Environmental hazard profile of gadolinium (Gd3+): Mechanistic insights into its ecotoxicity towards Euglena gracilis from a multi-level investigation.

As emerging environmental contaminants, rare earth elements (REEs) pose a growing ecotoxicological threat, making a mechanistic understanding of their toxicity in aquatic primary producers like microalgae crucial for accurate ecological risk assessment. This study investigated the multi-level adverse effects of gadolinium (Gd³⁺), a representative REE contaminant, on Euglena gracilis by integrating physiological, ultrastructural, and non-targeted metabolomic approaches. While background environmental concentrations of Gd are low, levels in anthropogenically impacted systems can exceed ∼60 mmol/L, providing the context for this toxicological investigation. Gd³⁺ exhibited potent, dose-dependent toxicity, causing a 35.77 % inhibition of growth at 80 μmol/L, with a calculated EC₅₀ for growth inhibition of 110.5 μmol/L (95 % CI: 95.8-127.5 μmol/L), alongside detrimental morphological shifts and severe chloroplast damage. While total photosynthetic pigments and paramylon decreased in the culture, their per-cell levels paradoxically increased, signifying a severe cellular stress response. Non-targeted metabolomics revealed extensive metabolic reprogramming, with lipid metabolism identified as the primary target of Gd³⁺-induced cellular damage, accounting for 65.8 % of the differential metabolites. This disruption included the significant upregulation of lysophospholipids, a nearly 400-fold increase in the signaling molecule 12-HETE, and the perturbation of key bioenergetic pathways like oxidative phosphorylation. In conclusion, Gd³⁺ exerts multi-target toxicity in E. gracilis through direct chloroplast damage, drastic reprogramming of lipid metabolism leading to membrane disruption and altered signaling, and consequent disorders in energy metabolism. These findings advance REE ecotoxicology and highlight that the disruption of lipid metabolism is a key toxic mechanism and a potential sensitive biomarker for REE-induced hazardous effects, providing crucial evidence to inform environmental risk assessments and establish water quality benchmarks for these materials.