Cross-Generational Exposure to Low-Density Polyethylene Microplastics Induced Hyperactive Responses in Eisenia fetida Offsprings

The extensive application of plastic products in daily human life has led to the accumulation of microplastics (MPs) in agricultural soil. However, little is known about the cross-generational toxicity of MPs on terrestrial invertebrates. In this study, two-generational Eisenia fetida was exposed to low-density polyethylene (LDPE, 0–5%, w/w) for 98 days to reveal the cross-generational toxicity and the underlying mechanisms. Results showed that LDPE-MPs not only perpetrated deleterious effects on the development, hatchability, and fecundity of the F0 generation but also stimulated the antioxidant defense activity, inhibited lipid peroxidation, and disordered neurotransmission in F1 generation individuals. The susceptibility of the epidermal–intestinal barrier to LDPE-MPs was dose-dependent. According to the transcriptomic analysis, the cross-generational earthworms confirmed significant perturbances in the cell cycle, neural activity-related pathways, and amino acid metabolism pathways (p < 0.05). Nevertheless, the metabolomic profile of F1 generation individuals exhibited significant hyperactive responses in glutathione metabolism and alanine, aspartate, and glutamate metabolism (p < 0.05). This study provides a comprehensive knowledge of LDPE-MPs toxicity on cross-generational earthworms and highlights the hyperactive responses in the antioxidant defense performance of the offsprings. Our findings also underscore the necessity for long-term investigations in assessing the adverse impacts of emerging pollutants.