Elsevier

Science of The Total Environment

Volume 484, 15 June 2014, Pages 176-184
Science of The Total Environment

The coating makes the difference: Acute effects of iron oxide nanoparticles on Daphnia magna

https://doi.org/10.1016/j.scitotenv.2014.03.023Get rights and content

Highlights

  • Effects of identical IONP with four different coatings on Daphnia magna were studied.

  • Presence of D. magna increased agglomeration of two IONP species.

  • Colloidally instable IONP caused strongest effects on daphnids.

  • Neither particle size nor the kind of stabilizing forces determined the effects.

  • Molting inhibition suggested as new endpoint of nanoparticle exposure to daphnids.

Abstract

The surface of nanoparticles (NP) is often functionalized with a capping agent to increase their colloidal stability. Having a strong effect on the characteristics of NP, the coating might already determine the risk from NP to organisms and the environment. In this study identical iron oxide nanoparticles (IONP; Ø 5–6 nm) were functionalized with four different coatings: ascorbate (ASC-IONP), citrate (CIT-IONP), dextran (DEX-IONP), and polyvinylpyrrolidone (PVP-IONP). Ascorbate and citrate stabilize NP via electrostatic repulsion whereas dextran and polyvinylpyrrolidone are steric stabilizers. All IONP were colloidally stable over several weeks. Their acute effects on neonates of the waterflea Daphnia magna were investigated over 96 h. The highest immobilizing effect was found for ASC- and DEX-IONP. In the presence of neonates, both agglomerated or flocculated and adsorbed to the carapace and filtering apparatuses, inducing high immobilization. Lower immobilization was found for CIT-IONP. Their effect was hypothesized to partly originate from an increased release of dissolved iron and the ability to form reactive oxygen species (ROS). Furthermore, incomplete ecdysis occurred at high concentrations of ASC-, DEX-, and CIT-IONP. PVP-IONP did not induce any negative effect, although high quantities were visibly ingested by the daphnids. PVP-IONP had the highest colloidal stability without any occurring agglomeration, adsorption, or dissolution. Only strong swelling of the PVP coating was observed in medium, highly increasing the hydrodynamic diameter. Each coating caused individual effects. Toxicity cannot be correlated to hydrodynamic diameter or the kind of stabilizing forces. Effects are rather linked to decreasing colloidal stability, the release of ions from the core material or the ability to form ROS, respectively.

Introduction

With increasing production volumes, nanomaterials (NM) or nanoparticles (NP) will most likely be released to the environment (Gottschalk and Nowack, 2011). Most NP tend to build agglomerates, to adsorb to bigger particles or surfaces, or to be decomposed (Bhatt and Tripathi, 2011, Klaine et al., 2008). To sustain their physical and chemical properties, they are usually functionalized with a surface coating against agglomeration or dissolution (Liu et al., 2012, Lu et al., 2007). Even though these ligands are used for colloidal stabilization they can have manifold different effects on the physicochemical properties of NP. Since the contact of NP to their environment mainly occurs via their surface (Moyano and Rotello, 2011), surface functionalization might even have a higher relevance for the toxicity and the risk assessment of NP than the core material.

Most studies investigated the influence of the surface functionalization of different NP in vitro. Surface properties influenced the cellular uptake, accumulation, transformation, and elimination (Zhu et al., 2013). In vitro toxicity was most often higher for positively charged NP due to better biocompatibility to the negatively charged cellular lipid bilayer (El Badawy et al., 2011, Nomura et al., 2013, Rivera-Gil et al., 2013, Yang et al., 2012). In contrast, Lee et al. (2013) found higher skin penetration into the stratum corneum of negatively charged NP compared to NP with positive charge. Others correlated negative effects to different physicochemical properties (e.g. colloidal stability or adhesion) or interaction with biomolecules determined by the coating (Cunningham et al., 2013, Kwok et al., 2012, Tournebize et al., 2012). In vivo studies are very limited (e.g. Kwok et al., 2012). Until now the role of surface properties in determining the (environmental) risk from NP is only poorly understood and cannot be generalized.

In the environment, stabilized and highly persistent NP will most likely appear in surface waters (Baun et al., 2008, Oberdörster et al., 2005). In general, freshwater test systems are preferred for the environmental risk assessment of NM (Kahru et al., 2008). Due to their sensitivity and biology, daphnids are among one of the preferred organisms in the testing of NM (Baun et al., 2008, Griffitt et al., 2008, Kahru et al., 2008). The filter-feeding crustaceans are known to be able to filter NP from the water column and to actively ingest them (Feswick et al., 2013, Heinlaan et al., 2011, Hu et al., 2012, Lovern et al., 2008, Mendonca et al., 2011, Rosenkranz et al., 2009). Together with gill respiration, a potentially high uptake via multiple routes is possible. Furthermore, daphnids showed incomplete ecdysis under NP exposure, e.g. molting inhibition due to NP adsorbed to the carapace (Dabrunz et al., 2011). Since daphnids play an important role in the food chain accumulated NM might be bio-concentrated in higher-tier organisms like fish (Bouldin et al., 2008, Cedervall et al., 2012, Ferry et al., 2009, Holbrook et al., 2008, Hou et al., 2013, Zhu et al., 2010b). So far, only very limited data is available concerning the impact of NP surface properties on daphnids, e.g. silver NP (Allen et al., 2010, Blinova et al., 2013), zero-valent iron NP (Keller et al., 2012), quantum dots (Feswick et al., 2013, Lee et al., 2010), and fullerenes (Klaper et al., 2009).

In this account we focused on the investigation of iron-based NP, since hardly any data exist on their environmental impact (Filser et al., 2013). Iron-based NP are mainly applied due to their magnetic properties or their highly increased, redox-reactive surface. Possible biomedical applications are, e.g., their use as contrast agents for magnetic resonance imaging (Chaughule et al., 2012, Qiao et al., 2009), or cancer tumor treatment (Yu et al., 2013). Due to its cost efficiency, the highest volume might be applied for the environmental remediation of contaminated surface and ground water, sediments and soil. Here, huge amounts of iron-based NP are released to the environment, because of their ability to process a wide range of contaminants (Karn et al., 2009). To achieve a high redox-reactivity, zero-valent iron NP (nZVI) are applied (Karn et al., 2009, Kharisov et al., 2012, Sanchez et al., 2011). Released to the environment, nZVI is easily oxidized in air and hydrolyzed in water to iron oxide NP (IONP) (Khin et al., 2012). So far, this technology is still experimental and there is a serious lack of knowledge about its efficiency or the fate of iron-based NP released to the environment (Grieger et al., 2010, Noubactep et al., 2012).

To study the possible impacts of iron-based NP, we used the environmentally more relevant IONP, which were all based on the same synthesis to ensure uniform primary particles. The study aimed to investigate the influence of the stabilizers on IONP agglomeration and their effects in bio-tests. IONP are predestined for testing the influence of coatings due to the low toxicity of iron oxide itself (Zhang et al., 2012) which should not mask the possible effects of the coating. The applied IONP were functionalized with two simple molecules, ascorbate (ASC) and citrate (CIT), preventing agglomeration by electrostatic repulsion. In contrast, the polysaccharide dextran (DEX) and the polymer polyvinyl pyrrolidone (PVP) were used for steric stabilization. A previous study had already documented the colloidal stability, charge, and further characteristics of these IONP species in different media (Arndt et al., 2012). Here, we investigated the influence of four different surface functionalizations on daphnids, using the Daphnia sp. acute toxicity test according to OECD Guideline 202 (OECD, 2004), but with a prolonged test span of 96 h.

Section snippets

Culturing of daphnids

The waterflea Daphnia magna was obtained from IBACON laboratories (Roßdorf, Germany) and cultured continuously in a climate controlled chamber at 20 ± 1 °C with a 16:8 h (light:dark) photoperiod. Four semi-static cultures of 30 animals were cultured in 1.5 L Elendt M7 (EM7) medium (for detailed composition see OECD, 1998), which was renewed twice a week. Animals were fed with the green algae Pseudokirchneriella subcapitata (#61.81, SAG, Göttingen, Germany) on a basis of 150 μg C daphnid 1 day 1 (OECD,

Physicochemical properties of IONP

The surface functionalization can have manifold effects on the physicochemical properties of NP. It determines their colloidal stability, their surface charge, their hydrodynamic diameter (HDD), and can also influence effects on organisms. The IONP tested here were all based on the same synthesis and were functionalized with four different coatings. This gave us the advantage of comparing four different IONP consisting of equal core particles. Furthermore, effects of electrostatically

Conclusions

The surface functionalization of NP has a strong influence on their physicochemical properties. It determines their colloidal stability, their HDD, and can also influence the effects on organisms. The IONP tested here were all based on the same synthesis and were functionalized with four different coatings. They had different HDDs, but were all colloidally stable in Elendt M7 medium at least for a few weeks (Arndt et al., 2012). Their acute effects on D. magna were manifold and individual for

Acknowledgments

The authors thank Y. Zhang for the support in developing the quantification method for free iron in IONP solutions and K. Nitsch for revising the language of the manuscript. J. Baumann and D. Arndt are grateful for a fellowship of the graduate school nanoToxCom funded by the Hans Böckler Foundation (German Labor Unions).

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