Accumulation of metal-based nanoparticles in marine bivalve mollusks from offshore aquaculture as detected by single particle ICP-MS

https://doi.org/10.1016/j.envpol.2020.114043Get rights and content

Highlights

  • The particle number of four NPs in mollusks followed an order of Cu > Ti ≈ Ag > Zn.

  • Ag bearing NPs had higher accumulation in mollusks than Ti, Cu, and Zn bearing NPs.

  • Four NPs were mainly accumulated in gill and digestive gland of mollusks.

  • NPs distributed in adductor muscle were smaller than those in other tissues.

Abstract

The exposure risk of metal-based nanoparticles (NPs) to marine organisms and related food safety have attracted increasing attention, but the actual concentrations of these NPs in seawater and marine organisms are unknown. In this work, single particle inductively coupled plasma-mass spectrometry (spICP-MS) was used to quantify the concentrations and size distributions of NPs in different marine mollusks (oysters, mussels, scallops, clams, and ark shells) from an offshore aquaculture farm. Results showed that Ti, Cu, Zn, and Ag bearing NPs were detected in all the five mollusks with the mean sizes at 65.4–70.9, 72.2–89.6, 97.8–108.3, and 42.9–51.0 nm, respectively. The particle concentrations of Ti, Cu, Zn, and Ag bearing NPs in all mollusks (0.88–3.26 × 107 particles/g fresh weight) were much higher than that in the seawater (0.46–0.79 × 107 particles/mL), suggesting bio-accumulation of NPs. For all the five mollusks, Ag bearing NPs had the highest number-based bioconcentration factors (NBCFs) in all the tested NPs due to the smallest mean size of Ag bearing NPs in seawater (30.5 nm). In addition, the clams exhibited the lowest NBCFs of the four NPs than other mollusks. All four NPs were mainly accumulated in the gill and digestive gland, and could transfer to adductor muscle of all mollusks. Although all the four metals (Ti, Cu, Zn, Ag) in mollusks were safe for human consumption by the estimated daily intake (EDI) analysis, the risk of NPs remaining in the mollusks should be further considered when evaluating the toxicity of metals for human health. The findings could improve our understanding on the distribution and health risk of NPs in marine mollusks under offshore aquaculture.

Introduction

With rapid development of nanotechnology, nanomaterials are widely used in commercial and consumers products, and their productions are expected to continue increasing in the future years (Kah et al., 2019; Deng et al., 2017). Metal-based nanoparticles (NPs) including TiO2, CuO, ZnO, and Ag are widely used engineered nanomaterials, with the global annual production of 3000, 1500, 550, and 55 tons, respectively (Bondarenko et al., 2013; Ganesan et al., 2016). These NPs are extensively incorporated into a large variety of products, including sunscreens/cosmetics, coatings, paints, and antibacterial materials (Barone et al., 2019; Minetto et al., 2016). Increasing production and utilization of nano-products result in the release of metal-based NPs into the marine environments, especially in offshore areas. The release of NPs in offshore areas raises great concerns about NP accumulation, long-term retention in marine organisms, and potential hazards to marine organisms, and even human health. Moreover, the adverse effects of metal-based NPs on marine organisms have been reported, and the toxicity mechanisms include teratogenesis, inflammatory responses, cellular membrane damage, oxidative stress, and DNA damage (Minetto et al., 2016; Barmo et al., 2013; Trevisan et al., 2014). Both toxicity and accumulation of NPs were highly size-dependent, and the NPs with smaller size could have higher bio-accumulation and greater toxicity (Recordati et al., 2016). It is reported that Ag NPs with the size at 20 nm were easier to accumulate in the gills and intestines of zebrafish, thus inducing greater toxicity than those at 110 nm (Osborne et al., 2015). Ag NPs at 10–20 nm could be taken up by scallop faster, and lead to higher accumulation in the hepatopancreas than Ag NPs at 70–80 nm (Al-Sid-Cheikh et al., 2013). TiO2 NPs at 10 nm were more toxic to mussel hemocytes and gill cells than TiO2 NPs with larger sizes (40 and 60 nm) (Katsumiti et al., 2014). Therefore, reliable characterization of the size distribution and quantification of number concentration of metal-based NPs in marine organisms are critical issues to assess the risk of NPs.

Reliable quantitative and qualitative characterization of NPs in organisms is particularly challenging. X-ray absorption spectroscopy (XAS), X-ray photoelectron spectroscopy (XPS), X-ray diffraction (XRD), and inductively coupled plasma-mass spectrometry (ICP-MS) are the commonly used detection methods for elemental analysis (Laborda et al., 2016). Scanning electron microscopy (SEM) and transmission electron microscopy (TEM) coupled with an energy dispersive X-ray spectroscopy (EDS), and synchrotron X-ray fluorescence imaging can provide direct visualization of NP distribution (Deng et al., 2017). For example, SEM/TEM-EDS and X-ray imaging were recently used to characterize the size distribution of TiO2 NPs in algae (Xin et al., 2019). However, the obtained NP results from the above approaches are usually qualitative or semiquantitative. The quantification of NP concentration and size distribution require the substantial amounts of tissues/samples, which limits the application of these approaches in biological sample detection (Deng et al., 2017). Single particle inductively coupled plasma-mass spectrometry (spICP-MS) is gaining increasing popularity to characterize the particle size distribution and particle concentration in the samples at short dwell times (∼100 μs) (Pace et al., 2011; Lv et al., 2019), and has been used to analyze the accumulation of TiO2, Au, and Ag NPs in different organisms such as rice (Deng et al., 2017), zebrafish (Monikh et al., 2018), and nematode (Johnson et al., 2016). For marine organisms, they face increasing stress from NPs pollution in coastal systems (Rocha et al., 2015). Bivalve mollusks are important marine organisms for accumulation of NPs due to the high enrichment of NPs in sediments (Rocha et al., 2015; Moore, 2006). However, to the best of our knowledge, there is only one report on the quantification of TiO2 NPs in mollusks by spICP-MS, which was mainly focused on the extraction efficiency of TiO2 NPs using ultrasound assisted enzymatic hydrolysis (Taboada-López et al., 2018). Different types of NPs are co-existing in marine environments, and could be simultaneously taken up and accumulated in mollusks, thus causing potential hazards to organisms and the food safety of humans. However, the distribution properties of NPs including metal type, size distribution, and particle number in different bivalve mollusks are still unknown.

In the present work, five mostly cultured and consumed marine bivalve mollusks (oysters, mussels, scallops, clams, and ark shells) obtained from the offshore aquaculture were therefore chosen to investigate the size distribution and particle concentrations of metal-based NPs. For the five mollusks, size distribution of metal-based NPs including Ti, Cu, Zn, and Ag bearing NPs in different tissues of marine bivalve mollusks was examined, and the main accumulation organs/tissues of mollusks were identified. The findings in this work will be helpful to gain insight into the health risk of NPs in different mollusks in offshore aquaculture.

Section snippets

Bivalve mollusk samples

Five bivalve mollusks were obtained from an aquaculture farm in Hongdao, Jiaozhou Bay (Qingdao, China). The fresh marine mollusks included oysters (Crassostrea gigas), mussels (Mytilus edulis), scallops (Chlamys farreri), clams (Ruditapes philippinarum), and ark shells (Scapharca subcrenata). Each fresh mollusk species with uniform sizes was chosen for further detection. Before digestion, all fresh mollusk samples were washed with ultrapure water, and the shells were then removed. Adductor

Particle recovery in spICP-MS

In order to determine the size distribution and particle concentration of metal-based NPs in mollusk tissues, the accuracy (analytical recovery) of spICP-MS was assessed firstly by spiking 50-nm Au NPs standard to ultrapure water. The measured median diameter of Au NPs by spICP-MS was around 49.1 ± 1.9 nm (Fig. S1), which was in good agreement with actual size of Au NPs standard (50 nm). In addition, the Au NP concentration recovery was 98.6 ± 3% (4.43 × 103 particles/mL detected for 4.50 × 103

Conclusions

In the present work, Ti, Cu, Zn, and Ag bearing NPs were detected in all the five marine mollusks, with the mean sizes of NPs ranging at 65.4–70.9, 72.2–89.6, 97.8–108.3, and 42.9–51.0 nm, respectively. Ag bearing NPs had higher bio-accumulation in all mollusks than Ti, Cu, and Zn bearing NPs, owning to its smaller individual size in seawater. In addition, clams exhibited lower accumulation towards NPs in comparison with oysters, mussels, scallops, and ark shells. For all the mollusks, gill and

CRediT authorship contribution statement

Lina Xu: Methodology, Investigation, Writing - review & editing. Zhenyu Wang: Supervision. Jian Zhao: Methodology, Supervision, Writing - review & editing, Funding acquisition. Meiqi Lin: Methodology. Baoshan Xing: Supervision, Writing - review & editing.

Acknowledgments

This research was supported by Natural Science Foundation of China (41530642, 41822705, 41629101), Natural Science Foundation of Shandong Province (JQ201805), Taishan Scholars Program of Shandong Province (tsqn201909051), the Youth Talent Support Program of the Laboratory for Marine Ecology and Environmental Science, the Pilot National Laboratory for Marine Science and Technology (Qingdao) (LMEES-YTSP-2018-02-09), and USDA-NIFA Hatch program (MAS 00549).

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