Environ Sci Pollut Res (2014) 21:7899–7912 DOI 10.1007/s11356-014-2745-7

RESEARCH ARTICLE

Fate and effects of metal-based nanoparticles in two marine invertebrates, the bivalve mollusc Scrobicularia plana and the annelid polychaete Hediste diversicolor Catherine Mouneyrac & Pierre-Emmanuel Buffet & Laurence Poirier & Aurore Zalouk-Vergnoux & Marielle Guibbolini & Christine Risso-de Faverney & Douglas Gilliland & Déborah Berhanu & Agnieszka Dybowska & Amélie Châtel & Hanane Perrein-Ettajni & Jin-Fen Pan & Hélène Thomas-Guyon & Paul Reip & Eugénia Valsami-Jones

Received: 31 October 2013 / Accepted: 5 March 2014 / Published online: 21 March 2014 # Springer-Verlag Berlin Heidelberg 2014

Abstract The objective of this paper is to synthesize results from seven published research papers employing different experimental approaches to evaluate the fate of metal-based nanoparticles (Ag NPs, Au NPs, CuO NPs, CdS NPs, ZnO NPs) in the marine environment and their effects on two marine endobenthic species, the bivalve Scrobicularia plana and the ragworm Hediste diversicolor. The experiments were carried out under laboratory (microcosms) conditions or under environmentally realistic conditions in outdoor mesocosms. Based on results from these seven papers, we addressed the following research questions: (1) How did the environment into which nanoparticles were released affect their

physicochemical properties?, (2) How did the route of exposure (seawater, food, sediment) influence bioaccumulation and effects?, (3) Which biomarkers were the most responsive? and (4) Which tools were the most efficient to evaluate the fate and effects of NPs in the marine environment? The obtained results showed that metal‐based NPs in general were highly agglomerated/aggregated in seawater. DGT tools could be used to estimate the bioavailability of metals released from NPs under soluble form in the aquatic environment. Both metal forms (nanoparticulate, soluble) were generally bioaccumulated in both species. Among biochemical tools, GST and CAT were the most sensitive revealing the

Responsible editor: Philippe Garrigues C. Mouneyrac (*) : P.Ag) (Barka et al. 2001). These mechanisms of defenses (CAT, GST) may be relatively efficient considering the general lack of response of markers of damage such as TBARS, AChE and LDH. However, the oxidative stress due to CuO, CdS, ZnO NPs and Ag NPs triggered the activation of cytosolic CSP suggesting that these NPs exerted cytotoxicity by an apoptotic process. These effects were observed despite the fact that clams activated antioxidant defences. Increased LDH activity is interpreted as an increased rate of organisms’anaerobic metabolism, suggesting a rapid need of additional energy to prevent chemical stress (Moreira et al. 2006). Usually, no changes in LDH activity (except for CdS NPs in seawater and ZnO NPs in sediment)

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were observed in organisms exposed to both metal forms (soluble or nanoparticulate). Even if 40 nm Au NPs frequently induced slightly higher responses (CAT, SOD), than smaller Au NPs (5 and 15 nm), there was not a clear pattern of size effect (Pan et al. 2012). At an environmentally realistic concentration of 67ZnO NPs in sediment, there was no strong evidence for a severe NP effect since most effects were also observed in the presence of the stabilizing solution (DEG) alone (Buffet et al. 2012). AChE is an enzyme essential for the degradation of the neurotransmitter acetylcholine in cholinergic synapses and thus responsible for the correct transmission of nerve impulses in both vertebrates and invertebrates. It is believed that AChE activity is inhibited after organisms are exposed to contaminants, and subsequently can interfere with behaviour. AChE activities showed no responses after exposure to both metal forms of Ag, Cd, Cu and Zn as ZnO NPs at sublethal doses (Buffet et al. 2011, 2012, 2013a, b). Unexpectedly, we observed that AChE activity in clams was significantly increased by Au NP exposure (Pan et al. 2012), perhaps as the consequence of a phenomenon of overcompensation as proposed by Badiou et al. (2008). However, behaviour does not depend only on the normal functioning of the nervous system and defense mechanisms were probably not sufficient to prevent burrowing impairments that were frequently observed as a consequence of NP exposures (CuO: Buffet et al. 2011, 2013a; Au: Pan et al. 2012; ZnO: Buffet et al. 2012; CdS via food) and decreases of feeding rate (CuO: Buffet et al. 2011, 2013a; Ag: Buffet et al. 2013b; CdS, ZnO: Buffet et al. 2012). In H. diversicolor, CAT and GST activities were very responsive, as previously described for S. plana (see above). Greater CAT activities were observed in worms exposed to CuO NPs (seawater) and CdS (food) compared with soluble Cu and Cd, respectively. The same pattern was shown for GST in worms exposed to CdS NPs (seawater). These results suggest an oxidative stress endured by animals exposed to metal-based NPs studied under our experimental conditions. LDH activity was increased in contaminated specimens by Ag NPs for direct exposure and by soluble Ag for food exposure. An increase in LDH activity was also observed with Au NPs (Pan et al. 2012). SOD activities showed no responses in H. diversicolor after exposure to both forms of metals (nanoparticulate, soluble) at sublethal doses. No significant change in TBARS levels was observed for Ag NPs, CdS NPs, CuO NPs (seawater) or Au NPs within the range of NP sizes tested. Antioxidant defenses (CAT, GST) may be sufficiently efficient to counter-act oxidant effect of NPs. For AChE, we observed in H. diversicolor the same pattern as described above for S. plana. At environmentally realistic concentration of 67ZnO NPs in sediment, there was no strong evidence for a severe NP effect in H. diversicolor since most effects were also observed in the presence of the stabilizing solution (diethylene glycol) alone (Buffet et al. 2012). CSP activity

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was usually induced for all NPs tested (CuO Ag, ZnO, CdS) with the exception of Ag NPs in food exposure. CSP activities were higher in worms exposed to CdS NPs (seawater, food) compared with soluble Cd. Genotoxicity Due to their small size and high surface area, coupled to other physico-chemical features such as metal content and charged/ capped surfaces, nanomaterials may well have unpredictable genotoxic properties (Xie et al. 2011). The first evidence for DNA damage revealed by comet assay was found in marine bivalves exposed to CuO NPs but also to soluble Cu as described in Buffet et al. (2013a). Indeed, Cu as a redox active metal is an oxidative stress inducer (Regoli et al. 2011) promoting the formation of highly reactive oxygen species affecting DNA integrity (Ozawa et al. 1993). In the digestive gland of clams, the most striking feature was the higher genotoxicity and lower CSP activity observed after 21 days of exposure in mesocosms to Ag NPs compared to soluble Ag. Ag NPs probably caused too severe DNA damage in cells that might not be able to repair DNA efficiently. The release of labile Ag from Ag NPs in the experimental medium alone cannot completely explain these observed effects and it might likely be an Ag NP specific effect. As for S. plana, DNA damage was revealed by the comet assay in ragworms exposed to CuO NPs (Buffet et al. 2013a) or Ag NPs but also to soluble Cu or Ag at 10 μg metal L−1. Cong et al. (2011) demonstrated that only Ag NP concentrations of 16 and 3 2 μ g A g L − 1 e n h a n c e d a g e n o t o x i c e ff e c t i n H. diversicolor, compared to lower concentrations (2, 4 or 8 μg L−1). Because the genome is actively involved in cellular metabolism, exposure to genotoxic metal-based NPs can impair development, reproduction and survival of individuals and finally contribute in endangering populations. Which tools were the most efficient to evaluate the fate and effects of NPs in the marine environment? Predicting the environmental implications of nanotechnology is complex and requires a sound characterization of NPs. Recently Handy et al. (2012) and Von der Kammer et al. (2012) reviewed the practical considerations for conducting ecotoxicity tests with manufactured nanomaterials and analytical methods, respectively. The necessity of characterizing the starting material or stock dispersions using more than one technique is well admitted in order to confirm the primary particle size and the size distribution in the dispersion solution. Full characterization of NPs in the experimental media during ecotoxicity tests is also needed but complicated by the presence of other solids in the matrix. In the seven published research papers, combined techniques such as TEM/SEM, DLS were used to determine the size and the size distribution

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and dialysis and DGTs for the estimation of metal release from NPs. TEM allows for the highest magnification of nano-sized structures but solely from a two-dimensional perspective whereas SEM is particularly useful for its ability to create three dimensional images. DLS represents the most common technique for particle size analysis. Outfitting a DLS instrument with a special cell that allows for an applied voltage provides measures of particle charge or zeta potential. DLS is suitable for spherical solid particles such as the metal-based NPs studied in these seven published research papers. Widely available instruments do not yet permit the characterization of NPs in complex matrices particularly sediment. For instance, light scattering methods do not allow the discrimination between NPs and other particles such as natural colloids present in these environmental matrices. However, application of tracer techniques such as stable isotopes labelling are well suited to distinguish metal added with NPs from metals naturally present in sediment and biota. Buffet et al. (2012) showed that the use of 67ZnO NPs was suitable to trace the fate of ZnO NPs in sediments and also investigated bio-uptake in clams and ragworms. Dissolution of metals from metalbased NPs can be estimated in the water phase using dialysis and/or high-speed centrifugation (Handy et al. 2012). However, if these experiments are carried out without the test organism present in the experimental media (missing the ligands released by the organism), or with different volumes of media compared to the ecotoxicity test protocol, then dissolution data from dialysis may be difficult to interpret. Results from the seven published research papers showed that DGT tools allowed the estimation of metal release from NPs both in the water phase and in the sediment compartment. This technique is relevant in experiments carried out at low doses since in this case no saturation of the resin occurs. In all cases, results from DGTs were in accordance with those from dialysis experiments. Finally, as detailed above, biomarkers are remarkably efficient for the detection of oxidative stress and genotoxicity.

Conclusion The present review contributes to the debate around the nanotoxicity of NPs themselves or the labile metals released from NPs into the experimental media. Results from the seven published research papers showed that metal‐based NPs in general were highly agglomerated/aggregated in seawater. Differences between the metal-based NPs employed were observed in the release of metals from NPs in the experimental media. Both metal forms studied were generally bioavailable and bioaccumulated in both species. Future works are needed to localize cellular targets and subcellular distribution of NPs. These studies require the use of spectroscopic methods such as X-rays spectroscopies using synchrotron radiation. There is

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also an urgent need of investigating the role of trophic transfers of ENPs in complex food webs. Concerning effects, results suggested that animals exposed to metal-based NPs endured oxidative stress. Among biochemical tools, GST and CAT were the most sensitive revealing the enhancement of anti-oxidant defenses in animals exposed to sub-lethal concentrations of metal-based NPs. Apoptosis and genotoxicity were frequently observed. Future works, such as transcriptomic approaches, are needed to unravel molecular mechanisms associated with ENPs toxicity. To fill the gap existing between (sub)organismal responses to NPs and effects occurring at higher levels of biological organisation, ecologically relevant biomarkers such as behaviour, and genotoxicity appeared as promising candidates since their responses could impair development, reproduction and survival of individuals and finally contribute in endangering populations. Concerning interspecies differences between S. plana and H. diversicolor, usually no consistent trends were observed since the bioaccumulation depends on the type of metal and metal forms (nanoparticulate or soluble) and the way of exposure. DGT tools deployed either in the water phase or in sediment could be used to estimate the bioavailability of metals released from NPs under soluble form in the aquatic environment. The use of the stable isotope tracing approach is of great interest to investigate the fate of NPs in sediment and to explore ecotoxicity effects of NPs under environmentally realistic conditions. Transformations and long-term fate of manufactured nanomaterials must be measured in realistic complex natural systems to accurately assess the risks that they may pose. In this way, outdoor mesocosms are powerful tools enabling the best compromise between a true representation of ecological processes and the possibility of controlling or at least monitoring a number of natural and contamination factors. They allow investigations on the types of transformations that nanomaterials will undergo in real, complex environments during long-term ageing, and the impact of these transformations on their speciation, distribution in the environment, bioavailability and toxicity potential on biota. Acknowledgements The research leading to these results has received funding from the European Union Seventh Framework Programme (FP7/ 2007–2013) under grant agreement no. 214478 (NanoReTox).

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