Effects of Chloride Ions on Dissolution, ROS Generation, and Toxicity

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Effects of Chloride Ions on Dissolution, ROS Generation, and Toxicity of Silver Nanoparticles under UV Irradiation Yang Li, Jian Zhao, Enxiang Shang, Xinghui Xia, Junfeng Niu, and John C. Crittenden Environ. Sci. Technol., Just Accepted Manuscript • DOI: 10.1021/acs.est.7b04547 • Publication Date (Web): 20 Dec 2017 Downloaded from http://pubs.acs.org on December 22, 2017

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Environmental Science & Technology

1

Effects of Chloride Ions on Dissolution, ROS Generation,

2

and Toxicity of Silver Nanoparticles under UV Irradiation

3

Yang Li1, Jian Zhao1, Enxiang Shang1, Xinghui Xia1, Junfeng Niu2, and John Crittenden3

4 5

1

6 7

2

8 9

3

State Key Laboratory of Water Environment Simulation, School of Environment, Beijing Normal University, Beijing 100875, People’s Republic of China School of Environment and Civil Engineering, Dongguan University of Technology, Dongguan, 523808, People’s Republic of China School of Civil and Environmental Engineering and the Brook Byers Institute for Sustainable Systems, Georgia Institute of Technology, Atlanta, Georgia 30332, United States

10 11

ABSTRACT: This work investigates the effect of chloride ion (Cl−) on dissolution, reactive

12

oxygen species (ROS) generation, and toxicity of citrate-coated silver nanoparticles (AgNPs)

13

under UV irradiation. The dissolution rate was decreased by 0.01 M Cl− due to AgCl

14

passivation on the AgNP surface. By contrast, high concentrations of Cl− (0.1 or 0.5 M)

15

promoted dissolution due to the formation of soluble Ag-Cl complexes (AgClx1-x). The

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generation of O2•− in the AgNPs/Cl−/UV system was promoted by 0.01 M Cl−, whereas was

17

retarded by 0.1 or 0.5 M Cl−, which was probably because the aggregation of AgNPs at high

18

ionic strength reduced the nanoparticles’ surface areas for radical formation. Additionally, Cl−

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contributed to •OH generation in the AgNPs/Cl−/UV system, in which the produced •OH

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concentrations increased with increasing Cl− concentrations. The reduction reaction between

21

silver ions and O2•− resulted in lower dissolution rates of AgNPs/Cl− mixtures under UV

22

irradiation than those in the dark. The phototoxicity of AgNPs toward E. coli with different

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concentrations of Cl− followed the order of 0.5 M>0 M>0.1 M>0.01 M. Both ROS and

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dissolved Ag played significant role in the phototoxicity of AgNPs. This work demonstrates

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the potential importance of anions in the fate and biological impact of AgNPs.

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KEYWORDS: Silver Nanoparticle; Chloride; Dissolution; Reactive Oxygen Species;

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Toxicity; UV Irradiation *

Corresponding author: e-mail: [email protected]; Phone: +86-10-5880 7612; Fax: +86-10-5880 7612. 1

ACS Paragon Plus Environment


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INTRODUCTION

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Silver nanoparticles (AgNPs) have been widely used in many fields, including

31

antimicrobial materials, electronics, biosensing, chemical catalysis, and surface-enhanced

32

Raman spectroscopy.1-3 AgNPs have been incorporated as antimicrobial agents into medical

33

equipment and various consumer products such as textiles, plastics, cosmetics, personal care,

34

and food storage containers.4,

35

AgNPs may enter the natural aquatic environments.6, 7 The concern with the release of AgNPs

36

into natural waters is due to their unknown physicochemical processes, such as dissolution,

37

reactive

38

microorganisms.8-10 To better perform the aquatic risk assessment, it is of great importance to

39

investigate how water chemistry affects environmental behaviors, bioavailability, and toxicity

40

of AgNPs.

oxygen

species

5

When these products are washed or disposed, remaining

(ROS)

generation,

and

toxicity

on

ecosystems

and

41

Chloride (Cl−) is one of the most prevalent monovalent anions in seawater and natural

42

aqueous systems.11, 12 In addition, Cl− is present in most bacterial culture media.13 Thus, it is

43

essential to consider the effect of Cl− on the behavior of AgNPs in the aqueous environment.

44

The interaction of Cl− and AgNPs is complex because of the formation of soluble and

45

insoluble Ag-Cl species, which depends on the Cl/Ag ratios (total Cl concentration versus

46

total Ag concentration).13 At low Cl/Ag ratios, the presence of Cl− leads to the formation of a

47

AgCl layer on the AgNP surface,14,

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dissolution rate of AgNPs.13 However, at higher Cl/Ag ratios, soluble species of AgClx1-x

49

begin to dominate the insoluble AgCl, which results in a higher AgNP dissolution rate.13

50

Although the interaction between Cl− and Ag+ and their effect on AgNP dissolution has been

51

previously studied,8, 13, 16 none of the works have considered the effects of light irradiation on

52

such dissolution as a function of Cl/Ag ratios. Clearly, potential photochemical interactions of

53

Cl− and the resulting Ag-Cl species are inevitable in the natural environment,9, 13, 16 and have a

15

which may completely inhibit or decrease the

2


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profound impact on the dissolution behavior of AgNPs, which is important for achieving a

55

holistic understanding.

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Reactive oxygen species (ROS) generation is one of the most important photochemical

57

processes of AgNPs in aquatic environments.17-19 Our previous work has demonstrated that

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bare AgNPs generate superoxide radical (O2•−) and hydroxyl radical (•OH) under UV

59

irradiation, while citrate-coated AgNPs only produce O2•−.9, 20 Likewise, the photoirradiation

60

of Cl− can result in the formation of hydrated electrons (Cl− + hv = Cl + eaq−).21-23 Whether

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the photogenerated hydrated electrons by Cl− could be transferred to AgNPs and improve the

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ROS generation capacity remains largely elusive. In addition, AgNPs are prone to aggregate

63

at high ionic strengths,8, 12, 24 which decrease the surface areas of AgNPs and their ROS

64

generation concentration. Therefore, a key question to explore is how the potentially opposite

65

effects induced by Cl− influences ROS generation by AgNPs.

66

Numerous studies have investigated the effect of AgNPs’ physicochemical properties

67

(i.e., size, shape, surface coating/area, chemical composition, and crystal structure) on their

68

toxicity toward organisms;17, 25 however, the effect of inorganic ions such as chloride on

69

AgNP toxicity has received little attention. For example, Levard et al.26 demonstrated that at

70

low Cl/Ag ratios, Ag+ precipitated with Cl− to form solid AgCl, which protects E. coli cells

71

from exposure to AgNPs and thus reduces their toxicity. At high Cl/Ag ratios, the formation

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of soluble AgClx1-x species caused greater toxicity toward E. coli.13 Another study indicated

73

the dependence of AgNPs’ toxicity to E. coli on Cl− concentrations and attributed this

74

dependence to the availability of dissolved AgClx1-x species, which is an additional effect

75

from ionic species rather than from nanoparticles.5 Nevertheless, previous studies have not

76

considered the factor of light exposure and associated photochemical impacts on the toxicity

77

of AgNPs.

78

The aim of the present work is to further investigate how different Cl− concentrations 3



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affect the dissolution, ROS generation, and toxicity of AgNPs under environmentally relevant

80

levels of UV light irradiation (365 nm). When AgNPs are released into natural waters, they

81

will inevitably be exposed to light from the sun or artificial lighting, such as UV, xenon lamps,

82

and conventional fluorescent tubes.9, 27 UV irradiation at a 365 nm wavelength (UV-365) is

83

the primary component of UV irradiation that reaches the earth’s surface.28, 29 In addition,

84

AgNPs will be exposed to UV light during wastewater treatment. E. coli are selected as

85

model organism because of their rapid propagation speed, well-established genetics, and

86

well-characterized physiological properties.30,

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microorganisms of fecal contamination are prevalent in surface water, sewage overflows, and

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urban stormwater,32 which makes the interactions between E. coli and AgNPs are likely to

89

occur in natural waters. We also investigate the Cl−-concentration-dependent photogeneration

90

of typical ROS (1O2, •OH, and O2•−) and Ag+ release on AgNPs under UV light irradiation. In

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addition, the toxicity of AgNPs toward E. coli cells as a function of Cl/Ag ratios was

92

investigated. Moreover, the toxicity of AgNPs was ultimately correlated to the released silver

93

ions and ROS levels in the AgNP/Cl− mixtures.

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MATERIALS AND METHODS

95

Chemicals.

Furfuryl

alcohol

(FFA),

31

In addition, E. coli as indicator

para-chlorobenzoic

acid

(pCBA),

96

3-Bis(2-methoxy-4-nitro-5-sulfophehyl)-2H-tetrazolium-5-carboxanilide

97

chloride (NaCl), trace-metal grade HNO3 (67%–70%, w/w), and citrate-stabilized AgNPs

98

stock suspensions (20 nm) were purchased from Sigma-Aldrich (St. Louis, MO, U.S.). The

99

total silver concentration of the citrate-AgNPs in the stock suspension was 19.47 ± 0.26 mg/L.

100

E. coli cells were purchased from Takara Co. LLC (Dalian, China). Yeast extract, tryptone,

101

NaH2PO4·2H2O and Na2HPO4·12H2O were purchased from J&K Co. LLC (Beijing, China).

102

HPLC-grade orthophosphoric acid and methanol were purchased from Fluka Co. LLC (Buchs,

103

Switzerland). A water purification system (Thermo Scientific, U.S.) was used to produce 4


(XTT),

2,

sodium

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ultrapure water (resistance > 18.2 MΩ). All reagents were of high analytical grade and used

105

without further purification.

106

Measurement of AgNP Photochemical Dissolution. For the dissolution experiments, a

107

series of 100 mL suspensions of AgNPs (200 µg/L) containing different concentrations of

108

NaCl (0, 0.01, 0.1, and 0.5 M) were irradiated by ultraviolet lamp (UVP model UVGL-21,

109

San Gabriel, CA, U.S.). The UV lamp has an output spectrum ranging from 315 to 400 nm

110

with peak intensity at a 365 nm wavelength. The light intensity on the surface of the AgNP

111

suspensions was 1.0×10-6 einstein·L-1·s-1. During UV irradiation, the temperature of the

112

suspension was maintained at 22 ± 2 oC by a Fisher Scientific Isotemp Digital-Control Water

113

Bath. After different irradiation times, 2.5 mL of AgNP suspension was collected and filtered

114

by Amicon Ultra-4 centrifugal ultrafilter containing porous cellulose membranes (3K,

115

Millipore, U.S.) to remove nanoparticles.33, 34 Two mL of the filtrate was collected and mixed

116

with 2 mL of trace-metal grade HNO3 to completely dissolve the AgNPs. The concentration

117

of dissolved Ag+ was analyzed using inductively coupled plasma-mass spectrometry

118

(ICP-MS, Elan DRC II, PerkinElmer, U.S.). Control experiments using 1×10-4 and 1×10-5

119

AgNO3 in ultrapure water were performed and the Ag+ recovery ranged from 97.5% to 97.6%,

120

respectively, indicating that the membrane sorption had a minor effect on dissolved Ag+. The

121

dissolution experiments were conducted in the dark. All dissolution experiments were

122

conducted in triplicate to confirm reproducibility. The dissolution experiment of 200 µg/L

123

AgNPs dispersed in different concentrations of NaCl solutions was also conducted in the dark

124

(no light exposure).

125 126

To quantitatively assess the effect of Cl− on the dissolution of AgNPs, the released Ag+ concentrations of AgNPs with or without Cl− were modeled by Eq. 1:

127

[Ag+] released = [Ag+] max [1- exp(-k· t)]

128

where [Ag+] released is the Ag+ concentration (μg/L) released by AgNPs at the reaction time of t 5


(1)


129

(h), [Ag+] max is the maximum Ag+ concentration (μg/L) released by AgNPs when t→∞, and k

130

is the pseudo-first-order rate constant (h-1).

131

ESR detection of O2•−, •OH, and 1O2. Production of 1O2 in the AgNPs/Cl− mixtures

132

was monitored using 2, 2, 6, 6-tetramethyl-4-piperidone (TEMP) as a spin trap agent. 5,

133

5-dimethyl-1-pyrroline-N-oxide (DMPO) was used as the spin trap agent for O2•− and •OH.

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The AgNPs/Cl− mixture for O2•− detection was prepared by mixing 20 mL DMPO (0.5 M), 3

135

mL NPs dispersed in DMSO (500 mg/L), 3 mL NaCl solution (1.0 M), and 274 mL DMSO.

136

The mixture for •OH detection was prepared by mixing 20 mL DMPO (0.5 M), 3 mL NP

137

suspension (500 mg/L), 3 mL NaCl solution (1.0 M), and 274 mL ultrapure water. For 1O2

138

detection, the mixture was prepared by mixing 6 mL TEMP (4 M), 3 mL NP suspension (500

139

mg/L), 3 mL NaCl solution (1.0 M), and 288 mL ultrapure water. The mixtures were placed

140

into a cylindrical quartz cell and irradiated by the same UV lamp. After 30 min, the mixtures

141

were removed with a capillary and quickly measured by electron spin resonance spectrometry

142

(ESR; ESP-300E, Bruker Instruments, Karlsruhe, Germany). TEMP was oxidized by 1O2 to

143

4-oxo-2, 2, 6, 6-tetramethyl-1-piperdinyloxy radical (TEMPO) when 1O2 was produced.

144

Accordingly, ESR signals for DMPO-O2•−, DMPO-•OH, and TEMPO adducts were used to

145

measure O2•−, •OH, and 1O2 formation, respectively.

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Detection of Photogenerated ROS by Molecular Probe Method. The reaction

147

suspensions containing 200 µg/L of AgNPs and different concentrations of NaCl (0, 0.01, 0.1,

148

and 0.5 M) were irradiated by the same UV lamp. One hundred μM XTT, 20 μM pCBA, and

149

850 μM FFA were used as molecular probes for O2•−, •OH, and 1O2,33, 34 respectively. For

150

XTT, 1 mL of the suspension was collected and injected into a quartz vial after different UV

151

irradiation times. The concentration of XTT-formazan in the color orange produced from the

152

reduction of XTT by O2•− was measured by UV-Vis spectrophotometer (Cary 50, Varian, Palo

153

Alto, U.S.) at 470 nm. For pCBA and FFA, 500 µL of the suspensions were filtered according 6


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to the reported method.33, 34 The filtration process was facilitated by centrifugation at 7000 ×

155

g for 40 min. Previous studies have shown that pCBA photolysis under UV irradiation and

156

adsorption of pCBA on filters is negligible. 27, 28 Concentrations of pCBA and FFA were

157

analyzed with a high-performance liquid chromatography (HPLC, Agilent 1100, U.S.)

158

following the published methods.33, 34

159

Toxicity Assessment of AgNPs under UV Irradiation. E. coli cells were incubated in

160

Luria-Bertani (LB) medium at 37 oC.27, 35 After incubation for 16 h, the E. coli suspension

161

was split into four vessels to wash the bacterial cells. Each vessel was centrifuged (7000 g for

162

5 min) to form a pellet. The pellet was resuspended in 0.85% NaCl solutions, and centrifuged

163

again. The supernatant was discarded, and the resulting pellets were resuspended in 100 mL

164

ultrapure water containing 200 µg/L of AgNPs and different concentrations of NaCl (0, 0.01,

165

0.1, and 0.5 M). The final cell density in the reaction suspensions were approximately 2×105

166

colony-forming units (CFU)/mL. During UV irradiation, the mixed suspensions were stirred

167

with a magnetic stirrer throughout the experiment. At different irradiation times, 0.1 mL of

168

the sample was collected and diluted to yield a viable cell density suitable for the plate

169

counting method. The LB agar plates were incubated at 37 °C for 24 h before counting the

170

number of viable bacterial colonies. The results were presented as the percentage of surviving

171

bacteria, which was calculated by dividing the number of colonies on the sample plate (Nt) by

172

the number of colonies on a control plate (N0) (no NP exposure) incubated under the same

173

conditions. For comparison, the same experiments were also conducted under dark

174

conditions.

175

A citrate control experiment was performed to observe the possible toxicity of the

176

coating, which showed no negative effect on bacterial growth. The same experiment was also

177

conducted to determine the effect of Ag+ only (as AgNO3 in DI water) on E. coli growth. The

178

viability of E. coli cells after exposure to AgNO3 at the same Ag+ concentration released from 7



179

AgNPs with or without Cl− was investigated. All experiments were performed in triplicate

180

under sterile conditions. The disruption of bacteria cell membrane and leakage of intracellular

181

constituents was assessed by UV-Vis spectrophotometer according to a reported method.34

182

RESULTS AND DISCUSSION

183

Influence of Light Irradiation and Chloride Concentrations on Dissolution Kinetics.

184

Figure 1 shows the effect of light irradiation conditions on dissolution concentrations of Ag+

185

over time as a function of Ag/Cl− ratios. The experimental data was fitted by Eq. 1 and the

186

model fits are shown by the dashed lines in Figure 1 with two fitting parameters of [Ag+] max

187

and k. Table 1 shows the correlation coefficients (R2), objective function (OF) as defined

188

elsewhere,7 and the fitted values of k and [Ag+] max. The data for AgNPs in the absence of Cl−

189

under UV irradiation yields the lowest OF value (0.06), which is indicative of the best fit.

190

Under other conditions, the OF values are no more than 0.30. The values of R2 are within

191

0.91 to 0.99, which indicates that the model could explain at least 91% of the variance of the

192

experimental data.

193

In the absence of Cl−, the fitted values of k and [Ag+] max for AgNPs under UV irradiation

194

was higher than those conducted in the dark. The faster photochemical dissolution rates of

195

AgNPs compared to those in the dark might be due to the photolysis of citrate coating, which

196

facilitates the interaction of AgNP surfaces with photons, electrons, or O2.36-38 Similar results

197

have also demonstrated that the dissolution rate of citrate-coated AgNPs in the dark was

198

lower than under light irradiation conditions (e.g., room light, solar, or simulated light

199

irradiation).9, 39, 40 In contrast, after the addition of Cl−, the fitted values of k and [Ag+] max for

200

AgNPs under UV irradiation was lower than those in the dark at the same Cl− concentration.

201

As shown in Table 1, both the UV irradiation condition and Cl− concentrations influenced the

202

fitting parameters of k and [Ag+] max. Under UV irradiation, the values of k and [Ag+] max 8


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followed the order of k0.5 ≈ 1.2k0.1 ≈ 1.3k0 ≈ 1.6k0.01 and [Ag+] max, 0.5 ≈ 1.2[Ag+] max, 0.1 ≈

204

1.4[Ag+] max,

205

followed the order of k0.5 ≈ 1.2k0.1 ≈ 2.1k0 ≈ 2.3k0.01 and [Ag+] max, 0.5 ≈ 1.1[Ag+] max, 0.1 ≈

206

1.8[Ag+] max, 0 ≈ 2.9[Ag+]max, 0.01, respectively.

0

≈ 3.3[Ag+] max,

0.01,

respectively. In the dark, the values of k and [Ag+] max

207

The dissolution rate and the maximum released Ag+ concentration under UV irradiation

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or in the dark were both inhibited by 0.01M Cl−. This inhibition could be due to the

209

encapsulation of AgNPs by AgCl (Ag+ + Cl− → AgCl(s)) as mentioned in the three published

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works.8, 14, 16 Higher concentrations (0.1 and 0.5 M) of Cl− substantially increased k and

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[Ag+] max with or without UV light irradiation, which were proportional to the concentration

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of Cl−. This was presumably due to the formation of soluble Ag-Cl complexes (AgClx1-x).13

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At the same concentration of Cl−, the dissolution rates of AgNPs in the dark were higher than

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those under UV irradiation. The dissolution rates of AgNPs in the presence of 0.1 and 0.5 M

215

Cl− in the dark were 1.6-fold and 1.5-fold higher than those under UV irradiation,

216

respectively. The maximum released concentrations of Ag+ in the presence of 0.1 and 0.5 M

217

Cl− in the dark were 1.3-fold and 1.2-fold higher than those under UV irradiation,

218

respectively. The decreased dissolution rates and maximal dissolution concentrations of

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AgNPs with Cl− under UV irradiation compared to those in the dark will be subsequently

220

discussed.

9



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Figure 1. The effect of Cl− concentrations on the dissolution kinetics of AgNPs (a) in the dark or (b) under UV irradiation (pH 5.6, AgNP concentration of 200 µg/L, particle size of 20 nm).

224 225

Table 1. Correlation coefficients (R2) and fitting parameters for the dissolution kinetics of AgNPs in the absence or presence of Cl− under UV irradiation. Light condition

Cl− concentration (mol/L)

OF

k (h-1)

[Ag+]max (µg/L)

R2

dark

0

0.23

0.034

70.67

0.99

dark

0.01

0.15

0.032

42.89

0.94

dark

0.1

0.20

0.063

120.70

0.99

dark

0.5

0.07

0.073

126.16

0.99

UV

0

0.06

0.037

80.67

0.99

UV

0.01

0.21

0.030

33.42

0.91

UV

0.1

0.30

0.040

90.23

0.93

UV

0.5

0.10

0.048

109.15

0.99

226

ESR Detection of O2•−, •OH, and 1O2. ESR was used to investigate whether ROS was

227

generated in the AgNP suspension, NaCl solution, or their mixture under UV irradiation. As

228

shown in Figure 2(a), six typical peaks of ESR spectral signals for DMPO-O2•− adducts are

229

detected in the AgNP suspension under UV irradiation. This is consistent with our published

230

results using the indicator probe method.9 When AgNPs are excited by light with wavelengths

231

longer than the NP size (in our case, UV light of 365 nm and AgNPs of 20 nm), the

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photoelectrons could be transferred to O2, facilitating the generation of O2•−.13, 17 In addition,

233

the conduction band of the Ag2O (−2.0 eV) layer on the UV-exposed AgNP surface is lower

234

than the redox potential of O2/O2•− (−0.2 eV),27,

235

photoexcited electrons in Ag2O could reduce O2 to O2•−. DMPO-O2•− adducts with lower

41, 42

thus the reductive powder of the

10


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intensity than those detected in the AgNP suspension was detected in the NaCl solution. It has

237

been found that UV irradiation of Cl− can lead to the generation of hydrated electron (Cl− +

238

hv = Cl + eaq-),21-23 which could be transferred to oxygen and produce O2•−. After the addition

239

of AgNPs into the NaCl solution, the mixture produced more O2•− than the NaCl solution or

240

AgNPs alone, as shown in Figure 2(a). The intensities of the DMPO-O2•− adducts in three

241

systems decreased in the order of AgNP/Cl− mixture > AgNPs > Cl−. No DMPO-O2•− signal

242

was observed in water samples containing only the spin probe under UV irradiation. In the

243

dark, the AgNP suspension, NaCl solution, or their mixture did not induce significant

244

generation of DMPO-O2•− adducts.

245

As shown in Figure 2(b), no DMPO-•OH adduct is observed in the citrate-coated AgNP

246

suspension using ESR under UV irradiation, which was consistent with our published results

247

in which citrate-coated AgNPs could not generate •OH measured by the molecular probe

248

method.9 This is probably because the citrate coating could scavenge •OH.9 However, a

249

four-line spectrum with relative intensities of 1:2:2:1 for the DMPO-•OH spin adduct was

250

observed in the NaCl solution. The photogeneration of •OH occurred primarily because the

251

generated O2•− could undergo disproportionation reaction and produce H2O2 that could be

252

transformed into •OH.9, 43, 44 The addition of AgNPs into the NaCl solution had negligible

253

effects on the intensities of DMPO-•OH addition compounds, indicating that the generation

254

of •OH in the AgNP/Cl− mixture was primarily attributed to the Cl−. Conversely, in the dark,

255

no measurable •OH was detected in the NaCl solution, AgNP suspension, or their mixture.

256

Also, no •OH signal was detected in water samples containing only DMPO under UV

257

irradiation. As shown in Figure 2(c), no characteristic peaks of TEMPO spin adducts are

258

observed in the NaCl solution, AgNP suspension, or their mixtures under UV irradiation,

259

meaning that no measurable amount of 1O2 was generated in the three systems.

260 11



261 262 263 264 265 266 267 268 269 270 271

Figure 2. ESR spectra recorded at ambient temperatures for (a) DMPO adduct with O2•−, (b) DMPO adduct with •OH, and (c) TEMP adduct with 1O2 in AgNP suspensions, NaCl solutions, or their mixtures under UV irradiation (pH 5.6, AgNPs of 5 mg/L, particle size of 20 nm, and Cl− of 0.01 M).

272

Generation Kinetics of ROS. Molecular probe assays were conducted to confirm the

273

effect of Cl− concentrations on the ROS generation in the NaCl solutions, AgNP suspensions,

274

or their mixtures under UV irradiation. Figure 3 shows the changes in the absorbance of

275

XTT-formazan at λ = 470 nm for the NaCl solutions, AgNP suspensions, or their mixtures

276

during a 6-h exposure to UV irradiation. Specifically, Figure 3(a) shows that in NaCl solution,

277

O2•− is produced progressively with time under UV irradiation. The production rates are

278

proportional to the concentration of Cl−. Previous studies have also detected O2•− in seawater

279

under natural sunlight irradiation where Cl− is the main constituent in the seawater.45-47 As

280

shown in Figure 3(b), absorption peaks at λ = 470 nm also increase with the UV irradiation

281

time in AgNP suspensions with some dependence on the NaCl concentrations. It has been

282

previously reported that citrate-coated AgNPs could generate H2O2, indicating that O2•−, a

283

precursor for H2O2 production, was generated by AgNPs under UV irradiation.16 Although

284

AgNPs enhanced the photogeneration rates of O2•− in NaCl solutions, no obvious

285

Cl−-concentration-dependent increased O2•− photogeneration rate was observed in the

286

AgNP/Cl− mixtures. After addition of 0.01 M Cl− to the AgNP aqueous suspension, more O2•− 12


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Page 13 of 25


287

was generated in the AgNP/Cl− mixture than in the AgNP suspension alone. The higher

288

generated O2•− concentration in AgNPs/Cl− mixture (0.01 M Cl−) was primarily due to

289

Cl−-induced O2•− generation. After addition of higher concentrations (0.1 M or 0.5 M) of Cl−

290

to the AgNP aqueous suspension, a lower amount of O2•− was generated than in the AgNPs

291

alone. Fast aggregation of AgNPs was observed in the presence of 0.1 or 0.5 M NaCl (Figure

292

S1). This is consistent with previous work in which the critical coagulation concentration of

293

citrate-AgNPs is 0.07 M for NaCl.48 The reduced O2•− generation rates at higher Cl−

294

concentrations may result from the significant aggregation of AgNPs that decreased the

295

available surface areas of NPs for reaction with photons, electrons, or oxygen. AgNPs

296

generated comparable amount of O2•− in 0.1 M or 0.5 M NaCl solutions. In addition, more

297

O2•− were detected in AgNP suspensions than those in the NaCl solutions at various Cl−

298

concentrations. In the darkness, no measurable amount of O2•− was detected in the NaCl

299

solutions, AgNP suspensions, or their mixtures within the experimental period of 6 h (data

300

not shown).

301 302 303 304 305 306 307 308

Figure 3. A time-course reduction of 100 μM XTT by (a) NaCl solutions or (b) AgNPs dispersed in different concentrations of NaCl under UV irradiation (other conditions were the same as in Figure 1)

309

Previous studies have shown that pCBA photolysis under UV irradiation is negligible.33,

310

34

As shown in Figure 4, NaCl solutions result in pCBA photodegradation, and the

311

degradation rates increase with increasing concentrations of Cl−. This indicates that more

312

•OH was generated at higher Cl− concentrations. The generation of •OH is primarily

313

attributed to the photolysis of peroxidic bond of H2O2, which formed via the 13



314

disproportionation reaction of O2•− under UV irradiation.43, 44, 49 In AgNP suspensions alone,

315

pCBA had no degradation under UV irradiation as shown in Figure 4(b). This indicates that

316

no significant •OH was generated by AgNPs, probably due to the quenching effect of citrate

317

coatings for •OH.9 In the AgNP/Cl− mixture, the •OH photogeneration rate increased with the

318

increasing concentration of Cl−. A comparison between parts (a) and (b) of Figure 4 shows

319

that the pCBA degradation rates in the AgNP/Cl− mixtures are similar to those in the NaCl

320

solutions, indicating that Cl− plays a governing role in the generation of •OH in the

321

AgNP/Cl− mixtures. In the darkness, no obvious degradation of pCBA was observed in the

322

AgNP suspensions, NaCl solutions, or their mixtures within the experimental period of 6 h

323

(data not shown). None of the NaCl solutions, AgNP aqueous suspensions, or their mixtures

324

induced photodegradation of FFA (Figure S1), which indicates that 1O2 is not produced in the

325

three systems under UV irradiation.

326 327 328 329

Figure 4. •OH generation kinetics as indicated by the degradation of 20 µM pCBA by (a) NaCl solutions or (b) AgNPs dispersed in different concentrations of NaCl solutions under UV irradiation (other conditions were the same as in Figure 1).

330

Effect of ROS Scavengers on AgNPs’ Dissolution Kinetics under UV Irradiation.

331

The effect of ROS scavengers on the dissolution kinetics of AgNPs at different

332

Cl− concentrations under UV irradiation was investigated using t-BuOH and SOD as

333

scavengers of •OH and O2•−,50 respectively. The experimental data in Figure S2 was fitted by

334

Eq. 1 and the model fits are shown by dashed lines. As shown in Table 2, the fitted values of k

335

and [Ag+] max for AgNPs in the presence of Cl− change slightly after addition of t-BuOH. This 14


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336

indicates that •OH played a minor role in the photochemical dissolution of AgNPs after the

337

addition of Cl−. By contrast, the addition of SOD promoted the photochemical dissolution of

338

AgNPs in different concentrations of Cl−. The photochemical dissolution rates of AgNPs

339

dispersed in the presence of 0.01 M, 0.1 M, and 0.5 M Cl− with SOD were 1.3-, 1.4-, and

340

1.7-fold higher than those without SOD, respectively. The fitted values of [Ag+] max for

341

AgNPs in the presence of 0.01 M, 0.1 M, and 0.5 M Cl− with SOD were 1.2-, 1.6-, and

342

1.2-fold higher than those without SOD, respectively. O2•− could reduce Ag+ to its metallic Ag

343

and decrease the dissolution rate of AgNPs exposed to natural sunlight.50 As O2•− scavenger,

344

SOD could consume O2•−, decrease the reduction rate of dissolved silver ions, and

345

subsequently increase the dissolution rate of AgNPs exposed to UV light. Thus, the

346

photogenerated O2•− should be responsible for the inhibition effect of UV light on the

347

dissolution of AgNPs compared to those in the dark. Similarly, the photogeneration of O2•−

348

from the phenol group of dissolved organic matter was reported to reduce Ag+ to its metallic

349

Ag and decrease the dissolution rate of AgNPs exposed to natural sunlight.51

350 351 352

Table 2. Correlation coefficients (R2) and fitting parameters for AgNP dissolution kinetics dispersed in different chloride concentrations in the presence of ROS scavengers under UV irradiation. Scavengers

Cl− concentration (M)

OF

k (h-1)

[Ag+]max (µg/L)

R2

SOD

0.01

0.45

0.040

39.2

0.99

0.1

0.26

0.055

143.4

0.86

0.5

0.11

0.081

130.9

0.98

0.01

0.40

0.031

30.3

0.85

0.1

0.13

0.041

100.8

0.98

0.5

0.20

0.047

102.4

0.94

t-BuOH

353

Effect of Cl− on Toxicity of AgNPs under UV-365 Irradiation. E. coli cells were

354

selected as model bacteria to assess the effect of Cl− concentration on the toxicity of AgNPs

355

in the dark or under UV irradiation. As shown in Figure 5a, the bacteria viability is decreased

356

by AgNPs alone in the dark with the 6-h survival rate (log(Nt/N0) of -0.2. The addition of 0.01

357

M Cl− did not induce significant toxicity toward bacteria in the dark with a 6-h survival rate 15



358

less than -0.1. Higher concentrations of Cl− (0.1 or 0.5 M) significantly increased the toxicity

359

of AgNPs toward E. coli cells in the dark (p < 0.05) compared to AgNPs alone. The toxicity

360

of AgNPs toward E. coli cells with different concentrations of Cl− in the dark decreased in the

361

order of 0.5 M > 0.1 M > 0 M > 0.01 M, which was consistent with the order of the released

362

concentrations of silver ions. The viability of E. coli cells after exposure to AgNO3 at the

363

same concentration of Ag+ released by AgNPs with or without Cl− was investigated in the

364

dark. The 6-h survival rates of bacteria after exposure to AgNO3 regardless of Cl− were at

365

least 1.8-fold higher than AgNPs. This result implies that the bactericidal activity of AgNPs

366

dispersed in the NaCl solutions in the dark was primarily because of the size effect of NPs

367

and dissolved silver ions, which strongly bind and inactivate sulfur-containing proteins and

368

phosphate-containing DNA. Notably, this is in good agreement with most toxicity assessment

369

literature that has attributed the antibacterial activity of AgNPs to both NPs and dissolved

370

Ag,13, 52, 53 although the relative importance varies significantly. Similarly, some previous

371

work has also demonstrated that low concentrations of Cl− mitigate the toxicity of AgNPs

372

primarily through the formation of AgCl, while higher concentrations of Cl− enhanced the

373

toxic effect of AgNPs due to the generation of soluble AgClx1-x.13, 26

374

A comparison between parts (a) and (b) of Figure 5 shows that the toxicity of AgNPs

375

under UV irradiation is higher than that in the dark with statistical significance (p < 0.05).

376

This is primarily due to the higher ion release rate and more ROS generation concentrations

377

in AgNP suspensions under UV irradiation. As shown in Figure 5(b), the addition of 0.1 or

378

0.01 M Cl− caused a statistically significant decrease (p < 0.05) in the bacterial death rates by

379

26.0% or 40.2%, respectively. However, the addition of 0.5 M Cl− caused a statistically

380

significant increase (p < 0.05) in the bacterial death rates under UV irradiation by about

381

15.2% compared to AgNPs alone. The toxicity of AgNPs toward E. coli cells with different

382

concentrations of Cl− under UV irradiation followed the order of 0.5 M > 0 M > 0.1 M > 0.01 16


Page 16 of 25

Page 17 of 25


383

M. This was inconsistent with that of dissolved Ag concentrations (0.5 M > 0.1 M > 0 M >

384

0.01 M), which indicated that ROS generation and the NP size effect also played significant

385

role in the photoinduced toxicity of AgNPs with Cl−. As discussed above, higher

386

concentrations of Cl− (≥ 0.1 M) resulted in the formation of more •OH and soluble AgClx1-x

387

species in aqueous suspension of AgNPs exposed to UV light. The generation concentration

388

of O2•− in AgNP suspensions changed slightly when Cl− concentrations were higher than 0.1

389

M. Thus the toxicity of AgNPs toward bacteria could be increased in higher than 0.5 M NaCl

390

solution under UV irradiation.

391

As demonstrated in the “Generation Kinetics of ROS” section, the total ROS

392

concentration generated by AgNPs without Cl− was lower than in 0.01 M NaCl solution, but

393

the dissolved silver concentration of AgNPs without Cl− was higher than in 0.01 M NaCl

394

solution. The higher toxicity of AgNPs without Cl− than in 0.01 M NaCl solution indicates

395

that the dissolved silver plays a more significant role in the toxicity than ROS. The toxicity of

396

AgNO3 solutions at the same Ag+ concentration as those released from AgNPs dispersed in

397

different concentrations of NaCl solutions was investigated under UV irradiation. As shown

398

in Figure S4, for each Cl− concentration, the toxicity of AgNO3 is lower than that of AgNPs

399

under UV irradiation. This indicates that other factors, such as ROS, also play an important

400

role in the photoinduced toxicity of AgNPs.

401

As a comparison, when AgNPs in 0.1 M NaCl solution were placed in the dark, the

402

toxicity of AgNPs toward E coli cells was similar to the results under UV irradiation (p >

403

0.05). As previously discussed, AgNPs in 0.1 M NaCl solution released less silver ions under

404

UV irradiation than in the dark, but generated more ROS under UV irradiation. The combined

405

effect of 0.1 M Cl− on ROS generation and ion release potentially caused minor changes to

406

the toxicity of AgNPs. At other concentrations of Cl−, UV irradiation significantly enhanced

407

the toxicity of AgNPs compared to that in the dark (p < 0.05). The UV-induced toxicity 17



408

increase of AgNPs compared to that in the dark was due to their enhanced ROS generation

409

concentrations.20, 27

410 411 412

Figure 5. The effect of different concentrations of NaCl on the toxicity of AgNPs (a) in the dark or (b) under UV irradiation (other conditions were the same as in Figure 1).

413

To assess the effect of Cl− concentrations on the bacterial membrane structure of E. coli

414

cells upon exposure to AgNPs, the leakage of nucleic acids was measured in the dark or

415

under UV irradiation. As shown in Figure S3, the absorbance at 260 nm increased when E.

416

coli cells were treated with AgNPs in the dark or under UV irradiation after extending the

417

reaction time. This indicates that the bacterial cell membranes were ruptured and the

418

intracellular substances (e.g., nucleic acid) were released. In the dark, the amount of released

419

nucleic acid from E. coli upon exposure to AgNPs dispersed in different concentrations of

420

NaCl solutions followed the order of 0.5 M > 0.1 M > 0 M > 0.01 M, which was consistent

421

with the bacterial death rates. Similarly, during the 6-h UV irradiation, the order of membrane

422

disruption of E. coli cells treated by AgNPs dispersed in different concentrations of NaCl

423

solutions was consistent with that of bacterial death rates. In conclusion, our results showed

424

that the exposure to AgNPs resulted in cell membrane rupture and subsequent bacterial

425

apoptosis of E. coli cells under UV irradiation.

426

Environmental Implications. In this study, the concentration of Cl− was found to

427

strongly affect the release of soluble Ag, ROS generation, and toxicity of AgNPs with 18


Page 18 of 25

Page 19 of 25


428

exposure to UV light. Nevertheless, in prior work, the effects of inorganic ligands (e.g., Cl−)

429

on environmental behavior and toxicity of AgNPs has not been properly considered. Our

430

result indicated that a small amount of Cl− (0.01 M, Cl/Ag ratios of 5×103) resulted in the

431

generation of AgCl layers on NP surface, which significantly decreased the photochemical

432

dissolution rate of AgNPs. However, when the Cl− concentrations was higher than 0.1 M

433

(Cl/Ag ratios of 5×104), the photochemical dissolution rate of AgNPs increased primarily due

434

to the formation of soluble Ag-Cl complexes (AgClx1-x).13 Previous works have reported that

435

the Cl/Ag ratios in river and seawater were in the range of 105 and 108,13, 54 respectively. Thus

436

it is most likely that no solid AgCl is expected to form under these “natural” aquatic

437

conditions. The formation of soluble AgClx1-x species will increase the hazardous effect of

438

AgNPs in any environmental waters.11 In summary, inorganic cations or anions should be

439

well accounted when elucidating the toxic mechanisms of AgNPs.

440

Many other constituents (such as Ca2+, K+, Mg2+, HCO3−, NO3−, and NOM) could also

441

affect the environmental behavior and toxicity of AgNPs in natural waters.33,

442

example, CaCl2 was demonstrated to be more efficient in destabilizing citrate-coated AgNPs

443

than NaCl because Ca2+ was more efficient in neutralizing the surface charge of AgNPs

444

through interactions with the carboxyl groups of citrate molecules.24, 37 The irradiation of

445

NOM could transfer energy and electron to NPs and affect their ROS generation

446

concentration and toxicity.33,

447

subsequently affects the dissolution rate and toxicity of AgNPs.16,

448

assessment of AgNPs should consider their possible interactions with other coexisting

449

constituents, which is an important but highly challenging problem and will be investigated in

450

our further works.

451

ASSOCIATED CONTENT

452

Supporting Information Available

55

37, 55

For

NOM could complex with the dissolved silver ions and

19


56

Therefore, the risk


453

The supporting information includes details about aggregation kinetics of AgNPs with

454

or without Cl−, 1O2 generation kinetics of AgNPs with or without Cl−, effect of ROS

455

scavenger on dissolution kinetics of AgNPs with or without Cl−, the t-test analysis of AgNPs

456

toxicity toward E. coli cells with or without Cl−, toxicity of AgNO3 toward E. coli cells with

457

or without Cl−, and nucleic acid released from E. coli cells exposed to AgNPs with or without

458

Cl−. This material is available free of charge via the Internet at http://pubs.acs.org.

459

ACKNOWLEDGMENTS

460

The study was financially supported by the National Key R&D Program of China

461

(2017YFA0605001), National Natural Science Foundation of China (Nos. 21407010 and

462

21677015), Fund for Innovative Research Group of the National Natural Science Foundation

463

of China (No. 51421065), the National Science Fund for Distinguished Young Scholars (No.

464

51625801), and the Fundamental Research Funds for the Central Universities. The authors

465

also appreciate support from the Brook Byers Institute for Sustainable Systems, the

466

Hightower Chair, and the Georgia Research Alliance at Georgia Institute of Technology.

467 468

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469 470 471 472 473 474 475 476 477 478 479 480

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