Article pubs.acs.org/est
Heavy Metal Uptake and Toxicity in the Presence of Titanium Dioxide Nanoparticles: A Factorial Approach Using Daphnia magna. Ricki R. Rosenfeldt,*,† Frank Seitz,† Ralf Schulz,† and Mirco Bundschuh†,‡ †
Institute for Environmental Sciences, University of Koblenz-Landau, Fortstrasse 7, D-76829 Landau, Germany Department of Aquatic Sciences and Assessment, Swedish University of Agricultural Sciences, Lennart Hjelms Väg 9, SWE-75007 Uppsala, Sweden
‡
S Supporting Information *
ABSTRACT: Unintentionally released titanium dioxide nanoparticles (nTiO2) may co-occur in aquatic environments together with other stressors, such as, metal ions. The effects of P25-nTiO2 on the toxicity and uptake of the elements silver (Ag), arsenic (As) and copper (Cu) were assessed by applying a factorial test design. The test design consisted of two developmental stages of Daphnia magna, two levels of nTiO2 (0 versus 2 mg/L) as well as seven nominal test concentrations of the respective element. The presence of nTiO2 increased Ag toxicity for juveniles as indicated by a 40% lower 72-h EC50, while the toxicities of As and Cu were reduced by up to 80%. This reduction was even more pronounced for Cu in the presence of dissolved organic carbon (i.e., seaweed extract) and nTiO2. This outcome coincides with the body burden of the elements, which was elevated 2-fold for Ag and decreased 14-fold for Cu in the presence of nTiO2. Although the underlying mechanisms could not be uncovered, the data suggest that the carrier function of nTiO2 plays a central role. However, to understand the processes and mechanisms occurring in the field due to the presence of nTiO2 further systematic investigations considering environmental variables and nanoparticle characteristics are required.
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INTRODUCTION Titanium dioxide nanoparticles (nTiO2) are the most frequently used nanoparticles and their production volume is still increasing.1 Given their widespread utilization in numerous products,2 including sunscreens and facade paints, a risk for nTiO2 entering surface water bodies is anticipated.3 In this context, median environmental concentrations of nTiO2 in surface water bodies are predicted to be in the ng to low μg/L range. 4 Westerhoff et al., 5 for instance, measured Ti concentrations of up to 15 μg/L in 0.7-μm-filtered wastewater samples. In wastewater treatment plant effluents and therefore also in the receiving water body, nTiO2 co-occurs with other anthropogenic stressors, for example, heavy metals. Indeed, Shafer et al.6 measured in the effluents of municipal wastewater treatment plants silver (Ag) and arsenic (As) concentrations of up to 2.6 and 5.2 μg/L, respectively. Copper (Cu) concentrations between 2.1 and 19.9 μg/L were also found.7 This raises questions about potential ecotoxicological interactions between nTiO2 and heavy metals, especially when considering the large surface area of the nanoparticles, compared to other ubiquitously occurring colloids and particles. Earlier studies indicate an elevated uptake of metal ions, that is, Cu, As, and cadmium, in the presence of nTiO2 for daphnids and carp,8−10 which may be accompanied by an increased toxicity.8,11 Besides an increase in the body burden of coexisting heavy metals, the unique photocatalytic properties of nTiO2 potentially explain the observed combined toxicity in the © 2014 American Chemical Society
presence of metal ions: the energy of photons enables electrons to overcome the band gap of nTiO2 (3.0−3.2 eV) generating electron-holes and finally reactive oxygen species (ROS). The electrons and the electron-holes usually recombine achieving the original constitution of nTiO2.12 However, metal ions adsorbed onto the particle surface may scavenge released electrons. Thereby the recombination rate is reduced, which increases the number of electron holes and eventually the generation of ROS by nTiO2.12−14 Understanding the role of metal ion’s properties (e.g., their charge) during their interaction with nTiO 2 is from ecotoxicological viewpoint still limited, especially in light of the current lack of consideration for a potentially enhanced generation of ROS. This limited knowledge is evident through the variable and partly contradictory effects of nTiO2 on heavy metal toxicity displayed in recent literature. Furthermore, nanoparticle characterization was incomplete in most studies (e.g., actual particle size and zeta potential in the medium) complicating their interpretation and comparison among investigations. The present study focuses on the combined toxicity of three elements as representatives of the subset “heavy metals” (i.e., Ag, As, and Cu), whose most toxic ions are Received: Revised: Accepted: Published: 6965
December 4, 2013 April 2, 2014 May 21, 2014 May 21, 2014 dx.doi.org/10.1021/es405396a | Environ. Sci. Technol. 2014, 48, 6965−6972
Environmental Science & Technology
Article
Table 1. Test Items, Main Ions in the Medium Used, Producer, Purity, The Nominal Concentrations Applied in the Respective Acute Toxicity Test and the Respective Literature 48-h EC50 exp.
a
element
test item
I
Ag
AgNO3
II
As
III
Cu
Na2HAsO4 × 7H2O CuSO4 × 5H2O
IV
Cu
Cu(NO3)2 × 3H2O
main ionsa Ag+ (82.4%), AgCl(aq) (15.9%), AgSO4− (1.6%) HAsO42− (93%), H2AsO4− (7%) CuCO3(aq) (88.2%), CuOH+ (5%), Cu2+ (2.6%) CuCO3(aq) (88.2%), CuOH+ (5%), Cu2+ (2.6%)
producer
purity (%)
nominal concentrations (μg/L)
literature 48-h EC50 (μg/L)
Roth
≥99.9
0, 0.5, 1, 2, 4, 8, 16
∼118
SigmaAldrich Fluka
98−102
∼250019
≥99.0
0, 1000, 2000, 4000, 8000, 16 000, 32 000 0, 6, 12, 24, 48, 96, 192
Merck
≥99.5
0, 6, 12, 24, 48, 96, 192
∼3019
∼3019
Main ions were determined via VMINTEQ (3.0, Stockholm, Sweden, 2011, http://www2.lwr.kth.se/English/OurSoftware/vminteq/index.html).
differently charged (mainly Ag+, HAsO42−, and Cu2+), in the presence (2 mg/L) and absence (0 mg/L) of well-characterized nTiO2. Since the crystalline phase of nTiO2 (e.g., anatase vs rutile) might influence the interaction of the nanoparticles and metal ions, please note that the present study employed a mixture of the crystalline phases anatase and rutile, that is, the product P25. Therefore, the ecotoxicity of each of the abovedescribed scenarios was assessed in three separate experiments for two developmental stages of Daphnia magna, namely juveniles (age
