Metabolomics-based assessment of nanoparticles (nZnO) toxicity in an infaunal marine annelid, the lugworm Arenicola marina (Annelida: Sedentaria)

Nanopollutants such as nZnO gain importance as contaminants of emerging concern due to their high production vol-ume and potential toxicity. Coastal sediments serve as sinks for nanoparticles but the impacts and the toxicity mech-anisms of nZnO in sediment-dwelling organisms are not well understood. We used metabolomics to assess the effects of nZnO-contaminated sediments on a benthic ecosystem engineer, an infaunal polychaete Arenicola marina. The worms were exposed to unpolluted (control) sediment or to the sediment spiked with 100 or 1000 mu g Zn kg-1 of nZnO. Oxidative lesions (lipid peroxidation and protein carbonyls) were measured in the body wall as traditional biomarkers of nanopollutant toxicity. Metabolite profiles (including amino acids, tricarboxylic acid (TCA) cycle and urea cycle intermediates) were determined in the body wall and the coelomic fluid. Exposure to nZnO altered metab-olism of the lugworms via suppression of the metabolism of gluconeogenic and aromatic amino acids, and altered the TCA cycle likely via suppression of fumarase activity. These metabolic changes may negatively affect carbohydrate metabolism and energy storage, and impair hormonal signaling in the worms. The total pool of free amino acids was depleted in nZnO exposures with potentially negative consequences for osmoregulation and protein synthesis. Exposure to nZnO led to accumulation of the lipid peroxidation products demonstrating high susceptibility of the cellular membranes to nZnO-induced oxidative stress. The nZnO-induced shifts in the metabolite profiles were more pronounced in the coelomic fluid than the body wall. This finding emphasizes the important metabolic role of the coelomic fluid as well as its suitability for assessing the toxic impacts of nZnO and other metabolic disruptors. The metabolic disruptions caused by environmentally relevant concentrations of nZnO can have negative effects on the organisms' fitness impairing growth and reproduction of the populations of marine bioturbators like the lugworms in nanoparticle-polluted sediments.

Automated summary

Nanopollutants such as nZnO are emerging contaminants with high production volume and potential toxicity. This study investigated the effects of nZnO-contaminated sediments on benthic ecosystem engineer Arenicola marina using metabolomics. The results showed that nZnO exposure altered the metabolism of the lugworms, suppressing gluconeogenesis and aromatic amino acid metabolism, and altering the TCA cycle. These metabolic changes may negatively affect carbohydrate metabolism, energy storage, and hormonal signaling. nZnO exposure also led to lipid peroxidation and depletion of free amino acid pool. The findings highlight the important role of coelomic fluid in assessing the toxic impacts of nZnO and other metabolic disruptors.