Article pubs.acs.org/est
Reducing Environmental Toxicity of Silver Nanoparticles through Shape Control Danielle E. Gorka,†,‡ Joshua S. Osterberg,†,§ Carley A. Gwin,†,∥ Benjamin P. Colman,†,⊥ Joel N. Meyer,†,§ Emily S. Bernhardt,†,⊥ Claudia K. Gunsch,†,∥ Richard T. DiGulio,†,§ and Jie Liu*,†,‡ †
Center for the Environmental Implications of NanoTechnology (CEINT), Duke University, P.O Box 90287, Durham, North Carolina 27708, United States ‡ Department of Chemistry, Duke University, Durham, North Carolina 27708, United States § Nicholas School of the Environment, Duke University, Durham, North Carolina 27708, United States ∥ Department of Civil and Environmental Engineering, Duke University, Durham, North Carolina 27708, United States ⊥ Department of Biology, Duke University, Durham, North Carolina 27708, United States S Supporting Information *
ABSTRACT: The use of antibacterial silver nanomaterials in consumer products ranging from textiles to toys has given rise to concerns over their environmental toxicity. These materials, primarily nanoparticles, have been shown to be toxic to a wide range of organisms; thus methods and materials that reduce their environmental toxicity while retaining their useful antibacterial properties can potentially solve this problem. Here we demonstrate that silver nanocubes display a lower toxicity toward the model plant species Lolium multif lorum while showing similar toxicity toward other environmentally relevant and model organisms (Danio rerio and Caenorhabditis elegans) and bacterial species (Esherichia coli, Bacillus cereus, and Pseudomonas aeruginosa) compared to quasi-spherical silver nanoparticles and silver nanowires. More specifically, in the L. multif lorum experiments, the roots of silver nanocube treated plants were 5.3% shorter than the control, while silver nanoparticle treated plant roots were 39.6% shorter than the control. The findings here could assist in the future development of new antibacterial products that cause less environmental toxicity after their intended use.
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INTRODUCTION Silver is the most widely used nanomaterial due to its antibacterial properties, and silver nanomaterials (AgNMs) are found in a variety of consumer goods including athletic clothing, toys, food storage containers, and wound dressings.1−4 Due to their simple synthesis methods and antibacterial properties, spherical silver nanoparticles (AgNPs) are the most studied silver nanomaterial, while other shapes of AgNMs are being increasingly used in other applications. For example, enhanced optical properties allow silver nanocubes (AgNCs) to be used as a substrate for surface-enhanced Raman scattering, and the enhanced electronic properties of silver nanowires (AgNWs) allow them to be used in transparent conducting thin films, interconnects, and sensors.5−7 Although much work has gone into studying the toxicity of AgNMs, little work has gone into examining shape-based toxicity. AgNMs are leached from consumer goods when washed, with the majority of this released silver expected to enter wastewater treatment plants and ultimately the environment.8,9 Increased use of AgNMs in consumer goods will drive increased release of silver nanomaterials into the environment. © 2015 American Chemical Society
After entrance into the environment, these released silver nanomaterials can cause toxicity to plants, terrestrial and aquatic organisms, and bacteria. Thus, these nanomaterials need to be studied in greater detail to determine if any environmental toxicity will occur after either accidental or incidental release. As silver nanoparticles with different shapes are being increasingly used in consumer products, these materials too need to be studied to determine if they will cause environmental toxicity. To investigate whether the shape affects the toxicity in environmentally relevant and model organisms, we studied the toxicity of three differently shaped AgNMs to the following organisms: a commonly studied wetland grass (Lolium multif lorum); a model fish (Danio rerio); a model terrestrial nematode (Caenorhabditis elegans); and three different environmentally relevant bacterial species (Esherichia coli, Bacillus cereus, Pseudomonas aeruginosa). In Received: Revised: Accepted: Published: 10093
April 5, 2015 June 18, 2015 July 6, 2015 July 6, 2015 DOI: 10.1021/acs.est.5b01711 Environ. Sci. Technol. 2015, 49, 10093−10098
Article
Environmental Science & Technology Table 1. Size, Concentration, and Surface Area of AgNMs at 100 ppm Aga sample AgNP AgNC AgNW
size (nm) 44.1 36.6 L: 82.2 W: 6755
± ± ± ±
7.0 5.7 17.3 3441
concentration (particles/mL)
surface area (cm2/mL)
2.12 × 10 ± 1.44 × 10 1.94 × 1011 ± 1.29 × 1011 3.18 × 108 ± 1.04 × 109
13.0 ± 2.44 15.6 ± 2.88 5.48 ± 2.47
11
11
a
Sizes are defined as diameter (AgNP), edge length (AgNC), and length and width (AgNW). AgNPs and AgNCs had similar sizes, concentrations, and surface area. AgNWs had a larger size and lower concentration, however surface area is within one order of magnitude. Note: error indicates standard deviation.
Nanomaterial Characterization. The size and morphology of the nanomaterials was determined using transmission electron microscopy (TEM), X-ray diffraction (XRD), and UV−vis absorption spectroscopy. The size of the nanomaterials was determined using a Tecnai G2 Twin transmission electron microscope (TEM, FEI, Hillsboro, OR, U.S.A.) at 160 kV. Samples for TEM were prepared by placing several drops of sample solution on a Formvar carbon coated grid (300 mesh, Ted Pella), allowing it to sit for 5 min, followed by wicking away excess solution. X-ray diffraction (XRD) data was acquired using an X’Pert PRO MRD HR diffractometer (PANalytical, Westborough, MA, U.S.A.) with a Cu Kα source at 5 kV and 40 mA between 20 and 80° 2θ. Samples were prepared by placing 50 drops of sample solution onto a glass microscope slide and allowing it to dry. UV−vis absorption spectra were collected using a Varian Cary 50 Conc spectrophotometer (UV−vis, Agilent, Santa Clara, USA) and a quart cuvette. Scans were collected in the absorbance mode between 800 and 300 cm−1. The nanomaterial size was determined by uploading representative TEM images into ImageJ (National Institutes of Health, Bethesda, MD, U.S.A.) and using the measure function on at least 100 individual particles per nanomaterial shape. The size listed in Table 1 indicates the diameter of AgNPs, the edge length of AgNCs, and the diagonal of AgNWs, as well as the AgNW length. Nanomaterial concentration and surface area were determined at a silver concentration of 100 ppm by assuming AgNPs were perfect spheres, AgNCs were perfect cubes, and AgNWs were perfect pentagonal prisms with flat ends.13 Additionally, the bulk density of silver was used in the nanomaterial concentration calculations. Lolium multif lorum. Lolium multif lorum, annual ryegrass, (L. perenne var. italicum, ERNST Seeds, Meadville, PA, U.S.A.) was used for plant toxicity measurements. For each treatment, 5 replicates were performed. For each replicate, a 110 mm filter paper was put into a 150 × 15 mm2 Petri dish and 5 mL of the test solution was added. Twenty-five seeds were placed on each filter paper, evenly spaced at least 1 cm apart. The Petri dish was closed and sealed with Parafilm. The seeds were allowed to germinate for 5 days in ambient laboratory conditions, approximately 20 °C. After the germination period, the root and shoot length were measured with digital calipers. One fresh root from each replicate was examined under light microscopy using a Lumar.V2 Stereomicroscope (Zeiss, Thornwood, NY, U.S.A.) to determine the root morphology. Roots were cut approximately 2 cm above the root tip and fixed to a microscope slide with glycerol. Images were taken at 75× and 150× magnification. The number of root hairs were determined by uploading representative images into ImageJ and counting the number of root hairs on a 1 cm length. Bacterial Tests. Three bacterial strains, B. cereus, E. coli K12, and P. aeruginosa PA01, were used as model organisms to
our study, we discovered that AgNCs show decreased toxicity toward model plants while having similar toxicity to other species compared to AgNPs and AgNWs
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EXPERIMENTAL METHODS Silver Nanomaterial Synthesis. Quasi-spherical silver nanoparticles were prepared by a polyol synthesis methodology modified from Silvert et al.10,11 Briefly, 2 g polyvinylpyrrolidone (PVP, MW 55 kDa, Aldrich) was dissolved in 5 mL ethylene glycol (Ampresco) with stirring. When dissolved, 150 mg silver nitrate (AgNO3, 99.99%, Alfa Aesar) was added and allowed to dissolve. When fully dissolved, the reaction was heated to 145 °C and allowed to react for 24 h. The particles were purified by diluting with acetone and centrifugation, and then resuspended with NanoPure water (18MΩ, Thermo-Scientific) to 10 mL. Silver nanocubes were prepared by a common ethylene glycol synthesis protocol.12 Briefly, 6 mL ethylene glycol was heated at 155 °C for 1 h with stirring. All reagent solutions were prepared in ethylene glycol. After 1 h, 80 μL sodium sulfide (sodium sulfide nonahydrate, 3 mM, 99.99%, Aldrich) was injected. Then 30 mg PVP (1.5 mL, 20 mg/mL) and 24 mg AgNO3 (0.5 mL, 48 mg/mL) were injected sequentially, and the reaction was allowed to proceed for 8 min. The solution turned from colorless to a transparent yellow to an opaque ruddy brown. The particles were purified by diluting with acetone and centrifugation, and then resuspended with NanoPure water to 5 mL. Silver nanowires were prepared by a common polyol synthesis methodology.13 Briefly, 5 mL ethylene glycol was heated at 160 °C for 10 min with stirring and under bubbled nitrogen. After 10 min, the nitrogen was removed and the solvent was heated for 50 min more. All reagents solutions were prepared in ethylene glycol. A 3 mL solution containing 48 mg PVP (144 mM), sodium chloride (220 μM, Fisher), and iron nitrate (iron nitrate nonahydrate, 22 μM, Aldrich) was prepared. A 3 mL solution containing 48 mg AgNO3 (94 mM) was also prepared. Both solutions were injected simultaneously with a syringe pump at a rate of 45 mL/h. The reaction was allowed to proceed for 60 min. The solution turned from colorless to clear yellow to an opaque light brown. The particles were purified by diluting with acetone and centrifugation, and then resuspended with NanoPure water to 10 mL. A 100 ppm dissolved silver solution was prepared by dissolving AgNO3 in NanoPure water. A control solution of 100 ppm PVP was also prepared, which was similar to the concentration of PVP found in the 100 ppm silver solutions. Dissolved silver and PVP solutions were diluted to equal the same concentration of silver nanomaterials in respective toxicity tests. All silver nanomaterials were stored in the dark until use. 10094
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Figure 1. Set of TEM images of silver nanomaterials. (A) Shows spherical silver nanoparticles. (B) Shows silver nanocubes. (C) Shows silver nanowires.
accounting for differences in the measured dimensions (diameter versus edge length, respectively, Table 1). The similarity in sizes between AgNPs and AgNCs corresponds to particle concentrations and total surface areas that are within an order of magnitude at a given silver mass concentration. Due to the large aspect ratio of AgNWs, they have a particle concentration that is 3 orders of magnitude smaller than either AgNPs or AgNCs. However, the surface area of AgNWs is still within an order of magnitude of the surface areas of the other NMs. Due to the similar surface coating and size of the AgNMs (both within an order of magnitude), any toxicity in organisms can be attributed to the shape of the nanomaterial. As AgNMs are likely to leave wastewater treatment plants in sewage sludge and subsequently be added as an amendment to agricultural soil, it is necessary to study their toxicity in plants, like the widely distributed forage grass L. multif lorum. Using a germination test following modified OECD guidelines, toxicity was defined as a decrease in root or shoot length compared to deionized water controls.24−26 When using these criteria, NMs and dissolved silver displayed some toxicity compared to controls (Figure 2) with AgNPs showing significant toxicity to
test the toxicity of variously shaped silver nanomaterials. Cells were grown overnight in LB broth at 37 °C and growth curve experiments were performed at room temperature (25 °C) in triplicate using 96-well plates and a kinetic protocol (Ascent Software v.2.6, Thermo Scientific) for 24 h on a Thermo Multiskan MCC (Thermo Scientific) plate reader. Initially, cells were normalized to an OD of 0.100 at 540 nm to reach a total volume of 200 μL consisting of treatment and bacterial strain of interest. All subsequent readings were also taken at 540 nm. Inhibition in growth was calculated at 24 h by subtracting control cell OD values from treatment OD values, then further dividing by control values. Statistical Analysis. Error reported for nanomaterial size is expressed as standard deviation when n=300, except AgNW diagonal where n = 100. Error reported for L. multif lorum root and shoot growth is expressed as standard deviation. Differences between variables were measured with one-way ANOVA and followed by Tukey’s HSD test when there was a significant difference of p < 0.05 using JMP 11 Pro software (SAS Institute Inc., Cary, NC, U.S.A.). For bacteria ANOVAs were performed in R (v.2.13.1; OD value as a function of treatment). If significance was indicated, then a Tukey’s HSD test was performed and comparisons producing an adjusted p-value ≤0.05 were considered significantly different from each other. Standard deviations for bacterial growth inhibition were calculated in Excel 2010.
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RESULTS AND DISCUSSION In our study, AgNPs, AgNCs, and AgNWs with a polyvinylpyrrolidone (PVP) coating were all synthesized from silver nitrate via commonly used polyol synthesis methodologies (Figure 1).10−13 The methods were chosen so all materials would have the same surface coating, as different surface coatings have been found to affect the toxicity of AgNMs preventing direct comparisons from being made.14 Additionally, surface coatings should display very little toxicity to prevent extraneous toxicity from being associated with the AgNM.15−17 Toxic capping agents such as CTAB may have accounted for some toxicity observed in other work, which has prevented direct comparison between different shapes.18 PVP was chosen as the surface coating in this work as it has been shown to be nontoxic and is confirmed as such by our studies.19 Additionally, PVP can be used for producing different AgNMs with precise shape control.20 To facilitate the comparison of different AgNM shapes on toxicity, size should also be kept consistent to reduce the previously described size-based toxic effects.21−23 In this work, AgNPs and AgNCs were approximately the same size after
Figure 2. L. multif lorum root and show growth for AgNMs. AgNPs were significantly more toxic than all other materials except dissolved silver. While AgNPs and dissolved silver showed significant toxicity in roots, only AgNPs showed significant toxicity toward shoots. Different letters signify differences (p < 0.05).27
both roots and shoots. AgNPs are also the only material that showed significant toxicity in shoots (26.0 versus 33.1 mm for control). Interestingly, dissolved silver showed toxicity in roots similar to that of AgNPs (growth of 21.8 versus 21.5 m, respectively), but significantly less toxicity in shoots (29.6 versus 26.0 mm, respectively). Compared to AgNPs, the other AgNMs showed lower toxicity overall. AgNCs displayed insignificant toxicity toward roots (35.2 versus 36.1 mm for control) and no toxicity in shoots (34.2 versus 33.1 mm for 10095
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attachment, in this case the plant seed and root, which results in high localized concentrations of dissolved silver and the resulting organismal toxicity.4,30 In these plant studies, shape was shown to play a large role in the toxicity of AgNMs to L. multif lorum. While displaying an insignificant amount of toxicity toward both the roots and shoots of L. multif lorum, AgNCs are the least phytotoxic NMs among those tested, suggesting that they will cause less environmental toxicity than other AgNMs. We then tested for shape-based toxicity differences in other species, including the aquatic zebrafish D. rerio, the terrestrial nematode C. elegans, and three bacterial strains to determine if the shape-based toxicity effect was specific to plants or was generalizable to other species. All these species tested showed similar results to one another: AgNMs showed less toxicity to D. rerio and C. elegans than dissolved silver and generally there was little difference among AgNM shapes, suggesting that shape-based toxicity may only be important in plants. More results on the toxicity of AgNMs to D. rerio and C. elegans can be found in the Supporting Information (SI), while toxicity to the three bacterial strains are discussed here. Following a trend similar to that of D. rerio and C. elegans, results in bacterial strains showed that AgNCs have similar toxicity as other AgNMs(Figure 4). Each bacterial strain was incubated in AgNMs or dissolved silver for 24 h and optical density (OD) was recorded each hour as a measure of bacterial growth, where decreased OD compared to negative controls indicated growth inhibition or reduction. Significantly less growth was found for all strains tested when the bacteria were incubated with dissolved silver. After 24 h, AgNMs were shown to be less effective at reducing growth than dissolved silver in all bacterial strains, although growth inhibition did occur at the highest silver concentration tested. Among the three species, E. coli K-12 was generally the most susceptible, with AgNMs showing slight toxicity with concentrations as low as 0.2 ppm. B. cereus showed moderate inhibition when exposed to AgNMs, with significant inhibition occurring as low as 20 ppm. P. aeruginosa PA01 was the least affected bacterial species showing toxicity only at 20 ppm dissolved silver and AgNMs having no significant toxicity at any concentration tested. Toxicity from AgNWs seen in all bacterial strains could potentially be due to the ability of the NM to pierce the outer membrane, as has been found with carbon nanotubes.31 P. aeruginosa showed increased growth compared to controls at 20 ppm when AgNPs were added, suggesting a possible hormetic effect. The hormetic effect has been shown previously when bacteria were exposed to nanomaterials and is thought to be caused by an increase in immune response from the bacteria.32,33 Overall, all three bacterial strains experienced lower toxicity from AgNMs compared to dissolved silver and there was very little difference among AgNM shape. In summary, we have shown that the shape of a nanomaterial can affect its toxicity. Our results indicate that AgNCs are less toxic toward model plants than AgNPs, while displaying similar bacterial toxicity. The results suggest that effective shape engineering could enable us to optimize the desired properties of AgNMs while reducing unwanted side effects within the environment. It is important to note that shape is only one of the many factors that determine the final toxicity of the nanomaterials in the environment. Other factors such as sulfidation, sunlight, and temperature, etc. need to be taken into consideration when evaluating the final environmental toxicity of any nanomaterial. Nonetheleess, achieving shape control and
control). Finally, AgNWs had insignificant toxicity toward both the roots (34.5 versus 36.1 mm for control) and the shoots (30.4 versus 33.1 mm for control). Symptoms of toxicity in L. multif lorum roots were also examined through stereomicroscopy (Figure 3). Root hairs are
Figure 3. Stereomicroscopy images of L. multif lorum root morphology. (A) shows very few root hairs were present when dissolved silver was used. (B) shows few root hairs were present when AgNPs were used. (C) shows more root hairs were present when seeds were treated with AgNCs or when seeds were treated with (D) AgNWs. (E) shows root hairs were found when water was used and when (F) PVP was used. Images were taken at 75× magnification.
a common marker of AgNM toxicity, characterized by a decrease in abundance when exposed to silver nanomaterials.24,27 Here, root hair abundance (hairs/cm2) showed the same trend as the lengths of roots and shoots (Table S2, Supporting Information). The more toxic AgNPs (14 ± 9) and dissolved silver (12 ± 4) resulted in significantly less abundant root hairs than the less toxic AgNCs (29 ± 6) and AgNWs (33 ± 10). Neither AgNCs nor AgNWs had a significantly different abundance of root hairs compared to the control (34 ± 10). The decreased abundance of root hair in AgNP exposed plants may explain some of the toxicity as root hairs are used to absorb water and nutrients required for plant growth.22 The two materials that resulted in significantly few root hairs also had significantly shorter roots and shoots, however at this time it cannot be determined if the decreased root hair abundance is the causation of reduced growth. Traditional toxicity tests have relied on a mass based dose to determine toxic effects, but recent studies have shown that particle number or surface areas are better metrics to evaluate nanomaterial toxicity.28,29 However, the disparity in L. multif lorum toxicity between the AgNPs and AgNCs can not be attributed to either the particle concentration or surface area as they were within an order of magnitude both controlled to be similar in our experiments. Additionally, the similarity in toxicities between AgNCs and AgNWs suggest that toxicity in L. multif lorum cannot be attributed to particle concentration either as these two materials differed by 3 orders of magnitude in their concentration. The differences in toxicity among the AgNMs when mass based dose, particle concentration, and surface area were similar suggest a shape-based toxic effect. Shape-based toxicity differences could be caused by differential dissolution, increased uptake of certain shapes, or stability of the nanomaterial in solution, though these were not investigated here and are the subject of future study. The higher toxicity of AgNPs to L. multif lorum compared to dissolved silver shows that ions alone could not account for all of the AgNM toxicity as has been reported previously.26 It has been theorized the AgNPs may act through a Trojan horse mechanism in which the NMs release ions at the site of 10096
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understanding the shape-dependent properties of AgNMs is a critical research area that could bring surprises to scientists.
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ASSOCIATED CONTENT
S Supporting Information *
Detailed methods, nanomaterial characterization data, discussion of D. rerio and C. elegans toxicity, and additional references. The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/ acs.est.5b01711.
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AUTHOR INFORMATION
Corresponding Author
*Phone: (919) 660-1549; fax: (919) 660-1605; e-mail: jliu@ duke.edu. Notes
The authors declare no competing financial interest.
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ACKNOWLEDGMENTS This material is based upon work supported by the National Science Foundation (NSF) and the Environmental Protection Agency (EPA) under NSF Cooperative Agreement EF0830093 and DBI-1266252, Center for the Environmental Implications of NanoTechnology (CEINT). Any opinions, findings, conclusions or recommendations expressed in this material are those of the author(s) and do not necessarily reflect the views of the NSF or the EPA. This work has not been subjected to EPA review and no official endorsement should be inferred.
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Figure 4. Percent growth reduction of bacteria compared to a no silver control after 24 h. Error bars represent one standard deviation (n = 3). In some samples, error bars are very small and are not visible. (A) shows dissolved silver was more toxic to E. coli K-12 than AgNMs, (B) shows dissolved silver was more toxic to B. cereus than AgNMs, but AgNCs displayed some toxicity, and (C) shows that AgNMs had very little effect on P. aeruginosa PA01, with AgNPs causing increased growth at the highest concentration tested. 10097
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