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

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.

Spectro‐Microscopic Techniques for Studying Nanoplastics in the Environment and in Organisms

“…This lack of commercially available NPs other than PS particles led to a surge in research on the synthesis of fluorescent particles, and several groups reported protocols to generate traceable particles, either by integrating fluorescent organics or metals. [24,[68][69][70] Fluorescent particles have been used to track the capture of NPs in nanocellulose networks, [71] test the stability of NPs in digestion protocols, [72] and to study the uptake in organisms such as maize plants, [73] marine larvae, [68] diatom algae, [69] acorn barnacle, [70] daphnia magna, [74][75][76] mouse brain cells, [77] zebrafish, [78,79] and freshwater mussels. [80] It should be noted that leaching of the fluorescent dye (even from commercial particles) and autofluorescence in organic matrices might make the interpretation of results challenging or misleading, as was shown when the fluorophores alone agglomerated within zebrafish larvae and the fish larvae itself displayed green autofluorescence.…”

Biodegradation of Typical Plastics: From Microbial Diversity to Metabolic Mechanisms

“…Brominated flame retardants have become the largest market group due to their high performance and low cost [ 24 ], while organophosphorus flame retardants are also growing at a rate of 4.6% per year [ 29 ]. It has been shown that flame retardants can cause decreased immunity, metabolic disorders, and endocrine disruption in marine organisms [ 30 , 31 ]. Bisphenol A (BPA) is commonly used as a stabiliser and antioxidant for plastic and as a monomer for polycarbonate (PC) [ 32 ].…”

A mechanistic understanding of the effects of polyethylene terephthalate nanoplastics in the zebrafish (Danio rerio) embryo

“…It is also used for textile, parts of automotives and electronics 35,36 . Although, several studies addressing the toxicity of nanoplastics focused on presence of other polymer, e.g., polystyrene (PS) nanoparticles [28][29][30][31][32] , the toxicity associated with PET and toxicity mechanisms, remain largely unstudied. PET particles have been found in groundwater, drinking water, soils and sediments and in the air 30,31,35,37 .…”

“…As nanoplastics are essentially inert, their toxicity might be caused by the particulate nature (which is often altered in the biological system due to adsorption with other biomolecules) or by additives or other small organic molecules that leach out after uptake and are hazardous to human health 25,27 . In past years, most toxicological studies have focused on polystyrene nanoparticles (PS NPs) [28][29][30][31][32][33] . Studies have been carried out using human cell culture or fish larvae to address the toxicological impact of PS NPs and to understand the metabolic pathways affected at cellular and molecular level [28][29][30][31][32][33][34] .…”

“…In past years, most toxicological studies have focused on polystyrene nanoparticles (PS NPs) [28][29][30][31][32][33] . Studies have been carried out using human cell culture or fish larvae to address the toxicological impact of PS NPs and to understand the metabolic pathways affected at cellular and molecular level [28][29][30][31][32][33][34] . It has been revealed that PS NPs enter the cell…”