Nanoplastic exposure in soil compromises the energy budget of the soil nematode C. elegans and decreases reproductive fitness

Abstract

Environmental nanoplastics (NPs) can accumulate in soils, posing a potential risk to soil ecosystems. However, the ecotoxicity of NPs for soil organisms has received little research attention. This study investigated whether NP exposure in soil leads to reproductive decline in the soil nematode Caenorhabditis elegans and sought to determine the mechanisms by which it may occur. Wild-type N2 C. elegans L1 larvae were exposed to various concentrations of nano-sized polystyrene (100 nm) in soil (0, 1, 10, 100, and 1000 mg/kg dry weight) for 96 h. We show that nano-sized polystyrene (100 nm) labeled with red fluorescence significantly accumulated in the intestine of C. elegans in a dose-dependent fashion via soil exposure (8%–47% increase). In addition, NP soil exposure led to 7%–33% decline in the number of eggs in utero and 2.6%–4.4% decline in the egg hatching percentage. We also find that the number of germ cell corpses (31%–55% increase) and the mRNA levels of germline apoptosis marker gene ced-3 (14%–31% increase) were significantly higher with greater NP soil exposure (10, 100, and 1000 mg/kg), while intracellular ATP levels were significantly reduced. Finally, the DEBtox model, which is based on the dynamic energy budget theory, was applied to show that the increased reproductive costs for C. elegans caused by NPs in soil are associated with energy depletion and reproductive decline. The threshold value (4.18 × 10−6 mg/kg) for the energy budget also highlighted the potential high reproductive risk posed by NPs in terrestrial ecosystems. Our study provides new insights into how soil organisms interact with NPs in soil ecosystems.