Mechanisms of nanoplastic-induced energy metabolism reprogramming in juvenile Sepia esculenta: mRNA profile, miRNA/mRNA network, and ceRNA network

The presence of nanoplastics (NPs) in aquatic environments poses significant threats to the health of aquatic organisms, garnering widespread attention. The Sepia esculenta , known for its high protein content, is a favored seafood among consumers in China. However, studies investigating the harmful effects of NPs on Sepia esculenta remain scarce. Given that juvenile animals are more vulnerable to environmental stressors, we focused our research on juvenile Sepia esculenta and established an NPs exposure model with one control group and two NPs treatment groups. We conducted sequencing of the mRNA, miRNA, and lncRNA transcriptomes across the three groups. In our results, mRNA profiling, along with miRNA/mRNA and lncRNA/miRNA/mRNA network analyses, provided evidence that NPs triggered a reprogramming of energy metabolism. This shift was characterized by the suppression of glycolysis and amino acid metabolism, resulting in reduced ATP synthesis capacity, while simultaneously enhancing GTP metabolism. Furthermore, results from both mRNA profiling and biochemical tests confirmed that NPs induced oxidative stress; interestingly, oxidative stress played a role in mediating the metabolic reprogramming. Importantly, miRNAs and lncRNAs were involved in energy metabolism reprogramming induced by NPs. Our findings will provide novel insights into the effects of environmental pollutants on Sepia esculenta , contributing to the conservation efforts for endangered species within the context of environmental contamination. • NPs poisoning model of juvenile Sepia esculenta was successfully established. • NPs inhibited ATP production capacity, promoted GTP metabolism and caused energy metabolism reprogramming. • miRNAs and lncRNAs were involved in the mechanism of energy metabolism reprogramming. • Oxidative stress mediated energy metabolism reprogramming under NPs stress.