Toxicological assessment of anthropogenic Gadolinium in seawater: Biochemical effects in mussels Mytilus galloprovincialis

Bruno Henriques,Francesca Coppola,Rui Monteiro,João Pinto,Thainara Viana,Carlo Pretti,Amadeu Soares,Rosa Freitas,Eduarda Pereira

doi:10.1016/j.scitotenv.2019.01.341

Abstract

Recently, anthropogenic enrichment of rare earth elements (REEs) have been reported in natural environments, due to increasing use and discharges of hospital/industrial wastewaters. Gadolinium (Gd), which is mainly used as contrast agent for magnetic resonance imaging in medical exams, may reach concentrations in water up to two orders of magnitude larger than baseline levels. Nevertheless, in marine systems scarce information is available concerning the toxicity of REE towards inhabiting organisms. This study aimed to evaluate the biochemical impact of anthropogenic Gd in the Mediterranean mussel Mytilus galloprovincialis, which is a species of commercial interest and one of the most accepted pollution bioindicator. Organisms were exposed to different concentrations of Gd (0, 15, 30, 60, 120 μg/L) for 28 days. At the end of the experiments, biomarkers related to mussels' metabolic (electron transport system activity and energy reserves content), oxidative stress status (cellular damage and the activity of antioxidant and biotransformation enzymes) and neurotoxic effects (activity of the enzyme Acetylcholinesterase) were measured, as well as Gd bioconcentration in organisms. Results showed a high content of Gd (2.5 ± 0.50 μg/g) in mussels exposed to the highest concentration, contrary to those at control condition and at 15 and 30 μg/L of Gd (levels below 0.38 μg/g). Although no mortality was observed during the experimental period, exposure to Gd strongly affected the biochemical performance of M. galloprovincialis, including the decrease on mussels' metabolism, induction of oxidative stress and neurotoxicity, particularly evidenced at intermediate concentrations. These results may indicate that up to certain stressful levels, although lowering their metabolism, organisms may be able to activate defence strategies to avoid cellular injuries which, on the other hand, may compromise mussels physiological performance such as growth and reproduction success. Nevertheless, our findings support that the widespread utilization of Gd may represent an environmental risk in the future.

Highlights

The rare earth elements (REEs) are distributed broadly in the Earth’s crust in concentrations ranging on average between 150 and 220 parts per million (Kamenopoulos et al, 2016)
The levels of Gd measured in water agreed well with expected ones, with maximum deviations to the nominal concentrations along the exposure period not higher than 10% (Table 1)
The activity of Acetylcholinesterase (AChE) was decreased in the presence of Gd, with a significant inhibition at concentrations C2, C3 and C4 (Figure 5). These results clearly revealed the neurotoxic capacity of Gd, which may be related to the fact that Gd has the capacity to block K-type Ca2+ channels (Palasz and Czekaj, 2000) a similar behaviour observed for La that inhibit Ca binding to brain synaptosomal membrane, with a marked depression in the activities of neural Ca2+-ATPase, Mg2+-ATPase, and cholinesterase after acute exposure to this element (Basu et al, 1982)

Summary

Introduction

The rare earth elements (REEs) are distributed broadly in the Earth’s crust in concentrations ranging on average between 150 and 220 parts per million (Kamenopoulos et al, 2016). These elements are called "rare" not because of their abundance, which is higher than that of gold or copper, but because REEs are typically dispersed in ores rather than in the native form of aggregates or nuggets (as in the case of gold or copper) (Goodenough et al, 2016; Zepf, 2015) Their unique characteristics, such as sharply defined energy states or ideal magnetic behaviour, made REE nowadays a strategic resource to high-technologies in different fields, from medicine to clean energy or electronics (Jacinto et al, 2018; Zepf, 2015). The toxicity of Gd appears to be related with its action as a blocker of Ca2+ channels because its ionic radius is nearly equal to that of divalent Ca2+ (Sherry et al 2009, as cited by Martino et al, 2017)

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