The global concern over ecological contamination from microplastics (MPs) and heavy metals prompts apprehensions about environmental integrity and human well-being. Yet, the co-exposure of MPs and toxic metals in the freshwater planarian Dugesia japonica remains poorly understood. We addressed this gap by studying the individual and combined toxic effects of Polystyrene MPs (PS-MPs) and lead (Pb2+ ions) on D. japonica. PS-MPs, at 20 mg/L, acted as carriers of Pb2+ ions, impacting planarian homeostasis, tissue regeneration, and neuronal development. In situ hybridization (WISH) and immunofluorescence showed that both Pb2+ and PS-Pb2+ interfered with stem cell differentiation and proliferation in homeostatic planarians, decreasing stem cells by 43.7% and 67.4%, respectively, compared with control. Molecular and genetic studies revealed that both Pb2+ ions PS-Pb2+ disrupted planarian antioxidant systems (enzymatic and nonenzymatic) and energy metabolism, while PS-MPs appeared to facilitate the disruptive effects of Pb2+ ions on energy metabolism, potentially triggering ferroptosis. Oxidative damage, including DNA damage, was caused as a result of this disruption, which inhibited mitochondrial function and prevented cell differentiation and proliferation, thereby slowing neuron regeneration. The results suggest that PS-MPs can function as 'Trojan horses', transporting Pb2+ ions into aquatic environments, and causing negative effects on benthic organisms.