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Jaehwan Seo • Soyoun Kim • Seona Choi •. Dongwook Kwon • Tae-Hyun Yoon • ... online: 26 July 2014. Ó Springer Science+Business Media New York 2014.
Bull Environ Contam Toxicol (2014) 93:257–262 DOI 10.1007/s00128-014-1337-z

Effects of Physiochemical Properties of Test Media on Nanoparticle Toxicity to Daphnia magna Straus Jaehwan Seo • Soyoun Kim • Seona Choi • Dongwook Kwon • Tae-Hyun Yoon • Woo-Keun Kim • June-Woo Park • Jinho Jung

Received: 15 July 2013 / Accepted: 14 July 2014 / Published online: 26 July 2014 Ó Springer Science+Business Media New York 2014

Abstract The physicochemical property of standard test media significantly influenced the aggregation and dissolution of Ag, CuO and ZnO nanoparticles (NPs) and the toxicity of the NPs to Daphnia magna. For all the NPs, the highest amount of metal ions was released from the ISO medium, whereas acute toxicity to D. magna was highest in the moderately hard water medium (EC50 = 4.94, 980, and 1,950 lg L-1 for Ag, CuO, and ZnO, respectively). By comparing EC50 values based on the total and dissolved concentrations of NPs with those of metal salt solutions, we found that both particulate and dissolved fractions were likely responsible for the toxicity of Ag NPs, whereas the dissolved fraction mostly contributed to the toxicity of CuO and ZnO NPs. Keywords Acute toxicity  Copper  Daphnia magna  Nanotoxicology  Silver  Zinc Metal and metal oxide nanoparticles (NPs), including silver (Ag), copper oxide (CuO), and zinc oxide (ZnO), are widely used in different areas such as the chemical industry, electronics, biomedicine, and cosmetics (Klaine et al. 2008). Thus, these NPs inevitably enter the

J. Seo  S. Kim  S. Choi  J. Jung (&) Division of Environmental Science and Ecological Engineering, Korea University, Seoul 136-713, Republic of Korea e-mail: [email protected] D. Kwon  T.-H. Yoon Department of Chemistry, Hanyang University, Seoul 133-791, Republic of Korea W.-K. Kim  J.-W. Park Ecotoxicology Research Center, Korea Institute of Toxicology, Daejeon 305-343, Republic of Korea

environment to cause significant adverse effects on aquatic organisms (Nowack and Bucheli 2007). For these reasons, many studies have generated acute and chronic toxicity data for NPs using standardized testing methods recommended by the International Organization for Standardization (ISO), Organization for Economic Co-operation and Development (OECD), and the US Environmental Protection Agency (USEPA; Garcia et al. 2011). However, despite the usefulness of the standard test methods for toxicity assessment of traditional chemical compounds, concerns have been raised regarding the different toxicity results, mainly due to the different colloidal stability of NPs in various test media (El Badawy et al. 2010). In addition, several studies showed that the relative contribution of dissolved and particulate fractions of NPs to aquatic toxicity were greatly dependent on particle size (Heinlaan et al. 2008), coating materials (Tejamaya et al. 2012), and test media (Romer et al. 2011). Only a few studies have investigated the stability of metal oxide NPs under different conditions of the test media. Romer et al. (2011) demonstrated that Ag NPs aggregate rapidly in the OECD test media with high ionic strength, and thus recommended a tenfold dilution of the media to reduce the aggregation. Tejamaya et al. (2012) also reported that citrate, PVP, and PEG-coated Ag NPs are stable in a tenfold diluted OECD media over 21 days. In addition, dissolution of NPs plays an important role in determining the toxicity of NPs (Keller et al. 2010; Chang et al. 2012). Several studies demonstrated that physicochemical characteristics of water, such as pH, dissolved organic carbon, ionic strength, and hardness, greatly influenced the solubility and toxicity of NPs (Hoecke et al. 2011; McLaughlin and Bonzongo 2012; Li et al. 2013). For instance, Li et al. (2013) reported that increasing concentrations of Ca2?, Mg2?, and HPO42- reduced the release of

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Table 1 Composition and chemical properties of the test media used in this study MHW

HW

ISO

64

Composition (mg L-1) NaHCO3

96

192

CaSO42H2O

60

120

60

120

CaClH2O MgSO4

294

MgSO47H2O KCl Chemical properties

120 4

8

5.75

pH

7.5

7.8

7.8

Ionic strength (mM)

6.87

10.39

12.83

Hardness (mg L-1 as CaCO3)

100

170

250

free Zn2? from ZnO NPs, and thus dramatically lowered the toxicity to Escherichia coli. These findings suggest that the characteristics of the test media greatly affect the toxicity results for NPs by changing the colloidal stability and solubility of these particles. However, previous studies have been limited to evaluate the change of toxicity using different types of NPs in various standard test media. Thus, this study aimed to investigate the effect of test media on the physicochemical properties of Ag, CuO, and ZnO NPs and on the corresponding change in the toxicity of the NPs toward the freshwater crustacean Daphnia magna.

Methods and Materials Ag NPs (99.98 %, SARPU 200KW) were purchased from ABC Nanotech (Daejeon, Korea). It was a water-based colloid containing 20.48 % Ag NPs (5–25 nm) and 1.0 % citrate as the capping agent (Asghari et al. 2012). CuO (99.0 %, Cat No. 44663) and ZnO (99.0 %, Cat No. 44533) NPs were obtained from Alfa Aesar (Ward Hill, USA). They were supplied as dry powder, and the particle sizes of CuO and ZnO NPs reported by the manufacture were 30–50 and 20–30 nm, respectively. Test media for physicochemical and toxicity testing were prepared following the USEPA standard method using moderately hard water (MHW) and hard water (HW) media (USEPA 2002), and the OECD-recommended ISO test medium (OECD 2004). The composition and chemical properties of the test media used in this study are given in Table 1. For comparison, NPs were also prepared in deionized water (DW) with a resistivity of 18.2 MX cm-1 (Puris, Esse-UP Water System; Mirae St Co., Korea). In addition, metal solutions were prepared by dissolving metal salts in the test media. Copper nitrate (Cu(NO3)23H2O, 99 %) and silver nitrate

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(AgNO3, 99.9 %) were purchased from Junsei Chemical (Japan) and Kojima Chemicals (Japan), respectively. Zinc chloride (ZnCl2, 99.5 %) was obtained from SigmaAldrich (USA). Prior to toxicity testing, the NP suspensions were sonicated for 30 min using a bath ultrasonicator (400 W; Power Sonic 420; Seoul, Korea) at a frequency of 40 kHz. Acute toxicity tests using D. magna were conducted according to the OECD standard procedures (OECD 2004). Daphnids were grown in the laboratory in Elendt M4 medium at 20 ± 2°C with a 16-h light and 8-h dark photoperiod. Each toxicity test consisted of six dilutions of NPs and one control with four replicates per treatment, and each test vessel contained 10 mL of the test solution and five neonates (B24 h old). Six concentrations were: 100, 50.0, 25.0, 12.5, 6.25, and 3.13 lg L-1 for Ag NPs; 20.0, 10.0, 5.00, 2.50, 1.25, and 0.63 mg L-1 for CuO NPs; 25.0, 12.5, 6.25, 3.13, 1.56, and 0.78 mg L-1 for ZnO NPs. Dilution and control water (pH = 7.8 ± 0.1 and hardness = 250 ± 25 mg L-1 as CaCO3) were prepared as described by the International Organization for Standardization (ISO 2012). Toxicity tests were conducted at 20 ± 2°C with a 16-h light and 8-h dark photoperiod for 48 h, and immobilization (defined as no response to gentle agitation) of the test species was determined. Immobilization was also used to calculate the EC50 (median effective concentration) values using the trimmed Spearman-Karber method (USEPA 2002). Standard reference toxicity tests were conducted with K2Cr2O7 in between the tests and compared with a control chart. The morphology of NPs in the suspensions was analyzed by transmission electron microscopy (TEM; H-760, Hitachi, Japan). Hydrodynamic size and zeta potential of NPs were also measured using dynamic light scattering method (DLS; Scatteroscope I, Qudix, Korea) and a ZetaPALS Analyzer (Brookhaven Instruments, USA), respectively. In addition, dissolution of NPs in the test media was measured after the 48-h acute toxicity test. Five hundred microliters of NP suspensions were centrifuged with 100-kDa centrifugal filters (regenerated cellulose; Amicon Ultra-0.5; Millipore, USA) to remove NPs. In the concentration range used in this study, 76.1 ± 11.9, 92.8 ± 6.9, and 93.5 % ± 2.1 % of Ag, Cu, and Zn ions, respectively, were recovered after the centrifugation. Metal concentrations in the supernatant were analyzed using an inductively coupled plasma-optical emission spectrophotometer (ICPOES; Varian Vista PRO, USA) and an inductively coupled plasma-optical mass spectrometer (ICP-MS; Varian Vista PRO, USA). Detection limit of the ICP-OES for Zn is 1 lg L-1, and detection limits of the ICP-MS for both Ag and Cu are less than 1 ng L-1. Standard solutions were freshly prepared, and standard calibration curves with r2 [ 0.995 were achieved daily.

Bull Environ Contam Toxicol (2014) 93:257–262

259

Fig. 1 TEM images of a Ag, b ZnO, and c CuO NPs in deionized water (pH 6.5 ± 0.2)

MHW

HW

ISO

Ag

-34.3 ± 4.0

-22.5 ± 1.2

-19.5 ± 3.2

-14.4 ± 1.7

CuO

?15.5 ± 0.7

-5.7 ± 0.2

-14.5 ± 0.5

?0.3 ± 0.6

ZnO

?19.8 ± 0.7

?1.7 ± 0.3

-8.1 ± 0.2

?3.9 ± 0.4

All statistical analyses were performed using SAS software version 9.4 (SAS Institute, USA). Significant differences were determined by analysis of variance (ANOVA) followed by Dunnett’s test (p \ 0.05).

Results and Discussion The primary particle sizes of Ag, CuO and ZnO NPs determined from their TEM images using Image J program (National Institute of Health, USA) were 9.5 ± 3.9, 31.3 ± 15.0, and 22.9 ± 4.7 nm, respectively (Fig. 1). However, the hydrodynamic particle sizes of NPs in different test media after 48-h exposure could not be confirmed by DLS measurements, due to low exposure concentrations and significant aggregation during toxicity testing. Considering that NPs having a zeta potential larger than -30 mV are found to be unstable (Jo et al. 2012), the aggregation of NPs seemed to have occurred in all test media except for Ag NPs (Table 2). The Ag NPs showed negative potentials high enough to be stable in DW and MHW media. Asghari et al. (2012) also reported that the citrate-coated Ag NPs remained very stable in the M4 medium. Several studies suggest that different water chemistry (pH, ionic strength, hardness, etc.) of the test media greatly influence the aggregation of NPs. Changes in pH can lead to the neutralization of surface charge at the point of zero charge of NPs, and an increase in ionic strength may

8

Dissolved concentration (µg L-1)

DW

MHW 6

ISO HW

4

2

0 0

20

40

60

80

100

120

Concentration of Ag (µg L-1)

(b) Dissolved concentration (µg L-1)

NPs

(a)

100

MHW ISO

80

HW

60 40 20 0 0

5

10

15

20

25

Concentration of CuO (mg L-1)

(c) Dissolved concentration (mg L-1)

Table 2 Zeta potential (mV) of nanoparticles in different test media (n = 3)

5

MHW 4

ISO HW

3 2 1 0 0

5

10

15

20

25

30

Concentration of ZnO (mg L-1) Fig. 2 Dissolved concentrations of a Ag, b CuO, and c ZnO NPs in different test media after 48-h exposure

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Bull Environ Contam Toxicol (2014) 93:257–262

(a)

Immobilization (%)

120 100 80 60

MHW ISO

40

HW 20 0 0

20

40

60

80

Concentration of Ag (µg

(b)

100

120

L-1)

Immobilization (%)

120 100 80 60

MHW ISO

40

HW 20 0 0

5

10

15

20

25

Concentration of CuO (mg L-1)

(c) 120

Immobilization (%)

100 80 60

MHW 40

ISO HW

20 0 0

5

10

15

20

25

30

Concentration of ZnO (mg L-1) Fig. 3 Dose-response curves of acute toxicity (48 h) of a Ag, b CuO, and c ZnO NPs in different test media toward Daphnia magna

constrict the electrostatic double layer and reduce the repulsive forces among NPs, both of which result in a greater aggregation (Hotze et al. 2010). In addition, several types of cation, including Ca2? and Mg2?, can bridge functional groups on the surface of NPs and accelerate the formation of aggregates (Zhang et al. 2009; Hotze et al. 2010; Chae et al. 2012). As indicated in Table 1, the MHW medium has the lowest values of ionic strength and hardness, suggesting that the aggregation of NPs may be least in the MHW medium. Considering that D. magna is able to feed on

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particle sizes of 400–4,000 nm (Tan et al. 2012), the size of aggregates may influence the toxicity of NPs toward D. magna. McLaughlin and Bonzongo (2012) demonstrated that differences in natural water chemistry (ionic strength/ dissolved organic carbon ratio) changed the particle size of Ag NPs, which resulted in a change in toxicity to aquatic organisms. The dissolution of Ag, CuO, and ZnO NPs in different test media after 48-h exposure is shown in Fig. 2. Generally, the highest amount of metal ions was released from the ISO medium for all NPs, and ZnO NPs were the most soluble. Blinova et al. (2010) reported that ZnO NPs were much more soluble than CuO NPs. In addition, Reed et al. (2012) demonstrated that the solubility of ZnO NPs was lower in the MHW medium compared to that in nanopure water due to the precipitation of a zinc carbonate solid phase. This result indicates that ZnO NPs have highest solubility in the ISO medium that contains the lowest bicarbonate concentrations among the three test media (Table 1). Acute toxicity of Ag, CuO, and ZnO NPs toward D. magna after 48-h exposure was compared in different test media (Fig. 3). Regardless of NPs, acute toxicity was found to be highest in the MHW medium (EC50 = 4.94, 980, and 1,950 lg L-1 for Ag, CuO, and ZnO, respectively) followed by the ISO medium, and the lowest toxicity was observed in the HW medium. This result is not fully explained by the solubility of NPs in the test media since the dissolved fraction of NPs was highest in the ISO medium (Fig. 2). These findings suggest that both dissolved ions and particles may be responsible for the observed toxicity. The median effective concentration (EC50) was calculated with the total and dissolved concentrations of NPs in different test media, and compared with that of metal salt solutions (Table 3). All NPs showed the highest acute toxicity to D. magna in MHW medium (p \ 0.05). This may be due to the fact that relatively greater aggregation were occurred in the HW and ISO media because their hardness and ionic strength values were higher compared to the MHW medium (Table 1). Romer et al. (2011) reported that Ag NPs aggregate rapidly in the OECD test media with increasing ionic strength, resulting in decrease of their acute toxicity to D. magna. In addition, increasing hardness and ionic strength may decrease the metal ion toxicity through competition, complexation, and reduction of ionic activity (Jo et al. 2010). The acute toxicity of Ag NPs based on total concentration (EC50 = 4.94 lg L-1) was quite similar to the toxicity of AgNO3 (EC50 = 4.68 lg L-1) in the MHW test medium (Table 3; p [ 0.05). In addition, acute toxicity of Ag NPs based on dissolved concentration was much higher than that of AgNO3 (p \ 0.05). Even considering the loss

Bull Environ Contam Toxicol (2014) 93:257–262 Table 3 Comparison of EC50 (lg L-1) values based on total and dissolved concentrations of nanoparticles and metal salts in different test media

NPs

Medium

Ag

MHW HW

CuO A,B,C

a,b,c

Significant difference (p \ 0.05) among total NPs, dissolved NPs, and metal salts

EC50 (median and 95 % confidence interval) Total NPs

ISO

Significant difference (p \ 0.05) among MHW, ISO, and HW treatments

261

4.94 (4.07–6.00)Aa 45.06 (38.16–53.21)

Ca

63.73 (56.81–71.49) Aa

780 (520–1,840)

ISO

1,730 (1,630–2,870)ABa

MHW ISO HW

2.17 (1.77–2.65)

3,710 (2,930–5,690) 1,570 (1,470–2,590)

Aa

3,120 (3,190–4,980)

Ba Ca

8,220 (7,840–13,380)

4.68 (3.53–6.08)Aa

Bb

2.51 (2.28–2.77)

9.73 (7.47–12.69)Bc

Bb

13.17 (8.19–21.16) Ba

of Ag ions after the centrifugal filtration (recovery was 76.1 % ± 11.9 %), dissolved concentrations of Ag NPs in the test media (Fig. 2) were still lower than the corresponding EC50 values of AgNO3. These findings suggest that particles as well as dissolved ions are the likely causes of the acute toxicity of Ag NPs toward D. magna in this study. Griffitt et al. (2008) demonstrated that Ag ions released from nanosilver were not enough to cause acute toxicity to Daphnia pulex, indicating that the observed toxicity of nanosilver may not be attributable solely to dissolved ions. In addition, Poynton et al. (2012) reported that Ag NPs disrupted different biological processes in D. magna that were distinct from ones caused by Ag ions. However, several studies demonstrated that Ag NPs toxicity to D. magna likely occurred through Ag ions released from the particles (Jo et al. 2010; Zhao and Wang 2012). These suggest that both particles and ions are attributable to the observed toxicity of Ag NPs, which may largely depend on the type of surface coatings and test species (Zhao and Wang 2011; Das et al. 2013). In the case of CuO NPs, EC50 values based on dissolved concentration of NPs were not significantly different from those based on Cu(NO3)2 in both MHW and HW media (p [ 0.05), possibly due to higher dissolved concentrations of CuO NPs in the test media (Fig. 2) than the corresponding EC50 values of Cu(NO3)2. Heinlaan et al. (2008, 2011) reported that the toxicity of bulk CuO to D. magna was mainly attributed to the dissolved Cu ions whereas the soluble fraction of the CuO NPs explained only a part of the toxicity. In addition, Jo et al. (2012) suggested that the acute toxicity of CuO NPs to D. magna was well explained by their dissolved concentrations varying with preparation methods. Similar to the result of CuO NPs, the acute toxicity of ZnO NPs based on dissolved concentration was not significantly different from that of ZnCl2, regardless of the test media (p [ 0.05). This result can be explained by the fact that ZnO NPs showed greater extent of dissolution in test

Metal salts

0.24 (0.17–0.38)Ab Ba

MHW HW

ZnO

Dissolved NPs

12.08 (9.96–14.65)Bc

Ab

17.42 (14.33–21.19)Ab

50.48 (44.65–55.53)Bb

29.73 (26.00–34.00)Bc

Cb

31.86 (26.02–39.02)Bb

38.83 (30.20–37.80) Ab

480 (390–590)Ab

680 (520–870)

Bb

1,000 (790–1,260)Bb

Bb

1,230 (950–1,600)Bb

1,350 (1,120–1,620) 1,230 (1,090–1,250)

media compared to other NPs (Fig. 2). Heinlaan et al. (2008) reported that dissolved Zn ions were responsible for the toxicity of bulk and nano ZnO to D. magna. In addition, Li et al. (2013) demonstrated that the toxicity of ZnO NPs to E. coli depended on free Zn ions released from ZnO NPs. These findings suggest that the dissolved metal ions mainly contributed to the acute toxicity of CuO and ZnO NPs. In conclusion, acute toxicity of Ag, CuO, and Zn NPs toward D. magna was highest in the MHW medium although metal ion release from the NPs was highest in the ISO medium, indicating that both particulate and dissolved fractions of NPs were responsible for the observed toxicity. The contribution of particulates to the toxicity appeared to be substantial in the case of Ag NPs, whereas in CuO and ZnO NPs, the dissolved fractions mostly explained the observed toxicity. However, the relative contribution of particles and metal ions may largely dependent on several factors including particle size and coating materials of NPs, the presence of complexing ligands, feeding type of test species. Thus, the underlying mechanism of NPs toxicity should be further investigated by evaluating particle size distribution of NPs, aqueous speciation of released metal ions, and their toxicokinetics in test species. Acknowledgments This study was supported by the research project for Environmental Risk Assessment of Manufactured Nanomaterials (KK-1303-03) funded by the Korea Institute of Toxicology (KIT, Korea), and by Korea Ministry of Environment as ‘‘Climate Change Correspondence Program’’. The authors would like to thank anonymous reviewers for their valuable comments.

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