Abstract
Single-use plastic production is higher now than ever before. Much of this plastic is released into aquatic environments, where it is eventually weathered into smaller nanoscale plastics. In addition to potential direct biological effects, nanoplastics may also modulate the biological effects of hydrophobic persistent organic legacy contaminants (POPs) that absorb to their surfaces. In this study, we test the hypothesis that developmental exposure (0–7 dpf) of zebrafish to the emerging contaminant polystyrene (PS) nanoplastics (⌀100 nm; 2.5 or 25 ppb), or to environmental levels of the legacy contaminant and flame retardant 2,2′,4,4′-Tetrabromodiphenyl ether (BDE-47; 10 ppt), disrupt organismal energy metabolism. We also test the hypothesis that co-exposure leads to increased metabolic disruption. The uptake of nanoplastics in developing zebrafish was validated using fluorescence microscopy. To address metabolic consequences at the organismal and molecular level, metabolic phenotyping assays and metabolic gene expression analysis were used. Both PS and BDE-47 affected organismal metabolism alone and in combination. Individually, PS and BDE-47 exposure increased feeding and oxygen consumption rates. PS exposure also elicited complex effects on locomotor behaviour with increased long-distance and decreased short-distance movements. Co-exposure of PS and BDE-47 significantly increased feeding and oxygen consumption rates compared to control and individual compounds alone, suggesting additive or synergistic effects on energy balance, which was further supported by reduced neutral lipid reserves. Conversely, molecular gene expression data pointed to a negative interaction, as co-exposure of high PS generally abolished the induction of gene expression in response to BDE-47. Our results demonstrate that co-exposure to emerging nanoplastic contaminants and legacy contaminants results in cumulative metabolic disruption in early development in a fish model relevant to eco- and human toxicology.
Highlights
As the rapidly increasing production of plastic overwhelms the world’s ability to efficiently manage its disposal, plastic pollution has quickly become one of the most pressing environmental issues
A qualitative increase in fluorescence signal was consistently observed in the PS nanoplastic exposed groups compared to the control group in the anterior part of eleutheroembryos containing the yolk sac and digestive tract, but not the caudal part containing skeletal muscle tissue (Figure 2)
Our study reveals that nanoplastics and BDE-47 affect organismal level metabolic phenotype in zebrafish larvae and that co-exposure exacerbates this effect
Summary
As the rapidly increasing production of plastic overwhelms the world’s ability to efficiently manage its disposal, plastic pollution has quickly become one of the most pressing environmental issues. Since 2013, the global annual production of plastic has exceeded 300 million tonnes (Mt) with rates reaching as high as 368 Mt in 2019 (www.plasticseurope.org). Due to their durability, low recycling rates and poor waste management, a significant portion of the plastic produced worldwide enters and persists in marine and, to a lesser degree, freshwater aquatic ecosystems (Barnes et al, 2009; Lebreton et al, 2017). A study of microplastic pollution in the Bohai Sea, a model chosen because it is almost entirely enclosed by land and exhibits limited self-cleaning abilities, found PS to be the third most abundant plastic particle after polyethene and polypropylene (Zhang et al, 2017). Water samples obtained from the coastlines of the Canterbury region of New Zealand showed that PS made up 55% of all particles identified (Clunies-Ross et al, 2016)
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