Photogeneration of Reactive Oxygen Species on Uncoated Silver

Publication Date (Web): April 1, 2013 ... Yang LiJian ZhaoEnxiang ShangXinghui XiaJunfeng NiuJohn Crittenden ..... Coordination Chemistry Reviews 2017...
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Letter pubs.acs.org/Langmuir

Photogeneration of Reactive Oxygen Species on Uncoated Silver, Gold, Nickel, and Silicon Nanoparticles and Their Antibacterial Effects Wen Zhang,† Yang Li,‡,§ Junfeng Niu,‡ and Yongsheng Chen*,§ †

Department of Civil and Environmental Engineering, New Jersey Institute of Technology, Newark, New Jersey 07102, United States State Key Laboratory of Water Environment Simulation, School of Environment, Beijing Normal University, Beijing 100875, People’s Republic of China § School of Civil and Environmental Engineering, Georgia Institute of Technology, Atlanta, Georgia 30332, United States ‡

S Supporting Information *

ABSTRACT: Oxidative stress induced by reactive oxygen species (ROS) is one of the major toxicity mechanisms of engineered nanoparticles (NPs). To advance our knowledge of the photogeneration of ROS on NPs, this Letter reports the ROS generation kinetics of uncoated silver (AgNPs), gold (AuNPs), nickel (NiNPs), and silicon (SiNPs) NPs in aqueous suspension under UV irradiation (365 nm) and analyzes the potential ROS photogeneration mechanisms as well as the associated antibacterial effects. The results showed that AgNPs generated superoxide and hydroxyl radicals, whereas AuNPs, NiNPs, and SiNPs generated only singlet oxygen. The electronic structure and redox potentials of SiNPs were shown to mediate ROS generation. By contrast, ROS generation on AuNPs, AgNPs, and NiNPs was primarily due to surface plasmon resonance. The antibacterial activities of these NPs toward E. coli cells under UV irradiation were AgNPs (strongest) > SiNPs > NiNPs > AuNPs. ROS generation and metal ion release significantly enhanced the NPs’ antibacterial activity.

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Some work has qualitatively described ROS generation on metallic NPs and attributed it to the surface plasmon resonance (SPR).18−20 However, two grand challenges still need our attention. First, considerable variations in experimental conditions (e.g., light intensity, pH, and medium characteristics) often hamper the quantitative comparisons of different studies, even those on the same types of NPs, which has made it difficult to interpret the ROS generation mechanisms quantitatively. Second, unlike semiconductors, metallic and single-element NPs have fundamentally different electronic structures that have not been explicitly correlated with ROS generation. For instance, our previous work analyzed the roles of electronic structure and redox chemistry in the photogeneration of ROS on metal oxide NPs.3 However, the roles of electronic properties remain elusive for metallic NPs or singleelement NPs in this regard. Such information is important to elucidating and predicting the underlying ROS generation mechanisms of engineered NPs. Moreover, knowledge for prediction will save the cost of conducting time-consuming experiments and provide guidance for the rational design of metallic NPs for applications such as phototherapy.21 This study used four uncoated NPs, including AgNPs, AuNPs, NiNPs, and SiNPs, as our representatives to investigate

he antimicrobial efficacy of engineered nanoparticles (NPs) such as metal oxide and carbon-based NPs has been widely studied.1−3 However, except for silver nanoparticles (AgNPs),4 the antibacterial potential of metallic NPs has been rarely investigated. A few studies have reported the antibacterial properties of gold nanoparticles (AuNPs)5,6 and copper nanoparticles (CuNPs).7,8 A major toxicity mechanism of nanomaterials is oxidative stress,9−11 which is caused by reactive oxygen species (ROS) generated on engineered nanomaterials.3,10,12 Typical ROS generated in an aqueous suspension include singlet oxygen (1O2), the hydroxyl radical (•OH), and the superoxide radical (O2•−). Among these, 1O2 is the most detrimental to cells because it reacts broadly with amine acids such as methionine, vitamins such as beta-carotene, unsaturated fatty acids, proteins, and steroids.13,14 Similarly, although short-lived, •OH is also highly reactive and can nonselectively oxidize virtually all types of macromolecules, including carbohydrates, nucleic acids, lipids, and amino acids.15 In contrast, although O2•− itself is not a strong oxidant, dismutation reactions of O2•− produce hydrogen peroxide (H2O2), which can be transformed into •OH and 1O2.16 Consequently, the three types of ROS (1O2, •OH, and O2•−) may coexist and exert complex oxidative stress on biological systems.3,10,12 A sizable number of studies (see the summary in Table S1 of the Supporting Information, SI) have demonstrated ROS generation on various metallic and single-element NPs.17−20 © XXXX American Chemical Society

Received: February 5, 2013 Revised: March 21, 2013

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the formation mechanisms and kinetics of three ROS (1O2, •OH, and O2•−) in an aqueous suspension of NPs under UV irradiation at a wavelength (λ) of 365 nm. Specifically, we quantitatively evaluated the ROS generation of different NPs under the same experimental conditions (e.g., light irradiation, dose of NPs, and water chemistry). Detailed experimental procedures and material characterizations of the selected NPs are given in sections S2 and S3 of the SI. These NPs were chosen because of their broad applications in industrial, commercial, and biomedical fields as well as their demonstrated antibacterial properties.4,5,18,19 Furthermore, we examined the antibacterial activity of these NPs on Escherichia coli (E. coli) cells to study the influence of the photogeneration of ROS on the toxicity of NPs. The overarching goal is to provide fundamental insight into the ROS generation mechanisms of the engineered metallic NPs and their potential as antibacterial agents. Figure 1a shows the changes in the absorption spectrum of the AgNP suspension in the presence of 2,3-bis(2-methoxy-4nitro-5-sulfophehyl)-2H-tetrazolium-5-carboxanilide (XTT, a ROS indicator dye) during 48 h of UV irradiation. The increasing absorption intensity at 470 nm indicates the evolution of XTT-formazan, a reaction product of XTT and O2•− that is used as an indirect measure of the O2•− concentration. Interestingly, of the four NPs tested, only AgNPs generated O2•− under UV irradiation (Figure S2). Furthermore, no absorption peaks were observed in the absence of NPs under UV irradiation or for any NP aqueous suspensions during 48 h in the dark. Similarly, only AgNPs yielded a considerable amount of •OH under 48 h of UV irradiation, as shown in Figure 1b; SiNPs, NiNPs, and AuNPs did not generate •OH, as indicated by the unchanged concentration of the para-chlorobenzoic acid (p-CBA) indicator both with and without UV exposure (data not shown). Figure 1c shows that a significant degradation of furfuryl alcohol (FFA) occurred in the SiNP, NiNP, and AuNP aqueous suspensions under 48 h of UV irradiation, whereas without UV irradiation (in the dark) no degradation of FFA was detected in any NP aqueous suspension. Clearly, 1O2 was the only ROS generated by SiNPs, NiNPs, and AuNPs, whereas AgNPs did not produce any measurable 1O2. The average concentrations of the three types of ROS generated by different NPs are shown in Table S4. As with semiconductors, the generation of a specific type of ROS (e.g., •OH, 1O2, or O2•−) in SiNP suspensions under UV illumination could be qualitatively predicted on the basis of the SiNP electronic structure and solution redox potentials (EH).3 For instance, the SiNP band gap is 2.0 eV,22 which is less than the incident photon energy (approximately 3.4 eV for the 365 nm UV light). Thus, SiNP electrons can be photoexcited from the valence band (Ev) to the conduction band (Ec), with the concomitant generation of a hole in the valence band. The photoexcited electrons and holes then react with an aqueous electron acceptor (i.e., O2) and donor (i.e., H2O and OH−) to produce different types of ROS. Figure 2 aligns the redox potential (EH) of each ROS couple with the positions of the SiNP conduction/valence bands. The redox couple of H2O/ •OH is 2.2 eV with respect to the normal hydrogen electrode (NHE),3 which is greater than the SiNP Ev (2.1 eV).22 Thus, the photoexcited holes of SiNPs cannot oxidize H2O into •OH, which agrees with our experimental observations. Similarly, the SiNP Ec value (0.1 eV)22 is greater than the EH of O2/O2•− (−0.2 eV).23 Thus, the reductive powder of the photoexcited

Figure 1. (Top) O2•− generation kinetics in an aqueous suspension of AgNPs under UV irradiation as indicated by the reduction of 100 μM XTT. (Middle) •OH generation kinetics in the aqueous suspension of AgNPs under UV irradiation as indicated by the degradation of 20 μM p-CBA. (Bottom) 1O2 generation kinetics in aqueous suspensions of SiNPs, NiNPs, and AuNPs under UV irradiation as indicated by the degradation of 0.85 mM FFA.

electrons in SiNPs is insufficient to reduce O2 to O2•−, which explains why no O2•− was detected in the SiNP suspension. Because EH for 1O2/O2 is 1.88 eV,23 which is less than the SiNP Ev (2.1 eV), the photoexcited hole has enough oxidizing power to facilitate 1O2 generation in the SiNP suspension. Although the role of semiconductor NP electronic structures in the photogeneration of ROS is relatively clear, 1O2 generation for SiNPs may involve complicated mechanisms. For example, SiNPs are very efficient spin-flip activators of O2 and thus can act as efficient photosensitizers for 1O2 formation.24,25 The transition from the chemically inert ground triplet state of O2 to the highly reactive excited singlet states (1Δ and 1Σ states) can be achieved through a spin-flip process, as shown in Figure S3. For noble metals (e.g., Ag, Au, and Cu), SPR significantly affects the photogenerated ROS.18−20,26 Metallic NPs contain many freely mobile electrons that can interact strongly with light by either absorbing or scattering the photons. When NPs are excited by light of wavelength longer than the size of the NPs (in our case, 356 nm UV-light-excited NPs of 20−30 nm), the oscillating electric field of the incoming radiation induces coherent collective oscillation of the free electrons (conduction band electrons) on the metal surface, as shown in Figure S4. When the surface electron oscillation frequency is equal to the B

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growth of E. coli cells, as demonstrated previously.3 Another control test in which E. coli cells were exposed to NPs under room lighting conditions showed that their survival rates (log(Nt/N0)) were approximately −0.2 for each of the four types of NPs (Figure 3a). This indicated that direct contact with these NPs did not produce significant bacteriostatic effects. Under UV irradiation, only AgNPs, NiNPs, and SiNPs in aqueous suspension under UV irradiation exhibited enhanced antibacterial activity compared to their suspension without exposure to UV (Figure 3b). Surprisingly, because of the strong antibacterial activity, AgNPs even at a dose of 50.0 μg/L led to a higher log removal efficiency than a 10.0 mg/L dose for any of the other three types of NPs. The minimum inhibitive concentration of AgNPs for E. coli cells without UV irradiation is approximately 2 mg/L.28 The observed toxicity of AgNPs toward E. coli cells was clearly enhanced by the photogeneration of ROS. Likewise, the increased antibacterial activity of NiNPs and SiNPs was also largely attributed to ROS generation. It is worth noting that even though no O2•− and •OH were generated the role of oxidative stress from the generation of 1O2 was also evident on NiNPs and SiNPs. In contrast, AuNPs exhibited almost the same antibacterial activity on E. coli cells with or without UV exposure, probably because of the chemically inert nature of AuNPs and the relatively low adverse impacts of released 1O2.

Figure 2. Band-edge positions of SiNPs in contact with aqueous solution at pH 5.6 (the initial pH of the SiNP suspension). The locations of the lower edge of the SiNP conduction band (Ec) in the blue shaded area and upper edge of the valence band (Ev) in the orange shaded area are indicated along with the SiNP band gap in eV. The energy scale is drawn with respect to the normal hydrogen electrode (NHE) and the absolute vacuum scale (AVS) as references. On the right side, the redox potentials of several redox couples are presented.

photon frequency, SPR is generated. SPR induces a strong absorption of the incident photon energy, which can be transferred to O2 and lead to 1O2 generation.20 This explains the 1O2 generation observed in AuNP and NiNP aqueous suspensions under UV irradiation. The photoelectrons transferred to O2 are responsible for the generation of O2•−, which can further promote the generation of •OH under UV irradiation. Similar to noble metals, magnetic transition metals such as NiNPs also exhibit SPR, but owing to their relatively large optical absorption coefficients, such materials have damped plasmon resonance, which leads to less ROS generation when compared to that for AgNPs and AuNPs.27 This explains why the total ROS concentration produced on NiNPs was much less than that on AuNPs and AgNPs, as shown in Table S4. Clearly, in view of the UV photon energy and SPR available, AuNPs, AgNPs, and NiNPs should be able to generate all three types of ROS. However, experimentally, AgNPs produced both O2•− and •OH but no detectable 1O2, whereas AuNPs and NiNPs produced only 1O2. Although the ROS production could be kinetically limited, the missing ROS was more likely caused by the pronounced ion release (or photocorrosion) of metallic NPs (i.e., AgNPs and NiNPs, as discussed below) during UV irradiation, which may lead to the consumption of •OH. Consequently, some redox couples, such as Ag+/Ag, Ag2+/Ag+, AgO/Ag+, and Ni2+/Ni, may coexist and disrupt the solution redox conditions. In addition, the hydrodynamic sizes of NPs dynamically increased as aggregation took place (Figure S5). Aggregation tends to reduce the available surface area and thus potentially affects ROS production and antibacterial activity.26 To determine the influence of the photogenerated ROS on antibacterial activity, we performed the standard bacterial inhibition assay with E. coli cells. In the control test without exposure to NPs, 2 h of UV irradiation did not compromise the

Figure 3. Two hour inactivation kinetics of E. coli cells by four types of NPs under (top) room lighting and (bottom) UV irradiation. All other conditions were the same as in Figure 1, except that the concentration of AgNPs was 50 μg/L, whereas that of the other three NPs was 10.0 mg/L. Asterisks (*) denote a significant difference from the control at the 95% confidence level.

As a result of the photooxidation and ROS formation, metallic NPs may undergo dissolution,29,30 which in turn can influence the antibacterial activity by changing the bioavailability of the NPs. The effect of UV irradiation on NP dissolution varied with particle type. As shown in Figure 4, NiNPs and AgNPs had more evident dissolution under 2 h of UV irradiation than in the dark, whereas AuNPs and SiNPs did not exhibit ion release at all (data not shown). After 48 h of UV irradiation, the released ion concentrations of AgNPs and NiNPs reached 8.6 ± 0.4 mg/L and 76.2 ± 3.5 μg/L, respectively. Thus, both oxidative stress and the released toxic C

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Notes

Ag and Ni ions likely contributed to the antibacterial activities of AgNPs and NiNPs under UV irradiation. Apparently, ROS is not the only dominant antibacterial mechanisms for AgNPs and NiNPs. Thus, to establish a single correlation between ROS generation and the antibacterial activity, one needs to rule out the potential effects of toxic ion release on the toxicity observation.

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS This study was partially supported by the U.S. Environmental Protection Agency Science to Achieve Results Program (grant RD-83385601), Engineering Research Center (ERC)/Semiconductor Research Corporation (SRC)/ESH (grant 425.025), and the China Scholarship Council.

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Figure 4. Ion release of AgNPs and NiNPs in the dark and under UV irradiation for 48 and 2 h (inset).

In conclusion, this study experimentally evaluated the photogeneration of ROS and its linkage to the antibacterial activity of selected metallic or single-element NPs. The photochemical experiments were performed under the same UV irradiation on the same NP mass basis to facilitate a quantitative comparison of the ROS generation ability of different NPs. The reported findings laid the groundwork for unraveling the ROS photogeneration mechanisms and antibacterial activities of engineered NPs.

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ASSOCIATED CONTENT

S Supporting Information *

Literature review for ROS generation of different engineered metallic or single elemental NPs. Materials and methods. Property information of engineered metallic or single elemental nanoparticles. Digestion method of engineered metallic nanoparticles for ICP-MS analysis. No O2•− generation by AuNPs, SiNPs, and NiNPs. Average ROS concentrations and quantum yield (QY) generated by different NPs. 1O2 generation mechanism of SiNPs. ROS generation mechanism of metallic NPs. Hydrodynamic diameter changes of NPs under UV irradiation. This material is available free of charge via the Internet at http://pubs.acs.org.

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REFERENCES

AUTHOR INFORMATION

Corresponding Author

*E-mail: [email protected]. Phone: (+1) 404894-3089. Fax: (+1) 404-894-2278. Author Contributions

W.Z. and Y.L. contributed equally to this work. D

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