PAH Sorption to Nanoplastics and the Trojan Horse Effect as Drivers of Mitochondrial Toxicity and PAH Localization in Zebrafish

Abstract

Plastics are world-wide pollutants that pose a potential threat to wildlife and human health. Small plastic particles, such as microplastics and nanoplastics, are easily ingested, and can act as a Trojan Horse by carrying microorganisms and pollutants. This study investigated the potential role of the Trojan Horse effect in the toxicity of nanoplastics to the vertebrate model organism, zebrafish (Danio rerio). First, we investigated if this effect could affect the toxicity of nanoplastics. Second, we analyzed if it could contribute to the biodistribution of the associated contaminants. And third, we focused on its effect on the mitochondrial toxicity of nanoplastics. We incubated 44 nm polystyrene nanoparticles with a real-world mixture of polycyclic aromatic hydrocarbons (PAHs) for 7 days and removed the free PAHs by ultrafiltration. We dosed embryos with 1 ppm of nanoplastics (NanoPS) or PAH-sorbed nanoplastics (PAH-NanoPS). Neither type of plastic particle caused changes in embryonic and larval development. Fluorescence microscopy and increased EROD activity suggested the uptake of PAHs in larvae exposed to PAH-NanoPS. This coincided with higher concentrations in the yolk sac and the brain. However, PAH-only exposure leads to their accumulation in the yolk sac but not in the brain, suggesting that that the spatial distribution of bioaccumulated PAHs can differ depending on their source of exposure. Both nanoplastic particles affected mitochondrial energy metabolism but caused different adverse effects. While NanoPS decreased NADH production, PAH-NanoPS decreased mitochondrial coupling efficiency and spare respiratory capacity. In summary, the addition of PAHs to the surface of nanoplastics did not translate into increased developmental toxicity. Low levels of PAHs were accumulated in the organisms, and the transfer of PAHs seems to happen in tissues and possibly organelles where nanoplastics accumulate. Disruption of the energy metabolism in the mitochondria may be a key factor in the toxicity of nanoplastics, and the Trojan Horse effect may amplify this effect.

Metabolic Consequences of Developmental Exposure to Polystyrene Nanoplastics, the Flame Retardant BDE-47 and Their Combination in Zebrafish

“…These findings are in line with previous reports confirming uptake of PS nanoplastics principally in the intestine ( Lu et al, 2016 ; Skjolding et al, 2017 ; Pitt et al, 2018 ; Brun et al, 2019 ; Trevisan et al, 2019 ; Trevisan et al, 2020 ). Oral ingestion following hatching has been characterized as the principal route of exposure in developing zebrafish, with limited biodistribution following ingestion for PS nanoparticles larger than 50 nm in size ( van Pomeren et al, 2017 ).…”

Interplay Between Nanoplastics and the Immune System of the Mediterranean Sea Urchin Paracentrotus lividus

“…In addition, harmful effects could arise by what PS NPs carry onto their surface, such as for instance contaminants already present in the aquatic environment (e.g., heavy metals, pesticides, hydrocarbons, and pharmaceuticals). As a result, PS NPs could act as vectors of other contaminants and enhance their cellular uptake and accumulation in selected organs (i.e., Trojan horse effect) (Trevisan et al, 2020;Zhang and Xu, 2020).…”

Screening of the Toxicity of Polystyrene Nano- and Microplastics Alone and in Combination with Benzo(a)pyrene in Brine Shrimp Larvae and Zebrafish Embryos

“…Higher bioaccumulation of phenanthrene was also observed in embryos co-exposed with small NPs (20 nm) than in embryos co-exposed with larger NPs (500 nm) or exposed to phenanthrene alone [ 34 ].While, 44 nm PS NPs (10 mg/L) alone and combined with PAHs from a sediment extract provoked a dysfunction of the mitochondrial function in zebrafish embryos. The reported mitochondrial dysfunction was no longer observed in the embryos exposed to the corresponding PAH mixture alone (5073 ng/mL), while cardiotoxicity and impaired brain vascularity were observed [ 35 ].…”