Article Cite This: Environ. Sci. Technol. XXXX, XXX, XXX−XXX
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Combined Toxicity of Silver Nanoparticles with Hematite or Plastic Nanoparticles toward Two Freshwater Algae Bin Huang,†,‡ Zhong-Bo Wei,§ Liu-Yan Yang,§ Ke Pan,*,† and Ai-Jun Miao*,§ †
Institute for Advanced Study, Shenzhen University, Nanhai Boulevard 3688, Shenzhen, Guangdong Province 518060, China Key Laboratory of Optoelectronic Devices and Systems of Ministry of Education and Guangdong Province, College of Optoelectronic Engineering, Shenzhen University, Shenzhen, Guangdong Province 518060, China § State Key Laboratory of Pollution Control and Resource Reuse, School of the Environment, Nanjing University, Mail box 24, Xianlin Road 163, Nanjing, Jiangsu Province 210023, China Environ. Sci. Technol. Downloaded from pubs.acs.org by UNIV OF ADELAIDE on 03/21/19. For personal use only.
‡
S Supporting Information *
ABSTRACT: In the natural environment, the interactions of different types of nanoparticles (NPs) may alter their toxicity, thus masking their true environmental effects. This study investigated the toxicity of silver NPs (AgNPs) combined with hematite (HemNPs) or polystyrene (PsNPs) NPs toward the freshwater algae Chlamydomonas reinhardtii and Ochromonas danica. The former has a cell wall and cannot internalize these NPs, while the latter without a cell wall can. Therefore, the toxicity of AgNPs toward C. reinhardtii was attributed to the released Ag ions, while AgNPs had direct toxic effects on O. danica. Moreover, nontoxic HemNPs ameliorated AgNP toxicity toward C. reinhardtii, by decreasing the bioavailability of Ag ions through adsorption. Despite their role as Agion carriers, HemNPs still reduced the toxicity of AgNPs toward O. danica by competitively inhibiting AgNP uptake. In both algae, Ag accumulation fully accounted for the combined toxicity of AgNPs and HemNPs. However, the combined toxicity of AgNPs and PsNPs was complicated by their significant individual toxicities and the synergistic interactions of these particles with the algae, regardless of differences in Ag accumulation. Overall, in environmental assessments, considerations of the combined toxicity of dissimilar NPs will allow more accurate assessments of their environmental risks.
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INTRODUCTION Engineered nanoparticles (NPs) are defined as particles with a diameter between 1 and 100 nm in at least two dimensions.1 As a result of their unique physicochemical characteristics, NPs have wide applications in various fields, and their annual production has been estimated to be approaching one million tons per year.2 A substantial fraction of these NPs will enter aquatic environments during their production, transportation, and utilization.3,4 Given the ever-increasing concern about the environmental risks posed by NPs, their toxicity toward organisms at different trophic levels has been intensively studied.5,6 Most of those investigations examined the toxicity of a single type of NP. However, the natural environment is a complicated system containing different types of NPs,7,8 such that the toxicity results of a single type of NP may not reflect its true environmental impact. Therefore, studies focusing on the combined toxicity of dissimilar NPs are indispensable. According to the conventional paradigm of combined/mixed toxicity,9 when two or more NPs are present simultaneously, their toxicities will reflect their synergistic, additive, or antagonistic interactions.10−12 Although studies of the combined toxicity of NPs are limited, the results have revealed various mechanisms (e.g., contact reduction between NPs and organisms, decreased bioavailability of the metal ions released © XXXX American Chemical Society
from the NPs by surface adsorption, and changes in the photocatalytic activity of the NPs) underlying the toxicity variation of one type of NP in the presence of another. For instance, Tong et al.13 examined the combined toxicity of ZnO and TiO2 NPs toward the bacteria Escherichia coli and Aeromonas hydrophila. They found that ZnONPs reduced the contact between bacterial cells and TiO2NPs, thus decreasing the toxicity of the latter. TiO2NPs, in turn, alleviated the toxicity of ZnONPs due to their adsorption of Zn ions. Huynh et al.14 reported that heteroaggregation between hematite NPs (α-Fe2O3, HemNPs) and silver NPs (AgNPs) decreased the antimicrobial toxicity of the latter, by physically preventing these particles from coming into direct contact or close proximity with E. coli cells. Other studies showed that, in the dark, TiO2NPs attenuated the toxicity of AgNPs toward E. coli, by surface adsorption of Ag ions,15 but during light exposure the toxic effects of these two NPs reflected their synergistic interaction: specifically, their enhanced photocatalytic activity and the production of reactive oxygen species (ROS).16 Hence, Received: Revised: Accepted: Published: A
December 12, 2018 February 24, 2019 March 18, 2019 March 18, 2019 DOI: 10.1021/acs.est.8b07001 Environ. Sci. Technol. XXXX, XXX, XXX−XXX
Article
Environmental Science & Technology
Malvern). Both DLS and NTA measure Brownian motion and then relate the determined movement to an equivalent hydrodynamic diameter of the particles. However, NTA tracks the movement of the particles on a particle-by-particle basis by imaging and thus avoids the bias toward large particles. The morphology and size of the NPs in the experimental suspension were further examined by transmission electron microscopy (TEM; JEM-200CX, JEOL, Tokyo, Japan).27 The axenic culture of C. reinhardtii (Chlorophyta) used in the present study was obtained from the Institute of Hydrobiology, Chinese Academy of Sciences (Wuhan, China), and that of O. danica (Chrysophyta, UTEX 1298) from the Provasoli-Guillard Center for the Culture of Marine Phytoplankton, Bigelow Laboratory (West Boothbay Harbor, ME). The two algae were cultured in a modified WC (WC*, pH = 7.0, ionic strength = 3.5 mM, Table S1, Supporting Information) and DY-V (DY-V*, pH = 7.0, ionic strength = 4.5 mM, Table S2, Supporting Information) medium, respectively.21,29 Although both media contain various metal ions, they are unsaturated, and thus, no metallic precipitates are formed. Both WC* and DY-V* were also the basis of all media used in the experiments. The culture temperature was 25 °C, with a light illumination of 50 μmol photons/(m2 s) in a 12 h/12 h light/dark cycle. Throughout the experiment, C. reinhardtii and O. danica were collected by centrifugation (1700g, 10 min). According to the results of the preliminary centrifuge experiments with either algal cells or NPs, the centrifugal speed and time were optimized so that the cells could be effectively collected while avoiding the sedimentation of NPs. Ag-Ion Adsorption Experiment. The adsorption medium was prepared 1 day in advance and left overnight to equilibrate before the addition of HemNPs (0, 10, and 100 mg Fe/L) or PsNPs (0, 3, and 30 mg C/L) on the following day. The nominal concentration of Ag ions in the adsorption medium was 1, 3, 10, 30, and 100 μg/L. After 12 h, the adsorption equilibrium was reached, and a 0.5 mL aliquot was collected and centrifuge-filtered (13 600g, 10 min) through a 10 kDa membrane (PALL Nanosep series). The membrane had a pore size of ∼1 nm and could thus retain both HemNPs and PsNPs. The concentration of Ag in the adsorption medium without filtration (total Ag: [Ag]T), in the
