Nanomaterial Probes in the Environment: Gold ... - ACS Publications

Research Article pubs.acs.org/journal/ascecg

Nanomaterial Probes in the Environment: Gold Nanoparticle Soil Retention and Environmental Stability as a Function of Surface Chemistry Samuel E. Lohse,*,†,‡ Nardine S. Abadeer,† Michael Zoloty,† Jason C. White,§ Lee A. Newman,∥ and Catherine J. Murphy*,† †

Department of Chemistry, University of Illinois at Urbana−Champaign, 600 South Mathews Avenue. Urbana, Illinois 61801, United States ‡ Department of Chemistry, Physical and Environmental Sciences, Colorado Mesa University, 1100 North Avenue, Grand Junction, Colorado 81501, United States § Department of Analytical Chemistry, The Connecticut Agricultural Experiment Station, 123 Huntington Street, New Haven, Connecticut 06504, United States ∥ Department of Environmental and Forest Biology, State University of New YorkSyracuse, 1 Forestry Drive, Syracuse, New York 13210, United States S Supporting Information *

ABSTRACT: The increased prevalence of functionalized nanomaterials in a range of applications will inevitably lead to nanoparticle contamination of soil and groundwater. Here, we investigate how gold nanoparticles’ (AuNPs) shape and surface chemistry influence their retention in soil columns and stability in simulated groundwater. When AuNPs are eluted from soil columns with simulated groundwater, spherical particles are more strongly retained in the soil than the rod-shaped AuNPs, regardless of the surface chemistry (as determined by ICP-OES). In a deionized water eluent, however, the same AuNPs showed a retention profile dependent upon surface chemistry (positively charged AuNPs are strongly retained by soil, while negatively charged particles are quickly eluted). This change in retention behavior suggests that the spherical AuNPs may undergo a physiochemical transformation (likely aggregation) during the elution process which reduces their mobility. AuNP stability against aggregation in simulated groundwater was investigated using absorbance spectroscopy and dynamic light scattering. We find that AuNP surface chemistry has a strong influence on AuNP stability against homoaggregation in simulated groundwater. The stability of the AuNPs depends primarily on the nature of the interaction between the AuNP surface and the capping agent (not simply the ligand charge). AuNPs protected with relatively labile capping agents are more susceptible to irreversible homoaggregation in groundwater than polyelectrolyte-coated AuNPs. However, in the presence of alginate, the AuNPs form heteroaggregates with the alginate polymers, regardless of the initial AuNP surface coating. KEYWORDS: Engineered nanoparticles, Aggregation, Homoaggregation, Nanomaterial contaminants, Environmental mobility

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INTRODUCTION

connection between nanomaterial properties and their environmental fate and transport must be investigated.10,11 Functionalized nanomaterials represent a unique class of environmental contaminants, because they exist in a size regime (∼1−200 nm) that is much closer to the colloidal materials making up naturally occurring sediment12 than typical chemical contaminants. Engineered nanomaterials’ environmental interactions should therefore be governed by some combination of their physiochemical properties (size, shape, and surface

The prevalence of nanomaterials in commercial products continues to increase.1,2 Over the past 2 decades, billions of dollars have been invested in research and development for nanomaterial-enabled consumer products, in areas such as skin care,3 sporting goods,4 industrial catalysis,5 antimicrobials,6 and cancer therapeutics.1−7 As nanomaterials proliferate in consumer products, the amount of engineered nanomaterials present in the environment will inevitably increase. 8,9 Accordingly, in order to inform future regulations on nanomaterial-enabled products and accurately estimate the environmental risk functionalized nanomaterials pose, the © 2017 American Chemical Society

Received: July 31, 2017 Revised: October 18, 2017 Published: October 25, 2017 11451

DOI: 10.1021/acssuschemeng.7b02622 ACS Sustainable Chem. Eng. 2017, 5, 11451−11458

Research Article

ACS Sustainable Chemistry & Engineering

Figure 1. Functionalized AuNP library. (a) Diagrams of the AuNPs and ligands used for functionalization. (b) Chemical structures of nanoparticle ligands. (c) TEM images of 15 nm Cit AuNPs, 15 nm CTAB AuNPs, and 50 × 12 nm CTAB AuNRs.

bacteria such as Pseudomonas aeruginosa26 and Azotobacter vinelandii27 during formation of bacterial biofilms. Thus, alginate is a useful matrix to investigate interactions between nanomaterials and natural organic matter.

chemistry). Prior to developing risk assessment profiles for any engineered nanomaterials released, we must first develop an understanding of how mobile nanomaterials are within different environmental matrices, how their mobility can be connected to their structure and composition, and how long they retain their original physiochemical properties.13,14 The behavior of functionalized gold nanoparticles (AuNPs) within different environmental matrices is of particular interest for three reasons. First, AuNPs are easier to track through environmental media than other NPs, being relatively stable against oxidation,15 easy to track and characterize,16 and gold occurs at an extremely low background level in most environments.17 Second, the physiochemical properties (size, shape,18 and surface chemistry19) of AuNPs can be controlled in exquisite detail. This allows the fate and transport of AuNPs in the environment to be closely correlated with material properties. Finally, because AuNPs are being investigated for use in biomedical applications,7 we can expect an increase in the prevalence of AuNPs in the environment. To date, there have been several limited studies investigating the environmental fate of gold nanomaterials.20−23 By systematically varying nanomaterial characteristics, as well as the chosen environmental medium, we can gain an improved understanding of the implications of nanomaterial exposure to the environment. Here, we prepared a library of functionalized AuNPs containing spherical citrate (Cit)- and cetyltrimethylammonium bromide (CTAB)-stabilized AuNPs, as well as CTAB-, sodium polyacrylate (PAA)-, and poly(allylamine hydrochloride) (PAH)-stabilized gold nanorods. We used these AuNPs probes to examine the mobility of functionalized AuNPs in two types of soils (an agricultural and a residential sample) and alginate as a function of AuNP shape and surface chemistry. We also investigated how the physiochemical properties of the AuNPs change as a result of groundwater, alginate, or soil exposure. The polysaccharide alginate is secreted by organisms such as brown algae,24 seaweed,25 and

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MATERIALS AND METHODS

Materials. All materials were used as received, unless otherwise noted. Soil samples were obtained from field sites in Connecticut (USA), dried, and characterized (Supporting Information, Table S1 and Figures S1 and S2). Gold tetrachloroaurate trihydrate (HAuCl4· 3H2O), sodium borohydride (NaBH4), ascorbic acid (C6H8O6), sodium polyacrylate (PAA; 30 wt % solution, 15000 MW), poly(allylamine hydrochloride) (PAH; 17500 MW), alginic acid (sodium salt), silver nitrate (AgNO3), hexadecyltrimethylammonium bromide (CTAB), L-ascorbic acid, sodium chloride (NaCl), and trisodium citrate (Cit, Na3C6H5O7) were obtained from SigmaAldrich. Calcium chloride dihydrate (CaCl2·2H2O) and magnesium chloride hexahydrate (MgCl2·6H2O) were obtained from Fisher. Sodium chloride was obtained from EMD Millipore. Deionized water (18.2 MΩ) was prepared using a Barnstead NANOPURE water filter. Unless otherwise noted, all nanomaterial syntheses and subsequent experiments were carried out using Nanopure deionized water. Transmission electron microscopy (TEM) grids (SiO on copper mesh, PELCO) were used for electron microscopy studies. Standard laboratory chromatography sand was obtained from Aldrich. Synthesis of Functionalized Gold Nanoparticles. AuNPs were synthesized and functionalized according to previously reported methods.28−34 Details of the NP synthesis and functionalization procedures are provided in the Supporting Information. Diagrams and TEM images of the functionalized AuNP probes used in these studies are shown in Figure 1. Nanoparticle Characterization. AuNPs were characterized using a combination of UV−vis absorbance spectroscopy (Varian Cary 500 UV−vis−near-IR spectrophotometer), transmission electron microscopy (JEOL 2100 TEM), and dynamic light scattering (DLS)/ζpotential (Brookhaven ZetaPALS). For TEM analysis, dilute AuNP solutions were drop-cast onto TEM grids. DLS and ζ-potential data for the as-synthesized AuNPs were obtained from solutions dispersed in deionized water (pH = 8.08) at a concentration of 1.0 nM for Au 11452



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nanorods and 5.0 nM for spherical AuNPs. AuNP concentrations were determined using absorbance spectroscopy, according to previously reported methods.35−37 Inductively coupled plasma optical emission spectroscopy (ICP-OES) analysis of the digested soil columns was performed using a PerkinElmer Optima 2000 ICP-OES apparatus (λem = 268 nm). Complete physiochemical characterization of the AuNPs can be found in the Supporting Information. AuNP Retention in Soil and Alginate Columns. The retention of functionalized AuNPs in the soil samples and alginate hydrogels was studied by constructing columns which were similar to chromatography columns described by Tripathi et al.38 The columns contained two different layers; either soil:sand (1:5 (w:w)) or an alginate hydrogel and sand (Figure S3). Aqueous liquid alginate was made in 2 wt %, and the solution was stirred overnight. Alginate hydrogels were formed by adding 3 mL of 0.1 M CaCl2 to 15 mL of liquid alginate.23,39 The gels were allowed to cross-link for 15 min and then were rinsed with water before being placed in the columns. Images of the alginate hydrogels are provided in the Supporting Information (Figures S4 and S5). For soil column retention experiments, 2.0 mL of a 5.0 nM spherical AuNP solution (or 2.0 mL of 1.0 nM Au nanorod solution) was added to the column and allowed to settle into the soil for 20 min prior to elution. The functionalized AuNPs were eluted using either Nanopure or simulated groundwater (2.5/2.5 ppm Ca2+/Mg2+) in separate experiments. Elution continued until AuNPs were observed (by absorbance spectroscopy) to have escaped the soil column, or until 300 mL of eluent had passed through the column. The maximum elution time for any of the AuNPs in the soil columns was ∼24 h. The percent of gold nanoparticles retained in the columns was determined by UV−vis absorbance spectroscopy of the eluent (if the AuNPs showed no signs of aggregation after elution, i.e., if the AuNPs were eluted with nanopure deionized water). However, if the AuNPs aggregated during elution, nanoparticle concentration was quantified using ICP-OES analysis of the digested soil samples. A comparison of AuNP quantitation by absorbance spectroscopy versus ICP analysis can be found in the Supporting Information. Prior to ICP analysis, soil samples were digested in boiling aqua regia (Caution: corrosive, strong oxidizer!) for 3 h. After digestion was complete, the resulting solution was gravity-filtered and diluted to a final concentration of 10% aqua regia with deionized water. Prior to analysis, the solution was further filtered with a 0.450 μm filter. For alginate column retention experiments, the column was hydrated with deionized water. Then, 2 mL of a 0.5 nM AuNP solution were loaded into the column. The AuNPs were allowed to diffuse through until they were at the top of the sand layer; then 30 mL of deionized water was added above the sand. Two fractions of eluent (15 mL) were collected. Another 10 mL of water was added above the sand, and a 13 mL fraction was collected. Absorbance spectroscopy analysis of the eluent was used to determine the percent of AuNPs that were transported through the column. Full details of column construction and analytical procedures can be found in the Supporting Information (Figures S3 and S6). AuNP Stability in Simulated Environmental Conditions. The stability of AuNPs against aggregation was investigated under three different environmental conditions: incubation in simulated groundwater (2.5/2.5 ppm Ca2+/Mg2+), simulated groundwater in the presence of alginic acid (1.0 and 600 mg/L sodium alginate), and immersion in an aqueous slurry of soil (1.0 g of soil in 5.0 mL of deionized water). The stability of the AuNPs in each of these media was assessed at [AuNP] = 1.0 nM for the spherical AuNPs and 0.20 nM for the gold nanorods, so that all samples would have an absorbance of 1 at their wavelength maximum. The aggregation state of the AuNPs was monitored using a combination of UV−vis absorbance spectroscopy and DLS. The stability of the AuNPs was monitored over a 48 or 72 h period, depending on the relative rate of aggregation that was observed. The experimental setup for these experiments is diagrammed in the Supporting Information (Figure S3).

Research Article

RESULTS AND DISCUSSION

Preparation and Characterization of the AuNP Library. We synthesized a library of functionalized AuNPs that possessed various sizes, shapes, and surface chemistries and used these NP probes to investigate the mobility of functionalized NPs in soil and alginate biofilms. The library included 15 nm spherical AuNPs protected with labile capping agents possessing both positive (CTAB) and negative (citrate) charges (though we note that citrate has recently been shown to act as a chelate on the AuNP surface and may only be truly labile under specific solution conditions).40−45 In addition, the library contained AuNRs (aspect ratio ∼ 4) coated with CTAB, PAA, and PAH. This provided AuNRs with both positive and negative surface charges and coated with both labile (monomeric) and nonlabile (electrostatically adsorbed polymer) capping agents. We have previously investigated the transport of several of the gold nanorods included in this library in estuary mesocosms, including the CTAB and PAA AuNRs.46,47 Following purification, the AuNPs’ physiochemical properties were characterized using UV−vis, TEM, ζ-potential, and DLS (Figure 1 and Table S2). AuNP Retention in Soil and Alginate Columns (Deionized Water Eluent). NP transport and retention, through columns containing environmental media, has been demonstrated to be a useful method to examine nanoparticle fate in the environment.35,48,49 Our previous studies in estuary mesocosms showed that CTAB-AuNRs and PAA-AuNRs partition into different organismal, sediment, and biofilm compartments.43,44 Therefore, we sought to understand how the physiochemical properties of AuNPs influence their retention in two types of soil (Lockwood Farm and chlordane residential) and in alginate biofilms. For these studies, the relevant soil samples or biofilms were combined with white quartz sand and packed into chromatography columns. AuNP solutions were then applied to the top of the column and eluted with deionized water (Figure S3). UV−vis absorbance spectroscopy was used to quantify the amount of AuNPs that had eluted from a given soil column. It quickly became evident that the positively charged AuNPs were strongly retained in columns prepared from either soil sample type (Supporting Information, Figures S7−S10). In fact, in the Lockwood Farm soil column, none of the positively charged AuNPs (15 nm CTAB AuNPs, CTAB AuNRs, and PAH AuNRs) were observed to exit their soil columns (Figure S7a). In contrast, the Cit AuNPs and the PAA AuNRs were quickly eluted from the soil columns. The same general trend was observed in the chlordane residential soil, except that the positively charged AuNPs were not completely retained by this soil type. While the difference in AuNP retention between the Lockwood and the chlordane residential soil was statistically significant for several AuNP samples (particularly the CitAuNPs and the PAH-AuNRs), the general trends in AuNP retention appear very similar. It is likely that the positively charged AuNPs are strongly retained in these soil types due to the strong interaction between the positively charged particles and the silicates and aluminates present in the soil (although natural organic matter [NOM] may also play a role in this regard). In order to visually verify that AuNP transport through soil columns obeyed basic electrostatics, we also examined AuNP transport through Celite columns (Supporting Information, Figures S8 and S9). Because the diatomaceous earth is white, it is possible to directly 11453


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Figure 2. Percent AuNPs retained by mass in soil columns, following elution with 2.5/2.5 ppm of Ca2+/Mg2+, as determined by ICP-OES: (a) Lockwood Farm soil and (b) chlordane residential soil.

observe the movement of the AuNPs down the entire length of these columns. The Cit-AuNPs eluted quickly through the column, but the positively charged CTAB-AuNRs hardly moved from the top of the Celite column, despite extensive elution. To further verify that positively charged AuNPs had greater affinity for the soil samples, we incubated solutions of the AuNP probes in soil samples that were slurried in deionized water. The sorption of the AuNPs to the colloidal soil components was qualitatively monitored using UV−vis absorbance spectroscopy. When the AuNP samples were incubated with the soil slurries, we again observed that positively charged AuNPs were strongly sorbed (Supporting Information, Figures S11−S17), while the negatively charged AuNPs (Cit, PAA) did not adsorb strongly to either soil type. We therefore conclude that the relative immobility of the positively charged AuNPs in the soil columns is governed by the electrostatic interactions between the AuNP capping agents and negatively charged colloidal material in the soil. Similar transport experiments through columns containing alginate hydrogels were carried out. The amount of AuNPs retained by these columns was again determined by absorbance spectroscopy analysis of the eluents (Supporting Information, Figures S7c and S10). The results from the transport experiments are shown in Figure S7c. Generally, AuNP retention in alginate was lower than in the soil columns; however, the trends across shape and surface chemistry are similar. This result demonstrates that the surface charge on AuNPs greatly influences interactions with environmental matrices, as expected. However, there were also differences in retention by shape and surface coating. For example, the PAHAuNRs had reduced retention compared to both the CTABAuNPs and the CTAB-AuNRs. These differences suggest that many nanomaterial characteristics (e.g., size, shape, and surface chemistry) can potentially influence the fate and mobility of AuNPs in the environment. AuNP Retention in Soil Columns (Simulated Groundwater Eluent). Elution with nanopure deionized water provided some basic insights into the mobility of our functionalized AuNPs within soil samples and biofilms. However, engineered NPs in the environment are more likely to be carried through soil by rainwater or groundwater, which have measurable ionic strengths. In order to better mimic AuNP transport through soil by groundwater, we repeated the

soil column retention experiment, but changed the eluent to a simulated groundwater solution (2.5/2.5 ppm of Ca2+/Mg2+). AuNP aggregation during elution is more likely at higher ionic strengths (e.g., in the simulated groundwater). Since any AuNP aggregation prevents accurate quantitation by absorbance spectroscopy, the total amount of Au present in the soil column following elution was determined using ICP-OES. Postelution, the soil column was removed and digested in boiling aqua regia. The total amount of Au retained in the soil was then determined by ICP-OES. The quantity of Au retained in the soil columns as a function of AuNP shape and surface chemistry is shown in Figure 2. Unlike the retention studies with Nanopure water as the eluent, there was a clear difference in the retention profiles between the spherical and the rodshaped AuNPs in both the Lockwood Farm and chlordane residential soil samples. In these trials, spherical AuNPs were more strongly retained (∼30% retention for both the Cit- and CTAB-AuNPs) in the soil columns than the AuNRs (∼7% retention), regardless of the particle’s surface charge. Overall, the particles were far more mobile in the soil columns when simulated groundwater was the eluent, compared to nanopure water (Figure S7 versus Figure 2). Previous studies have indicated that metal NPs are more mobile in soil in lower ionic strength eluents, but these studies were primarily performed using particles stabilized with nonionic surfactants.50,51 Furthermore, particle mobility in the nanopure water eluent was quantified using absorbance spectroscopy, rather than ICPOES; as such, we suggest caution when directly comparing the retention of the AuNPs in detail between the two eluents. It seems surprising that the shape of the AuNP should have such an effect on their soil retention, in this case. The rodshaped AuNPs have a transverse axis which is comparable in diameter to the width of the spherical AuNPs (∼15 nm). Therefore, we would expect that the shape of the particles should have little effect on their mobility and that the AuNP mobility should still be governed primarily by surface charge. Thus, it seems that, in simulated groundwater, the retention of the AuNPs in the soil columns is governed by more than the original size and surface charge of the particles. We hypothesized that the AuNPs might be undergoing some physiochemical changes (likely aggregation) during the elution process that reduced the mobility of the spherical AuNPs. It is now recognized that nanoparticles (such as AuNPs) that are resistant to oxidative dissolution under typical environmental conditions can undergo significant physiochemical 11454


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ACS Sustainable Chemistry & Engineering changes (e.g., homoaggregation, coating by proteins, or heteroaggregation with naturally occurring colloids).52,53 In order to better understand the results of our soil column studies, we chose to investigate possible changes in the AuNPs’ morphology, surface charge, and aggregation state when the AuNPs were exposed to simulated groundwater. The interaction of the AuNPs with the soil samples alone did not appear to produce physiochemical changes that would enhance AuNP retention in the soil (vide supra), so we focused specifically on physiochemical changes the AuNPs might experience when they were dispersed in groundwater and dispersed in simulated groundwater containing alginic acid. AuNP Stability in Simulated Groundwater. In order to determine how the physiochemical properties of AuNPs might change when they are dispersed in groundwater, the functionalized AuNPs were incubated in a solution of 2.5/2.5 ppm Ca2+/Mg2+. The physiochemical state of the AuNPs was monitored for a 48 h incubation period (the longest elution times in the soil column studies were ∼24 h). Both UV−vis absorbance spectroscopy and DLS measurements indicated that the Cit-AuNPs and CTAB-AuNPs completely aggregated within several hours of being dispersed in groundwater (as indicated by a loss of the surface plasmon absorbance features and a rapid increase in the hydrodynamic diameter (Figure 3 and Supporting Information, Table S3). This aggregation appears to be irreversible, as the aggregated Cit-AuNPs and CTAB-AuNPs could not be resuspended by sonicating the solution. TEM images of the resulting aggregates were also obtained (Figure 3). The TEM images of the spherical AuNPs (CTAB- and Cit-AuNPs) show that the AuNPs appear to have aggregated and fused, forming extended54 networks of larger particles or amorphous nanostructures (Figure 3a,b). Similar irreversible aggregation of Cit-AuNPs and Cit-AgNPs in moderately hard water containing calcium ions has been reported.55,56 Interestingly, the CTAB-AuNPs only aggregated in simulated groundwater if the AuNP samples had been purified twice by centrifugation and washing; if the CTABAuNP samples had only been centrifuged once, they showed high stability against aggregation (Supporting Information, Figure S18). In contrast to the spherical AuNPs, while the CTAB- and PAA-AuNRs show some loss of stability in simulated groundwater, the aggregation was far less, as indicated by UV−vis and DLS, compared to the Cit-AuNPs and CTABAuNPs (Figure 3). The PAH-AuNRs show little evidence of aggregation over the same time period. Similarly, the hydrodynamic diameter of the nanorods show relatively minor increases over the 48 h incubation period, when compared to the spherical AuNPs (Table S3). Aggregation is slow in these samples for both the polyelectrolyte-coated rods (which are stabilized by multiple electrostatic interactions with the AuNR surface) and for the CTAB-AuNRs (labile ligand). We note that the surface chemistry of the CTAB-AuNRs is not directly analogous to the spherical CTAB-AuNPs. The surface of the CTAB-AuNRs contains small amounts of adsorbed silver, bromide ions, and at least a double layer of CTAB around the particle surface with a possibly larger density of ligands on the sides of the rods compared to ends/spheres.57 This may explain why they are much slower to aggregate, in spite of the fact that they are stabilized by a relatively labile capping agent. We were able to re-disperse the CTAB-AuNRs using sonication, consistent with the TEM images showing intact nanorods after the aggregation event.

Figure 3. UV−vis absorbance spectra and TEM images of functionalized AuNPs exposed to simulated groundwater (2.5/2.5 ppm Ca2+/ Mg2+): (a) 15 nm Cit AuNPs, (b) 15 nm CTAB AuNPs, (c) 50 × 12 nm CTAB AuNRs, (d) 50 × 12 nm PAA AuNRs, and (e) 50 × 12 nm PAH AuNRs.

These observations indicate that even nanomaterials that are relatively stable against oxidation16,43,44 may be susceptible to physiochemical transformations (once dispersed in groundwater) that will substantially alter their size and shape due to aggregation (likely coupled with capping agents being released 11455


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AuNPs.22,51,61 The rapid aggregation of these AuNPs may have a significant impact on how the AuNPs partition in the environment, including how they biomagnify within the food chain. This rapid aggregation may also have significant consequences for AuNPs that are used in ecotoxicity studies involving typical indicator organisms (e.g., Daphnia or zebrafish).45,62,63

from the nanoparticle surface). The stability of the nanomaterials in environmental media therefore likely depends not only on the core material but also on the surface chemistry. In this case, it is the chemical nature of the interaction between the capping agent and the nanomaterial surface, rather than the NP’s surface charge, which appears to determine the NP’s stability. The rapid aggregation of the Cit-AuNPs and the CTAB-AuNPs in groundwater is consistent with the fact that these spherical AuNPs were more strongly retained in our soil columns than the rod-shaped gold nanoparticles. The large aggregates may be physically trapped in the soil columns and are therefore relatively immobile compared to the AuNRs. AuNP Stability in Simulated Groundwater Containing Alginic Acid. In addition to dissolved ions, most natural water sources contain some source of NOM, whether it be algae, humic acid, or other material. The presence of NOM in natural waters can reduce functionalized NP aggregation, depending on the pH and ionic strength of the solution.23,58 NOM may adsorb to the surface of the NP, stabilizing against aggregation, or may surround the NPs, linking the particles together in larger heteroaggregate structures.59 Accordingly, we explored whether the addition of NOM (in the form of alginic acid) might mediate the AuNP aggregation we observed in the simulated groundwater. The effect of alginate on AuNP aggregation in simulated groundwater was investigated using the same experimental setup as the groundwater stability studies, with the only difference being the addition of alginic acid at either 1 or 600 ppm. Absorbance spectroscopy measurements indicated that the rate of aggregation was slowed in the presence of alginate for all of the AuNPs tested and at both alginate concentrations (Supporting Information, Figures S19 and S20). Despite this, DLS measurements indicated an increase in the hydrodynamic diameter of the particles in the 600 ppm alginate solution. Furthermore, regardless of the initial surface charge, the ζpotentials of all the AuNPs were altered following immersion in the solution, and became largely negative, similar to the ζpotential of the alginate itself (Table S4). TEM images of the AuNP-alginate heteroaggregates show long chains of connected particles possessing a thin, transparent film (the alginate) around the AuNPs. These data suggest that at least some of the AuNPs form heteroaggregates with the alginate polymer; however, the nature of this heteroaggregation process is not clear. It is possible that alginate monomers adsorb to the AuNP surfaces first, and then alginate cross-links the already alginatecoated AuNPs by polymerization. Alternatively, alginate polymerization could occur first, and then the AuNPs could aggregate with the alginate polymer.60 Nevertheless, for the CTAB- and PAH-AuNRs, the heteroaggregation process can be observed in real time; visible flocculates are quickly seen to form when these AuNPs are immersed in either the 1 ppm or the 600 ppm alginate solutions (Supporting Information, Figure S21). Functionalized AuNPs are typically considered to be stable, particularly compared to silver NPs or metal oxide NPs (readily oxidized or sulfidized) under environmental conditions.10,13,14 However, we find that AuNPs stabilized with labile ligands are susceptible to irreversible aggregation in simulated groundwater, quickly giving rise to large nanowires or aggregate structures rather than individual AuNPs. This is an important consideration, as the majority of previous studies that have examined AuNP fate and transport in mesocosms or uptake into plants have used citrate-stabilized or CTAB-stabilized

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CONCLUSIONS In this study, we examined the mobility of functionalized AuNPs in soil columns and alginate biofilms and characterized the physiochemical transformations these AuNP probes undergo under typical environmental conditions. We find that the mobility of functionalized AuNPs in soil or alginate when the eluent is deionized water is well-predicted by considering the electrostatic interactions of the AuNP probes with the primary components of soil and alginate. Positively charged AuNPs are strongly retained by both soil and alginate biofilms, whereas negatively charged AuNPs remain relatively mobile. However, when simulated groundwater is the eluent, rodshaped AuNPs are more mobile in the soil columns than the spherical AuNPs, regardless of the AuNP’s surface charge. Analysis of the physiochemical transformations that the AuNP probes undergo in groundwater indicates that spherical AuNPs stabilized with labile ligands (e.g., citrate or CTAB) aggregate irreversibly, potentially reducing their environmental mobility. In contrast, polymer-wrapped AuNPs resist irreversible aggregation for a much longer time period and remain more mobile in our soil columns (though our study does not necessarily point to a direct causal link between these two phenomena). Furthermore, all the AuNPs tested form large heteroaggregates with aqueous alginate in the presence of free alginic acid. These results suggest that, for many AuNP probes, their movement through different ecosystem compartments might be better considered as the movement of large heteroaggregate species, rather than as individual nanoparticles.

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ASSOCIATED CONTENT

S Supporting Information *

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acssuschemeng.7b02622. Supplementary methods, data, and discussion, including additional soil characterization data and nanoparticle synthesis and characterization data, as well as additional data from the incubation trials (PDF)

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AUTHOR INFORMATION

Corresponding Authors

*(C.J.M.) E-mail: [email protected]. Tel.: 217-333-7680. *(S.E.L.) E-mail: [email protected]. Tel.: 970-2481590. ORCID

Catherine J. Murphy: 0000-0001-7066-5575 Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS This material is based in part upon work supported by the National Science Foundation under the Center for Sustainable Nanotechnology, Grant CHE-1503408. We acknowledge the 11456


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University of Illinois at Urbana−Champaign’s Microanalysis Facility for assistance with the ICP-OES analysis. N.S.A. acknowledges funding from the National Science Foundation Graduate Research Fellowship Program under Grant DGE1144245. We also acknowledge Colorado Mesa University for funding and instrumental assistance.

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