Nanoplastics Decrease the Toxicity of a Complex PAH Mixture but Impair Mitochondrial Energy Production in Developing Zebrafish

Plastics are recognized as a worldwide threat to the environment, possibly affecting human health and wildlife. Small forms of plastics such as micro- and nanoplastics can interact with other organic contaminants, potentially acting as chemical carriers and modulating their toxicity. In this study, we investigated the toxicity of polystyrene nanoparticles (Nano-PS) and a real-world environmental PAH mixture (Elizabeth River Sediment Extract, ERSE, comprised of 36 detected PAHs) to zebrafish embryos and larvae. Embryos were exposed to Nano-PS (0.1-10 ppm) or ERSE (0.1-5% v/v, equivalent to Sigma PAH 5.07-25.36 ppb) or coexposed to a combination of both. Larvae exposed to Nano-PS did not exhibit developmental defects, while larvae exposed to ERSE (2-5%) showed classic signs of PAH toxicity such as heart malformation and deformities in the jaw, fin, and tail. ERSE (5%) also impaired vascular development in the brain. When coexposed, Nano-PS decreased the developmental deformities and impaired vascular development caused by ERSE. This was strongly correlated to the lower PAH bioaccumulation detected in the coexposed animals (whole larvae, as well as the yolk sac, brain, and heart). Our data suggest that PAHs are sorbing to the surface of the Nano-PS, decreasing the concentration, uptake, and toxicity of free PAHs during the exposure. Such sorption of PAI-Is increases the agglomeration rate of Nano-PS during the exposure time, potentially decreasing the uptake of Nano-PS and associated PAHs. Despite that, similar induction of EROD activity was detected in animals exposed to ERSE in the presence or not of Nano-PS, suggesting that enough PAHs were accumulated in the organisms to induce cellular defense mechanisms. Nano-PS exposure (single or combined with ERSE) decreased the mitochondrial coupling efficiency and increased NADH production, suggesting an impairment on ATP production accompanied by a compensatory mechanism. Our data indicate that nanoplastics can sorb contaminants and potentially decrease their uptake due to particle agglomeration. Nanoplastics also target and disrupt mitochondrial energy production and act as vectors for the mitochondrial uptake of sorbed contaminants during embryonic and larval stages. Such negative effects of nanoplastics on energy metabolism and efficiency could be detrimental under multiple-stressors exposures and energy-demanding scenarios, which remains to be validated.