added. The concentrations of phage and bacteria were adjusted to 5.0 × 107 pfu/mL and 5.0 × 107 cfu/mL, respectively. For reference, 5 mg of a TiO2 photocatalyst (Aeroxide P-25, Evonik) was used for testing inactivation of phage or bacteria in suspensions (50 mL) under UV light irradiation (0.12 mW/ cm2). All of the inactivation experiments were repeated three times. Statistical analysis (error bar, standard deviation, averaged values, and log scale expression) was carried out in our study by use of Microsoft Excel. 2.4. Detection of •OH Produced by Photocatalyst. gSTO:Rh(1%) (25 mg) was dispersed in 10 parts per million (ppm) dimethyl sulfoxide (DMSO) aqueous solution (30 mL) and sonicated for 5 min. The suspension was irradiated at 110 mW/cm2 by a Xe lamp equipped with a Y-44 cutoff filter (λ < 440 nm) for 24 h. Methanesulfinic acid and methanesulfonic acid produced by photocatalytic oxidative decomposition of DMSO were detected by an ion chromatograph equipped with a conductivity detector (Shimadzu CDD-10A VP) and a column (Shimadzu Shim-pack IC-SA2) at 303 K. The mobile phase was a mixed solvent of 0.14% sodium hydrogen carbonate and 0.19% sodium carbonate aqueous solution at 1.0 mL/ min.

damaged under UV-light irradiation,35,36 it is difficult to achieve selective inactivation of phage. Therefore, photocatalysis using materials that respond to UV light is of limited use in the fermentation industry.30,37−39 Thus, a new technology that uses a visible-light-responsive photocatalyst is requested, because light of these wavelengths is of lower energy and hence less destructive to the probiotic bacteria whose viability is essential to fermentation. In recent years, Rh-doped SrTiO3 (denoted as STO:Rh) has gained attention as a visible-light-driven photocatalyst.40−46 Although pristine SrTiO3 does not exhibit photocatalytic activity under visible-light irradiation because of a wide band gap of 3.2 eV, Rh doping permits visible-light-responsive photocatalysis by generating impurity levels in the forbidden band of the semiconductor without shifting the conductionband level.47−51 Substituting a small amount of Rh atoms into the Ti sites of SrTiO3 stabilizes the valence state of Rh to 4+. In the photocatalytic reaction, the Rh valence state in the STO:Rh photocatalyst reversibly changes from 4+ to 3+ under visible irradiation in the presence of an electron donor such as methanol, and the Rh3+ ion allows efficient H2 evolution. Thus, the Rh valence state in STO:Rh is a key factor to photocatalysis.40,42 Another important factor in photocatalysis is large surface area, since contact between the target substances and the photocatalyst is required for reaction. We previously demonstrated that ball-milled (ground) visible-light-driven STO:Rh photocatalyst (denoted as g-STO:Rh) can be employed for environmental remediation, specifically for the degradation of volatile organic compounds upon irradiation with visible light,52 whereas STO:Rh shows negligible photocatalytic performance owing to smaller surface area. Ball milling thus is a suitable method for preparation of materials with enhanced photocatalytic performance. Herein, we present a chemical approach using g-STO:Rh photocatalyst to selectively inactivate phage without significant decrease of bacterial numbers. The antiphage and antibacterial activities under visible-light irradiation were examined by inactivation for phage and bacteria in the context of the Rh valence state of photocatalysts.

2. EXPERIMENTAL SECTION 2.1. Materials. STO:Rh was synthesized by a solid-state reaction according to a previous report.40 The starting materials SrCO3 (99.9%, Kanto Chemical Co., Inc.), TiO2 (99.9%, Soekawa Chemical), and Rh2O3 (95%, Wako Pure Chemical) were mixed at the required ratios to achieve the composition of Sr:Ti:Rh = 1.07:(1.00 − a):a in an aluminum crucible with the addition of a small amount of methanol. The resulting powder was calcined in air at 900 °C for 1 h and then at 1100 °C for 10 h. STO:Rh was obtained after cooling to room temperature. The sample is denoted as STO:Rh(x%), where x refers to the Rh doping percentage. Aliquots (1.0 g) of STO:Rh powder were transferred to 45 mL containers containing ultrapure water (5.0 mL) and zirconia balls (10.0 g; diameter = 1.0 mm). The powder was milled twice at 800 rpm for 30 min in a ball-milling device (Fritsch Pulverisette 7). Finally, the ground particles were collected by filtration, washed with ultrapure water, and dried at 60 °C for 24 h. The sample is denoted as gSTO:Rh(x%). Ground SrTiO3 codoped with Rh and Sb was synthesized with a modified procedure. Starting materials SrCO3 (99.9%, Kanto Chemical Co., Inc.), TiO2 (99.9%, Soekawa Chemical), Rh2O3 (95%, Wako Pure Chemical), and Sb2O3 (98%, Nacali Tesque Inc.) were used at the required ratios to achieve the composition of Sr/Ti/Rh/Sb = 1.07: B


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ACS Applied Materials & Interfaces 2.5. Detection of H2 with Photocatalyst in Bacterial Suspension under Visible-Light Irradiation. g-STO:Rh(1%) (60 mg) was dispersed in a bacterial suspension (30 mL) adjusted to 5.0 × 107 cfu/mL and sonicated for 5 min. The suspension was irradiated for 24 h at 110 mW/cm2 by a Xe lamp equipped with a Y-44 cutoff filter (λ < 440 nm). A gas chromatograph equipped with a thermal conductivity detector and a column (Shimadzu molecular sieve 13×) at 313 K was used for detection of H2. Argon was used as a carrier gas at 1.0 mL/min.

3. RESULTS AND DISCUSSION 3.1. Photocatalytic Antiphage and Antibacterial Performance with STO:Rh. Inactivation rates of phage in the presence of STO:Rh(1%) and g-STO:Rh(1%) in aqueous suspension under dark conditions and visible-light irradiation are shown in Figure 1. No significant decrease in survival rate of

Figure 2. Survival rate of phage in the presence of g-STO:Rh(0.5%, 1%, or 2%) photocatalysts with various Rh doping amounts in aqueous suspension under dark conditions and visible-light irradiation (110 mW/cm2, λ > 440 nm). Photocatalyst, 0.15 g; light source, 200 W xenon lamp with a Y-44 cutoff filter; volume, 50 mL; initial concentration of phage, 5.0 × 107 pfu/mL.

amount enhanced visible-light absorption (Figure S1) while concurrently providing more recombination centers between the excited electron and holes, thereby leading to reduced photocatalytic activities. Next, bacterial inactivation in the presence of STO:Rh(1%) and g-STO:Rh(1%) in aqueous suspension under dark conditions and visible-light irradiation were investigated, as shown in Figure 3. As with phage, no significant decrease in Figure 1. Survival rate of phage in the presence of STO:Rh(1%) and g-STO:Rh(1%) photocatalysts in aqueous suspension under dark conditions and visible-light irradiation (110 mW/cm2, λ > 440 nm). Photocatalyst, 0.15 g; light source, 200 W xenon lamp with a Y-44 cutoff filter; volume, 50 mL; initial concentration of phage, 5.0 × 107 pfu/mL.

phage was obtained without photocatalysts under visible-light irradiation or with photocatalyst under dark conditions, indicating that neither light illumination nor photocatalyst particles alone was sufficient to inactivate phage. In addition, STO:Rh(1%) caused negligible inactivation even under visiblelight irradiation, suggesting that STO:Rh(1%) photocatalyst is ineffective for inactivation of phage under visible-light illumination. In contrast, ∼5-log reduction in survival rate of phage was observed with g-STO:Rh(1%) after 4 h of irradiation. This improved inactivation for phage was attributed to the larger surface area of g-STO:Rh(1%) compared with that of STO:Rh(1%). These results were consistent with those discussed in the Introduction regarding the superior photocatalytic performance of g-STO:Rh(1%) to STO:Rh(1%) for the decomposition of volatile organic compounds under visiblelight irradiation. Large contact area between the target substance and the photocatalyst surface is important for facilitating photocatalytic activity. The optimal Rh doping of g-STO:Rh for inactivation of phage was evaluated, as shown in Figure 2. The survival rate of phage decreased slightly in the presence of g-STO:Rh(0.5%) and g-STO:Rh(2%), although, as mentioned, ∼5-log reduction in survival rate of phage was observed with g-STO:Rh(1%) after 4 h of irradiation. In photocatalytic H2 evolution, the best performance was also obtained with STO:Rh(1%).40 Thus, the optimal Rh doping amounts for inactivation of phage showed a trend similar to that for H2 evolution. Increasing the doping

Figure 3. Survival rate of bacteria in the presence of STO:Rh(1%) and g-STO:Rh(1%) photocatalysts in aqueous suspension under dark conditions and visible-light irradiation (110 mW/cm2, λ > 440 nm). Photocatalyst, 0.15 g; light source, 200 W xenon lamp with a Y-44 cutoff filter; volume, 50 mL; initial concentration of bacteria, 5.0 × 107 cfu/mL.

survival rate of bacteria was observed without photocatalyst under visible-light irradiation or with photocatalyst under dark conditions, indicating that neither light illumination nor photocatalyst particles alone was sufficient to cause bacterial sterilization. Additionally, STO:Rh(1%) caused no significant decrease in survival rate of bacteria even under visible-light irradiation, suggesting that STO:Rh(1%) photocatalyst is almost ineffective for bacterial sterilization under visible-light illumination. Interestingly, bacterial inactivation was also negligible in the presence of g-STO:Rh(1%) after 4 h of irradiation, which is in contrast to inactivation of phage. Obvious bacterial sterilization required more than 12 h of irradiation, which suggested that g-STO:Rh shows superior antiphage activity compared to bactericidal activity. Inactivation of bacteria in the presence of g-STO:Rh with various Rh doping C


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complex systems.30 Thus, bacteria can be more easily inactivated than phage by reactive oxygen species. To confirm the presence of •OH produced from g-STO:Rh under irradiation, we examined the photocatalytic decomposition of DMSO. DMSO is known to be oxidized to methanesulfinic acid and methanesulfonic acid by • OH generated on the photocatalyst.60−62 After visible-light irradiation of g-STO:Rh, both methanesulfinic acid and methanesulfonic acid were detected, indicating the production of •OH. Furthermore, we confirmed that H2 production was not observed in bacterial suspension after 24 h under visible-light irradiation, indicating that excited electrons induced by photocatalysis were consumed in oxygen reduction, resulting in possible production of O 2 − and/or H 2 O 2 . Nevertheless, with production of reactive oxygen species from g-STO:Rh under visible-light irradiation, superior bacterial inactivation compared with that of phage was not observed, indicated that g-STO:Rh is a unique photocatalyst showing effective antiphage activity and has a significant factor other than reactive oxygen species for the superior inactivation of phage. 3.2. Change of the Rh Valence State of g-STO:Rh under Visible-Light Irradiation. After photocatalytic inactivation of phage and bacteria with g-STO:Rh under visiblelight irradiation, the color of g-STO:Rh changed from gray to purple. We previously reported that STO:Rh has a high amount of Rh4+, which changes to Rh3+ by ball-milling with color changes.40,52 We assume that the color change of g-STO:Rh after photocatalytic inactivation may be attributable to changes in the Rh valence state. To elucidate the change in Rh valence state of g-STO:Rh before and after 4 h photocatalytic inactivation of phage, the associated diffuse reflectance spectra of the photocatalyst were recorded (Figure 5). Absorption

amounts in aqueous suspension under dark conditions and visible-light irradiation was evaluated to establish the optimal Rh doping amount, as shown in Figure S2. g-STO:Rh(1%) showed the highest antibacterial activity, yielding ∼4.5-log reduction in survival rate after 24 h of irradiation, whereas gSTO:Rh(0.5%) and g-STO:Rh(2%) exhibited ∼2-log and ∼3log reductions, respectively, following irradiation for the same interval. Superior antiphage activity compared to antibacterial activity of g-STO:Rh(1%) is a unique property. As mentioned, ∼5-log reduction in the survival rate of phage was observed with gSTO:Rh(1%) after 4 h of irradiation, while reduction in survival rate of of bacteria was almost negligible for the same interval. For reference, the antiphage and antibacterial activity of a representative photocatalyst, TiO2 (P25, Evonik), which is employed as an environmental remediation material, are shown in Figure 4. Survival rate of bacteria was significantly decreased

Figure 4. Survival rate of phage and bacteria in the presence of TiO2 photocatalyst under UV-light irradiation (0.12 mW/cm2). Photocatalyst, 5 mg; light source, black light; volume of aqueous solution, 50 mL; initial concentrations of phage and bacteria, 5.0 × 107 pfu/mL and 5.0 × 107 cfu/mL, respectively.

after 60 min, although that of phage did not show an obvious decrease, a result opposite to the trend for g-STO:Rh. Superior antibacterial activity compared to antiphage activity is typical for photocatalysis and other oxidant chemicals, such as chlorine, ozone, and chlorine dioxides.30 It has been reported that various reactive oxygen species on the surface of TiO2 under irradiation are generated in oxidative and reductive reactions as follows:56−59 Oxidative reactions: OH− + h+ → •OH

Figure 5. Diffuse reflectance spectra of g-STO:Rh(1%) photocatalyst before and after 4 h photocatalytic inactivation of phage. Diffuse reflectance spectra were converted from reflection to absorbance by the Kubelka−Munk method. Photocatalyst, 0.15 g; light source, 200 W xenon lamp with a Y-44 cutoff filter; volume, 50 mL; initial concentration of phage, 5.0 × 107 pfu/mL.

•

OH + •OH → H 2O2

Reductive reactions: O2 + e− → O2− O2− + H+ → •HO2 •

features at 420 and 580 nm are ascribed to Rh3+ and Rh4+, respectively:63 absorption at 420 nm is due to electron transition from the occupied state of Rh3+ to the conduction band of SrTiO3, and absorption at 580 nm is caused by electron transition from the valence band of SrTiO3 to the unoccupied d state of Rh4+. Thus, the Rh ions in g-STO:Rh are mixed-balance states of Rh3+ and Rh4+. After 4 h of irradiation with visible light, the Rh3+ absorption decreased, whereas the Rh4+

HO2 + e− + H+ → H 2O2

Bacteria can be inactivated by reactive oxygen species, such as • OH, O2−, and H2O2, and can be easily sterilized because even light damage to the bacterial cell surface can destroy metabolic systems of the bacterium, such as respiration or other active systems.37 On the other hand, phage has resistance for reactive oxygen species because of the lack of enzymes and other D


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dopant. Therefore, the phage and bacteria inactivation dependence on Rh4+ ion were evaluated by comparing the effects of STO:Rh and STO:Rh,Sb. X-ray diffraction measurement revealed that both g-STO:Rh and g-STO:Rh,Sb featured cubic SrTiO3 structures (Figure S4), although small peaks of TiO2 anatase (ca. 25°) were observed. Ž ivojinović et al.67 reported that SrTiO3, which was pulverized in a ball-milling device, formed antase TiO2 (tetragonal) as well as our result. They denoted that the reaction between SrTiO3 and atmospheric CO2 occurs in the ball-milling container, leading to formation of orthorhombic SrCO3 and antatase TiO2. Therefore, the peak of anatase TiO2 was observed in XRD patterns. We assumed that TiO2 anatase does not affect photocatalytic performance in our study because anatase responds to UV light. Additionally, the surface areas of g-STO:Rh and g-STO:Rh,Sb were comparable (∼41 m2/g) (Table S1), suggesting that the photocatalytic activities of the two substances should not differ due to this parameter. Interestingly, both gSTO:Rh(0.5%),Sb(0.5%) and g-STO:Rh(1%),Sb(1%) exhibited negligible phage inactivation; nevertheless, gSTO:Rh(1%) provided a 5-log reduction after 4 h of irradiation, as shown in Figure 7. These results showed that the photocatalysis-induced Rh4+ ion contributes to antiphage activity.

absorption of g-STO:Rh increased, indicating that the valence state of partial Rh ion in g-STO:Rh changed from 3+ to 4+. In STO:Rh, the Rh valence state changed from Rh4+ to Rh3+ during photocatalytic water splitting, as reported by Konta et al.,40 while that in g-STO:Rh partially changed from Rh3+ to Rh4+ under visible-light irradiation. It is reported that reduction of Rh4+ to Rh3+ in STO:Rh is attributed to photogenerated electron in the presence of electron donor, which indicates that the electron donor has an important role in reduction of Rh4+. In the case of g-STO:Rh, therefore, if the electron donor exists for g-STO:Rh, we speculate that oxidation of Rh3+ to Rh4+ should be suppressed. To prove this hypothesis, we added methanol as an electron donor to the aqueous solution containing g-STO:Rh powder and irradiated the solution with visible light. As a result, change of the Rh valence state from Rh3+ to Rh4+ was not observed, as evidenced by the fact that the absorption features originating from Rh3+ and Rh4+ were not changed in diffuse reflectance spectrum (Figure 6), indicating

Figure 6. Diffuse reflectance spectra of g-STO:Rh(1%) photocatalyst in methanol aqueous solution (10 vol %) before and after 4 h visiblelight irradiation. Diffuse reflectance spectra were converted from reflection to absorbance by the Kubelka−Munk method. Photocatalyst, 0.15 g; light source, 200 W xenon lamp with a Y-44 cutoff filter; volume, 50 mL; initial concentration of phage, 5.0 × 107 pfu/ mL. Figure 7. Survival rate of phage in the presence of g-STO:Rh(1%),gSTO:Rh(0.5%),Sb(0.5%), or g-STO:Rh(1%),Sb(1%) photocatalyst in aqueous suspension under dark conditions and visible-light irradiation (110 mW/cm2, λ > 440 nm). Photocatalyst, 0.15 g; light source, 200 W xenon lamp with a Y-44 cutoff filter; volume of aqueous solution, 50 mL; initial concentration of phage, 5.0 × 107 pfu/mL.

3+

that the change of Rh valence state in g-STO:Rh from Rh to Rh4+ was due to the absence of electron donor in photocatalytic antiphage evaluation. As will be discussed, the presence of photocatalysis-induced Rh4+ has an important role for efficient inactivation of phage. 3.3. Photocatalytic Antiphage and Antibacterial Performance in Comparison with g-STO:Rh and gSTO:Rh,Sb. To examine the correlation between photocatalysis-induced Rh4+ ion and inactivation of phage and bacteria, survival rates in the presence of g-STO:Rh and gSTO:Rh,Sb were compared. Previous reports have suggested that the Rh valence state can be stabilized as Rh3+ by doping with Sb: because antimony can be oxidized to Sb5+ and the SrTiO3 host contains equivalent amounts of Rh3+ and Sb5+, Rh4+ formation is largely suppressed in Sb-doped material.64,65 Thus, the Rh valence states of STO:Rh,Sb would not be interchangeable under visible-light irradiation.64,66 Figure S3 shows the diffuse reflectance spectra of g-STO:Rh(1%),Sb(1%) before and after 4 h photocatalytic inactivation of phage. Although most rhodium ions exist as Rh3+ in prepared gSTO:Rh,Sb, a small amount of Rh4+ ion also exists. However, Rh3+ and Rh4+ absorption features changed minimally after irradiation, presumably due to the presence of the antimony

Figure 8 shows the survival rates of bacteria in the presence of g-STO:Rh and g-STO:Rh,Sb in aqueous suspension under dark conditions and visible-light irradiation. As seen with gSTO:Rh, bacterial inactivation was negligible with gSTO:Rh,Sb under dark conditions, indicating that gSTO:Rh,Sb photocatalyst particles do not cause bacterial sterilization. In contrast, under visible-light irradiation, no obvious differences in bacterial sterilization were observed between g-STO:Rh and g-STO:Rh,Sb. It is therefore suggested that the Rh4+ ion in g-STO:Rh,Sb under visible-light irradiation had no significant contribution to bactericidal performance. Subsequently, to investigate the dependence of antiphage and antibacterial performance on Rh(IV) species, we prepared Sr2RhO4, which is an oxide containing Rh(IV) species, in accordance with the paper published by Banerjee et al.68 We checked the XRD pattern of Sr2RhO4 as shown in Figure S5, indicating the successful preparation of Sr2RhO4. The molar E


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Figure 8. Survival rate of bacteria in the presence of g-STO:Rh(0.5%, 1%, or 2%), g-STO:Rh(0.5%),Sb(0.5%), or g-STO:Rh(1%),Sb(1%) photocatalyst in aqueous suspension under dark conditions and visible-light irradiation (110 mW/cm2, λ > 440 nm). Photocatalyst, 0.15 g; light source, 200 W xenon lamp with a Y-44 cutoff filter; volume, 50 mL; initial concentration of bacteria, 5.0 × 107 cfu/mL.

Figure 9. Survival rate of pathogens in a mixed suspension of phage and bacteria in the presence of g-STO:Rh(1%) photocatalyst in aqueous suspension under visible-light irradiation (110 mW/cm2, λ > 440 nm). Photocatalyst, 0.15 g; light source, 200 W xenon lamp with a Y-44 cutoff filter; volume of aqueous solution, 50 mL; initial concentrations of phage and bacteria, 5.0 × 107 pfu/mL and 5.0 × 107 cfu/mL, respectively.

mount of Rh(IV) species in Sr2RhO4 is required to be set to that of Rh(IV) species in g-STO:Rh in order to compare the antiphage and antibacterial performances as well as the paper reported by Qiu et al.,38 who compared those of 0.25% CuxO/ TiO2 with 0.25% Cu2O/TiO2 prepared by physically mixing commercial Cu2O and TiO2 powder. We prepared g-STO mixed with Sr2RhO4 (denoted as Sr2RhO4/g-STO) in an agate mortar. Sr2RhO4, calculated relative to the molar amount of Rh species in g-STO:Rh(1%), was added to g-STO. The survival rates of phage and bacteria in the presence of Sr2RhO4/g-STO were evaluated as shown in Figure S6. It can be seen that negligible antiphage and antibacterial performance with Sr2RhO4/g-STO was observed; that is, Rh4+ species cause slight antiphage and antibacteria performances. Therefore, it was assumed that efficient antiphage performance with g-STO:Rh(1%) was caused by the photocatalysis-induced Rh4+ ion as mentioned earlier. Moreover, we irradiated g-STO:Rh(1%) with visible light for 4 h and then evaluated the photocatalytic antiphage performance compared with that of g-STO:Rh(1%) under dark conditions. Interestingly, phage inactivation of g-STO:Rh(1%) was still observed even under dark conditions as shown in Figure S7, suggesting that the effect of antiphage performance of photocatalysis-induced Rh4+ ion remains under dark conditions. In these studies, the inactivation of phage and bacteria was examined separately. To investigate the antiphage performance of g-STO:Rh(1%) in the presence of bacteria, the inactivation rate of pathogens in a suspension containing both phage and bacteria in the presence of g-STO:Rh(1%) was evaluated with visible-light irradiation. Distinct phage inactivation was still observed in the presence of bacteria, as shown in Figure 9; a 3log reduction was noted after 2 h of irradiation, an interval at which negligible bacterial sterilization was observed. Therefore, our results suggested that g-STO:Rh(1%), which preferentially exhibits antiphage activity over bacterial activity, has promise as an effective visible-light-driven photocatalyst in addressing phage infection in the fermentation industry. The surface of bacteria mainly contains the lipopolysaccharide consisting of lipid and polysaccharide, while that of phage consists of protein. It is known that the denaturation of protein easily occurs by transition metal ions.69 Therefore, it may be assumed that Rh4+ ion in g-STO:Rh under visible-light irradiation works by

oxidation or denaturation of protein, leading to the inactivation of phage.

4. CONCLUSIONS In conclusion, visible-light-driven g-STO:Rh(1%) photocatalyst showed efficient antiphage performance at irradiation intervals that did not cause bactericidal activity. The Rh valence state of g-STO:Rh(1%) partially changed from 3+ to 4+, accompanied by a color change from gray to purple under visible-light irradiation. The presence of Rh4+ ion induced by photocatalysis and the large surface area of g-STO:Rh under visible-light irradiation contributed to the high antiphage performance. Moreover, antiphage activity was observed even in the presence of bacteria. We demonstrated that the Rh4+ ion in g-STO:Rh under visible-light irradiation contributed to effective and selective inactivation of phage. The precise inactivation mechanisms, possibly via attachment inhibition and/or nucleic acid denaturation, etc., have not yet been determined, in part because of the complexity of such processes. However, research toward elucidating the mechanism, which is under way, is expected to be important for the design and fabrication of efficient antiphage materials. Specifically, it will be critical to determine the relationship between antiphage activity and the function of Rh4+ ions in g-STO:Rh under visible-light irradiation. The present findings demonstrate the potential of a visible-light-driven STO:Rh photocatalyst for deactivating phage (a bacterial predator) in the bacterial fermentation industry.

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S Supporting Information *

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acsami.7b07786. Seven figures showing diffuse reflectance spectra, survival rates of bacteria and phage, and XRD patterns; one table listing surface areas (PDF)

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AUTHOR INFORMATION

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Chiaki Terashima: 0000-0002-8874-1481 Kazuya Nakata: 0000-0002-6648-8534 Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS This work was supported by Joint Usage/Research Center program of the Photocatalysis International Research Center, Research Institute for Science and Technology, Tokyo University of Science.

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REFERENCES

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