Transcriptomic insights into an ancient and endangered species: Adverse effects of nanopolystyrene on the behavior and energy metabolism of Tachypleus tridentatus

Abstract

The widespread presence of nanoplastics in marine environments raises concerns about their toxicological impacts on marine organisms. Juvenile Tachypleus tridentatus inhabits intertidal zones where micro- and nanoplastics accumulate. This study exposed juvenile T. tridentatus to four nanopolystyrene (NPS) concentrations (0, 1, 10, and 100 μg/L) to assess impacts on swimming performance (average and maximum speeds), light avoidance ability, burrowing behavior, key respiratory metabolic enzymes (hexokinase, phosphofructokinase, pyruvate kinase, pyruvate dehydrogenase, succinate dehydrogenase), and transcriptomic profiles. Results revealed reduced swimming performance across treatments, with enhanced burrowing behavior at higher concentrations. NPS increased glycolysis and tricarboxylic acid cycle enzyme activities. Transcriptomic analysis on day 21 identified 1043, 907, and 1328 differentially expressed genes for the 1, 10, and 100 μg/L treatments, respectively. KEGG and GO enrichment analysis highlighted key pathways affected by NPS, including oxidative stress-related processes (glutathione metabolism, cytochrome P450-mediated xenobiotic metabolism, ferroptosis) and energy metabolism pathways (glycolysis, oxidative phosphorylation, carbohydrate digestion). Behavioral and transcriptomic data suggest that NPS impaired swimming, light avoidance and burrowing behavior, potentially linked to changes in neuroactive ligand-receptor interactions and serotonergic synapse activity. These findings provide novel insights into nanoplastic toxicity mechanisms and offer potential biomarkers for evaluating environmental stress in marine organisms.

Keywords: Behavior; Energy metabolism; Nanopolystyrene; Tachypleus tridentatus; Transcriptomics.