Size-Controlled Dissolution of Silver Nanoparticles at Neutral and

Article pubs.acs.org/est

Size-Controlled Dissolution of Silver Nanoparticles at Neutral and Acidic pH Conditions: Kinetics and Size Changes Tanya S. Peretyazhko,*,† Qingbo Zhang, and Vicki L. Colvin Department of Chemistry, Rice University, Houston, Texas 77005, United States S Supporting Information *

ABSTRACT: Silver nanoparticles (AgNP) are widely utilized in increasing number of medical and consumer products due to their antibacterial properties. Once released to aquatic system, AgNP undergoes oxidative dissolution leading to production of toxic Ag+. Dissolved Ag+ can have a severe impact on various organisms, including indigenous microbial communities, fungi, alga, plants, vertebrates, invertebrates, and human cells. Therefore, it is important to investigate fate of AgNP and determine physico-chemicals parameters that control AgNP behavior in the natural environment. Nanoparticle size might have a dominant effect on AgNP dissolution in natural waters. In this work, we investigated size-dependent dissolution of AgNP exposed to ultrapure deionized water (pH ≈ 7) and acetic acid (pH 3) and determined changes in nanoparticle size after dissolution. Silver nanoparticles stabilized by thiol functionalized methoxyl polyethylene glycol (PEGSH) of 6 nm (AgNP_6), 9 nm (AgNP_9), 13 nm (AgNP_13), and 70 nm (AgNP_70) were prepared. The results of dissolution experiments showed that the extent of AgNP dissolution in acetic acid was larger than in water. Solubility of AgNP increased with the size decrease and followed the order AgNP_6 > AgNP_9 > AgNP_13 > AgNP_70 in both water and acetic acid. Transmission electron microscopy (TEM) was applied to characterize changes in size and morphology of the AgNP after dissolution in water. Analysis of AgNP by TEM revealed that the particle morphology did not change during dissolution. The particles remained approximately spherical in shape, and no visible aggregation was observed in the samples. TEM analysis also demonstrated that AgNP_6, AgNP_9, and AgNP_13 increased in size after dissolution likely due to Ostwald ripening.

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INTRODUCTION Silver nanoparticles (AgNP) are one of the most used type of nanomaterial with the estimated production of 500 tons per year.1 Silver nanoparticles are widely utilized in increasing number of medical and consumer products including cosmetics, textiles, electronics, paints, and water desinfectants due to their antibacterial properties.2 The bactericidal activity of AgNP is considered to be mainly due to Ag+ leaching from AgNP, while the relative importance of contribution of AgNP itself remains questionable.3,4 The released silver ions have been demonstrated to damage cell functioning directly by binding to thiolcontaining biomolecules5 and/or indirectly by production of reactive oxygen species.6 The accidental release of AgNP to the environment can have a severe impact on various organisms, including indigenous microbial communities, fungi, alga, plants, vertebrates, invertebrates, and human cells.7 For better understanding of AgNP fate, bioavailability and toxicity it is critical to investigate the processes that govern AgNP behavior in complex natural environment. Dissolution is one of the main processes that controls AgNP behavior in aquatic systems. Dissolution of AgNP occurs through oxidation of metallic Ag and release of Ag+ into solution. 8 Release of Ag + is determined by intrinsic © XXXX American Chemical Society

physicochemical properties of AgNP and by those of the solution. Parameters that either enhance or suppress AgNP dissolution are ionic strength, pH, dissolved oxygen concentration, temperature, dissolved complexing ligands (organic matter, sulfur, chlorine), AgNP surface coating, shape and size.7,9 Often dissolution of AgNP is controlled by a combination of solution and intrinsic properties making it challenging to evaluate contribution of each parameter to dissolution. Studies of AgNP dissolution in natural and synthetic waters revealed that particle size might have a dominant effect on AgNP dissolution. For instance, studies of AgNP dissolution in acetate buffer (pH 4) revealed more Ag+ release from 4.8 nm than from 60 nm particles. Nevertheless surface-area-normalized Ag+ release was similar for both sizes suggesting that AgNP dissolution is sizecontrolled.10 In general, the particle size has an inverse effect on AgNP dissolution: small nanoparticles (26 d) is necessary to get to equilibrium. No dissolution was observed in the AgNP_70, concentration of dissolved Ag+ was ∼0.2 μM at t = 0 d and did not change throughout the dissolution experiment (Figure 3a). The extent of dissolution ([Ag+]end/[Ag]total) followed the order AgNP_6 > AgNP_9 > AgNP_13> AgNP_70 and was equal to 14.9, 5.5 and 3.2% in the AgNP_6, AgNP_9, and AgNP_13, respectively, after 80 d incubation. Similar to AgNP samples in water, dissolved Ag+ increased with time in acetic acid and

[Ag +]t = [Ag +]total *(1 − exp−kt )

(1)

where concentration of dissolved Ag+ ([Ag+]) and time (t) were measured experimentally (Figure 3) while total dissolved Ag+ ([Ag+]total) and pseudo-first-order rate constant (k) were

Figure 2. Absorption spectra of AgNP in water as a function of dissolution time (a) AgNP_6, (b) AgNP_9, (c) AgNP_13, and (d) AgNP_70. D

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of the dissolved AgNP were shifted to larger particle sizes with respect to the initial AgNP sizes. Comparison of AgNP sizes also revealed that dissolved AgNP contained particles of the size that were not present in the initial samples (Figure 4). The 80 d dissolved AgNP_6 contained ∼21% particles of the size 12−25 nm, AgNP_9 contained ∼10% of the size 20−30 nm, and AgNP_13 contained ∼2% of the size 23−26 nm. The AgNP_6, AgNP_9, and AgNP_13 average diameters after dissolution were 10.4 ± 3.5 nm (1841 particles), 13.3 ± 4.1 nm (919 particles), and 16.0 ± 3.3 nm (737 particles) and were larger than the initial diameters (Table 1). The average diameter of AgNP_70 after dissolution was statistically the same as the initial one and was equal to 72.0 ± 13.4 nm (116 particles). X-ray diffraction analysis of the 80d-dissolved AgNP_6 revealed that no mineralogical changes occurred during dissolution. Metallic Ag was present in the samples before and after dissolution (SI Figures S4 and S5). No other crystalline Ag-containing phases were visible by XRD.

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DISCUSSION Studies of PEGSH-coated AgNP dissolution revealed that solubility of nanoparticles was larger in acetic acid than in water and Ag+ release followed the order AgNP_6 > AgNP_9 > AgNP_13 > AgNP_70 in both water and acetic acid (Figure 3). The proposed mechanisms of AgNP dissolution is oxidative dissolution through reaction of metallic Ag with dissolved oxygen and protons8 following reactions: Figure 3. Dissolved Ag in μM and % as a function of time in AgNP suspensions in (a) water and (b) 0.05 M acetic acid. Total AgNP concentration at the beginning of dissolution was 74 μM. Dissolved Ag+ in % was calculated as [Ag+]/[Ag]total × 100%.

4Ag(s) + O2 = 2Ag 2O(s)

(2)

Ag 2O(s) + 2H+ = 2Ag + + H 2O

(3)

+

Dissolution is initiated by oxidation of metallic Ag on the surface of AgNP by dissolved O2 and formation a 1−2 atomic layer thick silver(I) oxide19 (Ag2O). The layer of Ag2O dissolves releasing Ag+ into solution until Ag2O is extinguished.7,10,20 Once the Ag2O layer is completely dissolved, further oxidation of metallic Ag to Ag2O might occur, and AgNP dissolution will continue. Our observation of increase of AgNP dissolution when pH decreased from 7 (water) to 3 (acetic acid) might further support formation of Ag2O surface layer. In the presence of water, the surface of Ag2O is covered with surface hydroxyl groups (AgOH) which undergo protonation at acidic pH (AgOH2+21). Protonation tends to weaken and break surface AgO bonds, resulting in larger Ag+ release into solution at acidic than at neutral pH. According to thermodynamic calculations, AgNP are not stable in aerobic waters with pH ranging from 4 to 12 and will dissolve completely.8 However, in our study no complete dissolution of AgNP was observed. The extent of dissolution varied between 3 and 15% in water and between 6 and 41% in acetic acid. Similar AgNP behavior was observed in other dissolution studies that found an extent of AgNP dissolution of 30% in acetate buffer (pH 4),8 10−27% in Hoagland medium (pH 5.6),13 11−52% in water (pH not reported)19,22 and 1− 60% in 1 M NaHCO3 solution (pH 8).12 The results indicate that kinetic factors play an important role in inhibiting complete AgNP dissolution. Incomplete dissolution could be due to Ag+ adsorption on AgNP, limited diffusivity of O2 and protons to reaction sites, AgNP stabilization by PEGSH, and particle aggregation.10,12 We hypothesized that the partial dissolution of AgNP observed in our study is due to an increase in the particle size leading to a solubility decrease.

fitted parameters (Table 2). We found that dissolution kinetics depended on the particle size and the fastest dissolution Table 2. First-Order Kinetic Fitted Parameters water AgNP

[Ag ]total, μM

AgNP_6 AgNP_9 AgNP_13 AgNP_70

15.5 5.5 1.7

+

0.05 M acetic acid k, d

−1

1.24 0.43 0.15

[Ag+]total, μM

k, d−1

29.1 13.4 9.0 4.7

1.65 0.65 0.29 0.25

kinetics was observed in the AgNP_6. Comparison of the pseudo-first-order rate constants for AgNP dissolution in water and acetic acid revealed that kinetics was faster for all AgNP in acetic acid (Table 2). AgNP after Dissolution. Analysis of AgNP by TEM revealed that particle morphology did not change after 80 d dissolution in water. The particles remained approximately spherical in shape and no visible aggregation was observed in the samples (SI Figure S3). The particle size distributions of the AgNP_6, AgNP_9, and AgNP_13 at the end of dissolution experiment were significantly different than the distributions of the initial AgNP, while the size distributions of the AgNP_70 remained the same (Figure 4). We found that size distributions of the dissolved AgNP_6, AgNP_9, and AgNP_13 became broader than the initial ones and the most pronounced broadening was observed in the AgNP_6 (Figure 4). Moreover, size histograms E

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Figure 4. Normalized size distributions before and after dissolution in water of (a) AgNP_6, (b) AgNP_9, (c) AgNP_13, and (d) AgNP_70.

Ag and 79% Ag2O. High Ag2O content in the AgNP_6 sample after dissolution would allow XRD detection if the precipitated Ag2O was crystalline. However, XRD analysis of the sample after dissolution revealed that only metallic Ag was present, eliminating precipitation of crystalline Ag2O (SI Figure S5). In addition, saturation of solution with respect to Ag2O was calculated using solution composition data at 80 d time point [pH = 7.1 (SI Figure S2), dissolved Ag+ concentrations of 11 μM at 80 d (Figure 3) and Ag2O solubility product (log Ksp = −7.7223]. Solution was undersaturated with respect to Ag2O (saturation index, −16.03) at the end of dissolution experiment, suggesting that no precipitation of Ag2O occurred. Experimental evidence of increase in average particle size as well as broadening of size distribution might indicate that Ostwald ripening was responsible for AgNP size growth.24,25 Ostwald ripening is explained by the fact that larger particles with small surface to volume ratios are more stable than smaller particles with large surface to volume ratios, leading to dissolution of smaller particles and redeposition of the released atoms at larger particles. Growth of AgNP follows oxidation− reduction mechanisms, first smaller AgNP are oxidized by O2, Ag+ is then dissolved, followed by Ag+ reduction and Ag deposition on larger AgNP.26 Such mechanism would likely lead to a decrease in concentration of dissolved Ag+ with time as observed in AgNP_6 and AgNP_9 samples (Figure 3a). However, the dissolved Ag+ concentration decrease, 5 and 0.8 μM (Figure 3a), would result in an average size growth to 7.2 and 9.5 nm in AgNP_6 and AgNP_9, respectively, which is smaller than the observed diameters at the end of dissolution experiment (Table 1, size increase is calculated using “magic numbers” of nanoclusters27 and total number of nanoparticles).

Analysis of AgNP by TEM revealed that the average diameter increased after dissolution of AgNP_6, AgNP_9, and AgNP_13 and remained unchanged in nondissolving AgNP_70 (Table 1). The absence of size increase in the nondissolving AgNP_70 suggested that release of Ag+ during AgNP dissolution was necessary for the nanoparticle growth. We considered two possible mechanisms of AgNP size growth: (1) precipitation of dissolved Ag+ on the surface of AgNP and (2) Ostwald ripening. The first hypothesis was evaluated based on the XRD analysis of the 80 d-dissolved AgNP_6 (SI Figure S5), calculations of mass increase due to Ag+ precipitation and saturation index calculations. The AgNP_6 size increased from 6.2 ± 1.6 nm to 10.6 ± 3.5 nm by the end of dissolution experiment. Increase in dissolved Ag+ concentration might shift eq 3 equilibrium toward Ag2O precipitation. Assuming that the size increase was due to Ag2O precipitation, the mass increase (Δm) with respect to the initial mass could be calculated from the change in average volume by the following: ⎤ ρAg O ⎡ average i=1 2 ⎢ Δm = − 1⎥ × 100% 3 ⎥ ρAg ⎢⎣ j average ⎦ j=1

(4)

where ρAg2O and ρAg are densities of Ag2O (7.14 g/cm3) and Ag (10.5 g/cm3), respectively; i = 1 to 1841 and j = 1 to 1039 are numbers of particles after and before dissolution, respectively, obtained from sizing analysis by TEM, and D is a diameter of an individual particle. According to eq 4, the particle mass increased by 310% with respect to the initial mass due to Ag2O precipitation. On the basis of the obtained mass increase, the final AgNP suspension should contain 21% metallic F

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AgNP_6 before and after dissolution). This material is available free of charge via the Internet at http://pubs.acs.org/.

The discrepancies in concentration changes and size growth suggest that oxidation of metallic Ag and reduction of Ag+ occurred simultaneously after reaching equilibrium. Similar observations were reported by Jang et al.25 for Ostwald ripening of gold nanoparticles (AuNP) during which dissolved Au concentration did not change while particles increased in size. We were not able to determine what reducing agent was responsible for Ag(I) to Ag(0) transformation in our dissolution studies. Jang et al.25 studied Ostwald ripening of AuNP in the presence of H2O2 and Br−. The authors demonstrated that H2O2 induced both oxidation of smaller AuNP to Au(III) and Au(III) reduction leading to the increase in size of larger ones. Hydrogene peroxide production was detected during dissolution of citrate-coated AgNP in airsaturated water.8 The authors revealed that after a 3 h dissolution experiment, up to 0.4 μM H2O2 was produced in the presence of AgNP, while no H2O2 was detected in a control AgClO4 solution. In the study of AgNP behavior in the presence of H2O2, He et al.28observed reduction of Ag+ at pH > 5.5. The authors demonstrated that the final AgNP increased in size, and the morphology changed from spherical to more irregular shape.28 We hypothesized that oxidative dissolution of AgNP might catalyze production of H2O2, which further reduced Ag+ to Ag atoms. Deposition of Ag atoms on the AgNP surface resulted in the particle growth.

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*E-mail: [email protected]. Present Address †

Jacobs, NASA JSC, Texas 77058, United States.

Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS This research was supported by the National Science Foundation (CMMI-1057906).

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ENVIRONMENTAL SIGNIFICANCE Our study demonstrated that the extent of AgNP dissolution depends significantly on the particle size and pH of the aqueous system. We found that small AgNP (≤13 nm) are more soluble than large ones (70 nm), confirming previous observations.9−13 A decrease of pH from 7 to 3 dramatically increased extent of AgNP dissolution. We observed that the nondissolving at neutral pH AgNP_70 become active at acidic pH resulting in ∼7% dissolution. The observation suggested that no AgNP could be considered absolutely nonreactive toward dissolution. Changes in aquatic chemistry could activate AgNP dissolution and, therefore, enhance harmful properties of AgNP due to release of toxic Ag+. The studied AgNP did not dissolve completely at both pHs. The TEM analysis of the AgNP dissolved in water revealed that AgNP_6, AgNP_9, and AgNP_13 increased in size while AgNP_70 remained the same at the end of dissolution experiment. We hypothesized that the partial dissolution of AgNP observed in our study was due to increase in the particle size leading to a solubility decrease. The finding of AgNP size increase has an important implication for the aquatic systems. The nanoparticle growth might lead to long-term stability of AgNP and consequently prolonged exposure of indigenous organisms to silver. The exact mechanisms of observed AgNP growth in our experiments remained unknown. No particle size increase in the nondissolving AgNP_70 let us hypothesize that the presence of dissolved Ag+ was necessary for the nanoparticle growth. We assumed that Ostwald ripening through oxidative dissolution of AgNP, reduction of Ag+ to Ag and Ag deposition was responsible for the size increase. Further studies are required to investigate factors controlling AgNP size increase including role of dissolved Ag+ and nature of reducing agent.

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AUTHOR INFORMATION

Corresponding Author

ASSOCIATED CONTENT

S Supporting Information *

Additional figures (AgNP absorbance, pH changes during AgNP dissolution, TEM images of AgNP after dissolution, and XRD of G

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