Article pubs.acs.org/est
Sequestration of Zinc from Zinc Oxide Nanoparticles and Life Cycle Effects in the Sediment Dweller Amphipod Corophium volutator Julia Fabrega,*,† Ratna Tantra,‡ Aisha Amer,† Bjorn Stolpe,§ Jordan Tomkins,‡ Tony Fry,‡ Jamie R. Lead,§ Charles R. Tyler,† and Tamara S. Galloway*,† †
Biosciences, College of Life and Environmental Sciences, Geoffrey Pope Building, University of Exeter, EX4 4QD, United Kingdom Nanoanalysis Group, National Physical Laboratory, Teddington, Middlesex, TW11 0LW, United Kingdom § School of Geography, Earth and Environmental Sciences, University of Birmingham, Edgbaston, Birmingham, B15 2TT, United Kingdom ‡
S Supporting Information *
ABSTRACT: We studied the effects of ZnO nanoparticles [ZnO NPs, primary particle size 35 ± 10 nm (circular diameter, TEM)], bulk [160 ± 81 nm (circular diameter, TEM)], and Zn ions (from ZnCl2) on mortality, growth, and reproductive endpoints in the sediment dwelling marine amphipod Corophium volutator over a complete lifecycle (100 days). ZnO NPs were characterized by size, aggregation, morphology, dissolution, and surface properties. ZnO NPs underwent aggregation and partial dissolution in the seawater exposure medium, resulting in a size distribution that ranged in size from discrete nanoparticles to the largest aggregate of several micrometers. Exposure via water to all forms of zinc in the range of 0.2− 1.0 mg L−1 delayed growth and affected the reproductive outcome of the exposed populations. STEM-EDX analysis was used to characterize insoluble zinc precipitates (sphaerites) of high sulfur content, which accumulated in the hepatopancreas following exposures. The elemental composition of the sphaerites did not differ for ZnO NP, Zn2+, and bulk ZnO exposed organisms. These results provide an illustration of the comparable toxicity of Zn in bulk, soluble, and nanoscale forms on critical lifecycle parameters in a sediment dwelling organism.
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INTRODUCTION The manufacture of many engineered nanomaterials exceeds thousands of tonnes per year, and there is a growing concern from regulatory and public sectors for their potential adverse effects on human and ecosystem health.1,2 Studies have shown the toxicological effects of a wide range of engineered nanomaterials and have indicated that factors such as their small size, specific surface area, shape, and metal composition may influence toxicity and cellular uptake.3−5 Despite this, the environmental impact and toxicological implication of the release of engineered nanomaterials remains uncertain. In situ measurements of engineered nanomaterials in the aquatic environment are completely absent, although modeled predictions indicate that some engineered nanomaterials could reach environmental concentrations sufficient for inducing harm in exposed organisms.6,7 One of the most commonly used engineered metal oxide nanomaterials of high economic importance is zinc oxide (ZnO NPs). The UV absorption efficiency of ZnO NPs makes them highly effective for protecting against skin damage, and they are therefore used widely in sunscreens and cosmetics.8,9 The increased use of ZnO NPs will inevitably lead to their release to the environment. Predicted environmental concentrations (PECs) are currently estimated to be in the region of tens of © 2011 American Chemical Society
nanograms per liter in surface waters, while acknowledging that local conditions such as wastewater treatment plant effluents may generate concentrations of ZnO NPs far in excess of those modeled for the general environment.6 Consequently, their (eco)-toxicological effects have been investigated in a variety of terrestrial and aquatic organisms. In those studies, the degree of aggregation, morphology, surface charge, type of coating, and dissolution have all been reported to affect their toxicity and bioavailability.8,10,11 For ZnO NPs, dissolution and release of Zn2+, which is toxic, is an important factor in considering biological effects in exposed animals.8,12 The sediment dwelling amphipod Corophium volutator (Pallas 1766) is an abundant estuarine species that lives in burrows in the upper layer of sediment. It feeds on particulate matter both in the sediment and suspended in the water column and has a key ecological role in the marine food web. This organism is a well-established test species13,14 because it is easily cultured under laboratory conditions and undergoes a complete lifecycle within 100 days. While tolerant to living Received: Revised: Accepted: Published: 1128
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Husbandry of Corophium volutator. Sediment and C. volutator organisms were collected from an intertidal area of the Otter estuary, south Devon, U.K. (used as a local reference site because of the low levels of anthropogenic pollution14. Organisms were transported back to the laboratory and acclimated at 12 ± 0.6 °C in trays containing sediment with 1 cm of overlying seawater (25 ± 0.8 ppt) in a 12:12 h light:dark cycle for 7−10 days prior to any experimental work. Further information of the test conditions can be found in Table S1 of the Supporting Information. C. volutator were fed weekly with 2 drops of aquarium invertebrate food (Liquefy Marine, Interpret Ltd., Dorking, U.K.). Weekly seawater changes were conducted 24 h after feeding. Sediment Analysis. Sediment samples were sieved with metal sieves to separate and quantify the proportion of sand (>63 μm particles), silt (399 ± 14 nm for bulk ZnO. The larger aggregates present in bulk ZnO suspensions lead to a higher precipitation rate of bulk ZnO compared with ZnO NP (half-life values of 228 vs 402 min for the bulk and NP, respectively). The findings that the hydrodynamic diameters were larger in seawater than in DIW indicate increased aggregation in seawater due to the higher concentrations of mono and divalent salts.22−25 The zeta potential DIW was positive for both ZnO NPs (+17 ± 2.1 mV) and bulk ZnO (+13.9 ± 0.66 mV) but negative in seawater (−10 ± 2.6 mV and −13 ± 1.9 mV, respectively). Thus, the isoelectric point is found at a pH between that DIW (typically pH 6) and seawater (pH 8), and therefore, pH is likely to play an important role in the stability of ZnO particles. The fundamental understanding of the effects of ionic strength and pH can be applied to estimate travel distance of the nanoparticle from its source of discharge26 and residence time in suspension. From these data, we hypothesize that the increase in the size of the aggregates of bulk ZnO particles may have led to an enhanced rate of precipitation and accumulation in the upper sediment layers, potentially increasing the contact time of the organisms with zinc, and this should be borne in mind in later discussions. As predicted by the Gibbs−Thompson effect, ZnO NP had higher equilibrium solubility than that for bulk ZnO. Particle dissolution increased with increasing time, and after 7 days the dissolution of ZnO NP was 28.13 ± 3.4% and the bulk 16.97 ± 2.11% from the starting 20 mg L−1 nominal concentrations. When using a filtration technique (0.1 μm nominal pore size) to separate ZnO NPs from its dissolved fraction, the Zn2+ fraction obtained with this technique was 6% higher than that obtained using the dialysis system, and this was likely to be the result of >100 nm aggregates and primary ZnO NPs passing though the filters used (Figure S2, Supporting Information). While the concentrations used for these studies exceed those used for exposures, they provide a useful comparator for the behavior of Zn in the exposure vessels. Toxicity of ZnO NPs. Effect on Survival, Growth, and Reproduction. Chronic exposures of C. volutator across the full lifecycle (100 days) were performed using sublethal concentrations (0.2, 0.5, and 1 mg L−1) of ZnO NP and compared to
Transmission Electron Microscopy and Energy Dispersive X-ray Analysis. The chemical composition of the granules formed in the hepatopancreas of the organisms after exposure for 100 days to the different forms of zinc (ZnO NP, bulk ZnO, and Zn ions) was investigated by scanning transmission electron microscopy (STEM) and energydispersive X-ray spectroscopy (EDX, Jeol 7000F with Oxford Inca EDX). Whole C. volutator organisms were sampled, and preparation of tissue for STEM-EDX analysis is further described in Section 1.2 of the Supporting Information
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RESULTS AND DISCUSSION Sediment Characteristics. The organic content of the sediment collected from Otter estuary, Devon, U.K. was 4.18 ± 1.15%. Grain size analysis revealed a sand:slit ratio of 65.2:34.8%. The concentration of naturally occurring Zn in sediment was 49.5 mg/kg of dry weight. All of these values are typical for the type of sediment in which C. volutator is typically found and are within the quality control limits for the methodology, as outlined in U.S. EPA.20 The elemental composition of the Otter estuary sediment is provided in Table S2 of the Supporting Information. Characterization of ZnO NPs and Bulk Particles. The sizes of individual discrete particles (circular diameter) determined by TEM were 35 ± 10 nm (n = 316) for ZnO NPs and 160 ± 81 nm (n = 204) for bulk ZnO, while the crystallite diameter determined by the Scherrer’s equation from X-ray diffraction (XRD) data was 24.1 nm for the ZnO NP and 41.5 nm for the bulk ZnO. Both particle types were mostly ellipsoidal, but the bulk particles also occurred as more elongated particles, as indicated by TEM images (Figure S1, Supporting Information). In both media, both types of particles were largely present as aggregates, as indicated by the TEM and by dynamic light scattering (DLS) measurements, showing high polydispersity indexes and hydrodynamic diameters that were considerably larger than the sizes of the discrete particles. Moreover, the hydrodynamic diameters were larger in seawater (670 ± 31 nm for NPs, 770 ± 32 nm for bulk) than in DIW (196 ± 8.4 nm for NPs, 390 ± 23 nm for bulk). Disc centrifugal sedimentation (CPS) data showed that mass appeared to be dominated by smaller aggregates for ZnO NPs, with 90% of the 1130
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Figure 2. Multiple box-and-whisker plots showing the size (body length, mm) of C. volutator in populations exposed to 0, 0.2, 0.5, and 1 mg L−1 ZnO NPs, bulk ZnO, and soluble zinc at (A) 23, (B) 63, and (C) 100 days after the onset of exposure. Asterisks (∗) represent treatments where growth was affected (ANOVA, Bonferroni p < 0.05).
trations of ZnO NPs, bulk ZnO, and Zn+ causing about 11, 12, and 21% reduction of growth, respectively, from unexposed populations. After 63 days from the onset of exposure, only the populations exposed to bulk ZnO and Zn+ showed a slower growth rate (Table S4, Supporting Information). After 100 days, in most populations individuals had reached adult size (5.11 ± 0.84 mm, Figure 1 and Table S4, Supporting
an equal mass of soluble Zn and bulk ZnO. All forms of zinc effected the survival of C. volutator (Table S3, Supporting Information), and the effects were greatest at the highest exposure concentration and after 100 days from the onset of exposure (ANOVA, p < 0.05). Specific growth rate (SGR, Table S4, Supporting Information) was significantly reduced 23 days after the onset of exposure, with the highest concen1131
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Figure 3. Light microscopy images of the hepatopancreas of C. volutator (A1) unexposed, (B1) exposed for 100 days to 1 mg L−1 of ZnO NPs, and (C1) exposed for 100 days to 1 mg L−1 of Zn2+ and correspondent transmission electron micrographs of unexposed (A2) organisms and representative micrograph of sphaerites formed in hepatopancreatic cells after exposure to ZnO NPs (B2) and Zn2+ (C2). EDX spectrum of control hepatopancreatic tissue (A3) and EDX profile of sphaerites in ZnO (B3) and Zn2+ (C3). Bar represents 500 μm.
such as identification of Zn originating from particles through the use of a tracer compound. The sublethal effects of zinc itself include slowed growth, delayed sexual maturation, and reduced fecundity, at concentrations ranging between 0.2 and 1 mg L−1. Hence, exposure to a sublethal concentration of zinc could potentially affect the population by reducing individual reproductive fitness and overall reproductive output. Observed impairment in growth of C. volutator exposed to zinc has been previously associated with a reduced availability of metabolic energy due to a decrease in feeding rates,27 respiration, excretion, and moulting frequency.28 Reproduction in C. volutator is associated with growth, and there is a linear relationship between fecundity and body size,29 with organisms needing to reach a minimal critical body size of 4 mm to be reproductive viable.15 The reduction in specific growth rate observed in our study is likely to be a contributing factor in the lack of reproduction occurring at the end of the exposure (100 days) for populations exposed to all forms of zinc (Figures 1 and 2). Indeed, in terms of reproductive success 28 days after exposure, 48% of the
Information). The one exception to this was the population exposed to 1 mg L−1 bulk ZnO, where the organisms were still significantly smaller (ANOVA, p < 0.05). We hypothesize that this reduced growth rate could be the consequence of the higher rate of sedimentation of bulk ZnO when compared to ZnO NPs, resulting in organisms living in the upper sediment layers having prolonged contact with higher concentrations of bulk ZnO and/or soluble Zn in sediments. In common with many benthic invertebrates, C volutator feeds on particulate organic matter of various forms and inorganic sediment particles, browsing from the sediment surface. C volutator is a selective feeder under certain feeding conditions, i.e., it is capable of selecting particles to ingest on the basis of specific gravity, surface texture, and organic content, although there is currently nothing known of its selectivity in dealing with aggregations of bulk or nanoform metals. Given the high natural background concentration of Zn (Table S2, Supporting Information), in the experimental system, testing of this hypothesis would require a method of tracing bioaccumulation, 1132
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unexposed population of C. volutator had undergone sexual differentiation, whereas in populations exposed to 0.5 mg L−1, a clear delay in the timing of sexual differentiation was already observed (Figure 1). At the end of the exposure, animals in all populations had reached sexual maturity; however, at the time of final sampling (100 days), only unexposed populations had reproduced (8.87 ± 3.3 neonates per female). Solubility studies indicated that populations exposed to both, NPs and bulk ZnO, were exposed to increasing concentrations of soluble zinc ions released from the particles. After 7 days, ∼28% and 17% of the ZnO NP and bulk ZnO, respectively, were solubilized, producing an estimated total pool of Zn+ of 56, 112, and 280 μL−1 for 0.2, 0.5, and 1 mg L−1 ZnO NP exposures, respectively, and 34, 85, and 170 μL−1 for bulk ZnO for the same exposure concentrations. Thus, if the effects observed were due only to zinc ions, then in theory the highest concentration of ZnO NPs (1 mg L−1 ZnO NP = 0.28 mg L−1 Zn+) should have shown a similar inhibitory effect on growth and survivorship as the populations exposed to the lowest concentration of soluble Zn+ (0.2 mg L−1), but this was not the case, indicating there may have been an additional nanoparticle specific effect. It is certainly possible that uptake routes may have differed among Zn forms and throughout the exposure duration, impacting direct comparison between the exposures. While Zn from ZnCl2 remained in solution, ZnO NPs and the bulk ZnO aggregated in the media. Dietary borne uptake of bulk ZnO and large ZnO NPs might have thus prevailed. As noted previously, it is not known to what extent C. volutator might be able to selectively feed in the presence of metal oxide aggregates. Certainly, the prediction of ingestion rates and hence of ingested doses of any contaminants associated with them will be dependent on the type of feeding, selective ingestion of particles on the basis of size or composition, wider range of food availability, and gut uptake efficiency.30 It would be of great future interest to be able to track and follow these processes for Zn in soluble, bulk, and nano forms in greater detail. C. volutator is considered more susceptible to metals in water than bound to sediment because the ions can cross respiratory surfaces, leading to a higher overall exposure than if they were ingested only during feeding.31 It is also possible an enhanced toxicity for ZnO NPs may be because ZnO NPs carry zinc ions across membranes delivering zinc ions more effectively into cells.32 Bioavailability and Uptake of ZnO NPs. Micrographs of hepatopancreas tissue in C. volutator exposed for 100 days to ZnO NP, bulk ZnO, or Zn ions showed electron dense areas corresponding to deposited metal granules or sphaerites of ∼300−500 nm in diameter (Figure 3). The presence of sphaerites in crustaceans is well known as one of the most common energy efficient strategies adopted for heavy metal detoxification,31 and their formation in C. volutator has been reported previously.32,33 These granules are usually found as membrane bound vesicles or vacuoles in epithelial cells of the hepatopancreas.34,35 Chemical analysis (EDX) of the granules confirmed the presence of high concentrations of sulfur and the presence of zinc, and these results are in agreement with reported composition of heavy metal detoxification granules formed in many other crustaceans.31,34 Zinc derived from ZnO NP in aqueous environments could have been taken up by the organisms across the integument34 or though the gut during the process of feeding. As discussed earlier, zinc bioaccumulation from ZnO NPs, bulk ZnO, or Zn2+ in C. volutator could not be quantified using elemental analysis with ICP-MS because of the
high natural abundance of this element in biological tissues. Measured concentrations of zinc in C. volutator (body tissue) at the end of the exposure (100 days) were in the range of 98− 129 μg/g, and they did not differ significantly (ANOVA p > 0.05) from those in control organisms (Figure S5 of the Supporting Information). It is not yet possible to determine if the metal granules formed in the hepatopancreas were as a consequence of the uptake and sequestration of soluble zinc dissolved from the NP, the nanoparticle, or a combination of both. It is apparent, however, that the organisms are processing and detoxifying the ZnO NPs in a similar manner (Figure 3) in each of the test exposures. One way in which a more comprehensive understanding of the fate, behavior, and uptake of ZnO NPs in this complex yet environmentally realistic exposure system could have been achieved would be to use a tracer, e.g., radioactively or fluorescently labeled particles. In fact a major bottleneck in environmental exposure modeling of NPs has been the lack of analytical and in situ techniques and instruments that can detect, quantify, and characterize NPs in complex environmental media and trace uptake in organisms at ambient levels. Conventional methods such as radiolabeling are not conducive for large scale exposure studies of NPs via the water, and indeed, the labeling process can modify the nature of the NP. Recently, the use of labeling with highly enriched stable isotopes has been proposed to address this issue.36 This would have the advantage of enabling the highly sensitive and selective detection of NPs, even in the presence of high elemental background levels (as for Zn) in complex natural samples such as those experienced here. Such experiments remain an important future objective for obtaining a better understanding of the ecotoxicology of ZnO NPs and other metal oxide nanomaterials. In conclusion, this study provides one of the first insights into the long-term effects of environmentally relevant ZnO NPs on an ecologically important marine invertebrate across a full lifecycle. Exposures of C. volutator to waterborne concentrations of 1 mg L−1 ZnO NPs showed significant effects on survival, growth, and reproduction. Solubility studies suggested that toxicity of NPs was not solely due to Zn2+. C. volutator was able to accumulate and detoxify all forms of zinc in the hepatopancreas tissue in the form of insoluble precipitates (sphaerites), illustrating how ZnO NPs may be processed and detoxified by sediment reworking organisms in the aquatic environment.
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ASSOCIATED CONTENT
S Supporting Information *
Additional experimental information. This information is available free of charge via the Internet at http://pubs.acs. org/.
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AUTHOR INFORMATION
Corresponding Author
*Tel. +44(0)1392 263436 (T.S.G). E-mail:
[email protected]. uk (T.S.G),
[email protected] (J.F.). Address: College of Life and Environmental Sciences, Geoffrey Pope Building, University of Exeter, EX4 4QD, United Kingdom.
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ACKNOWLEDGMENTS This work was funded by grants from EPSRC, EP/G043140/1, and DEFRA, LK0852. We gratefully acknowledge the NERC 1133
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Environmental Nanoscience Facility (FENAC) for help with TEM-EDX imaging; Peter Splatt for help with microscopy imaging; Alan Scarlett and Jason Weeks for sharing their knowledge on husbandry, sampling, and dissections of C. volutator; Jan Shears, Mike Wetherell, and Phil Shears for technical help and advice; and Alex Cackett and Roger Peck for their help with nanoparticle characterisation.
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