Multiomics analyses uncover nanoceria triggered oxidative injury and nutrient imbalance in earthworm Eisenia fetida

The toxic stress caused by nanoceria remains vague owing to the limited efforts scrutinizing its molecular mechanisms. Herein, we investigated the impacts of nanoceria on earthworm Eisenia fetida, at the molecular level using the multiomics-based profiling approaches (transcriptomics, metabolomics, and 16 S rRNA sequencing). Nanoceria (50 and 500 mg/kg) significantly increased the contents of malondialdehyde (MDA), Fe, and K in worms, suggesting oxidative injury and nutrient imbalance. This was corroborated by the transcriptomic and metabolomic analyses. Nanoceria decreased the levels of certain genes and metabolites associated with glycerolipid and glycerophospholipid metabolisms, suggesting the production of reactive oxygen species and subsequent oxidative stress. Additionally, the ABCD3 gene belonging to ABC transporter family was upregulated, facilitating Fe uptake by worms. Moreover, the higher contents of MDA, Fe, and K after exposure were tightly associated with the imbalanced intestinal flora. Specifically, a higher relative abundance of Actinobacteriota and a lower relative abundance of Proteobacteria and Patescibacteria were induced. This study, for the first time, revealed that nanoceria at nonlethal levels caused oxidative stress and nutrient imbalance of earthworms from the perspective of genes, metabolites, and gut microbiome perturbations, and also established links between the gut microbiome and the overall physiological responses of the host.