Abstract
There is growing evidence from experimental and human epidemiological studies that many pollutants can disrupt lipid metabolism. In Arctic wildlife, the occurrence of such compounds could have serious consequences for seasonal feeders. We set out to study whether organohalogenated compounds (OHCs) could cause disruption of energy metabolism in female polar bears (Ursus maritimus) from Svalbard, Norway (n = 112). We analyzed biomarkers of energy metabolism including the abundance profiles of nine lipid-related genes, fatty acid (FA) synthesis and elongation indices in adipose tissue, and concentrations of lipid-related variables in plasma (cholesterol, high-density lipoprotein, triglycerides). Furthermore, the plasma metabolome and lipidome were characterized by low molecular weight metabolites and lipid fingerprinting, respectively. Polychlorinated biphenyls, chlordanes, brominated diphenyl ethers and perfluoroalkyl substances were significantly related to biomarkers involved in lipid accumulation, FA metabolism, insulin utilization, and cholesterol homeostasis. Moreover, the effects of pollutants were measurable at the metabolome and lipidome levels. Our results indicate that several OHCs affect lipid biosynthesis and catabolism in female polar bears. Furthermore, these effects were more pronounced when combined with reduced sea ice extent and thickness, suggesting that climate-driven sea ice decline and OHCs have synergistic negative effects on polar bears.
Highlights
Since many chemicals are lipid-soluble, it is relevant to investigate whether their concurrent and continuous presence in adipose tissues may be harmful[1]
In female polar bears, which were in a feeding state, we measured higher expressions of peroxisome-proliferator activated receptor gamma (PPARG), PGC1 and FA synthase (FASN) transcript levels (Table S1) in adipose tissue as compared to fasting bears
Several variables related to lipid metabolism remained unchanged between the two metabolic states, including PNPLA2, LIPE, ADIPOQ, Cluster of differentiation 36 (CD36) and FA binding protein 4 (FABP4) transcript levels and concentrations of cholesterol and high-density lipoprotein (HDL) (Table S1)
Summary
Since many chemicals are lipid-soluble, it is relevant to investigate whether their concurrent and continuous presence in adipose tissues may be harmful[1]. Several experimental and epidemiological studies on mammals have indicated that organohalogenated compounds (OHCs) such as polychlorinated biphenyls (PCBs), organochlorine pesticides (OCPs), polybrominated diphenyl ethers (PBDEs) and poly- and perfluoroalkyl substances (PFASs) affect lipid metabolism[15,16,17,18,19] Arctic top predators, such as polar bears (Ursus maritimus), are among the most polluted species in the world[20] and have evolved large body lipid stores in response to seasonal variation in prey availability and cold temperatures[21]. Within a few months (generally from April to July), polar bears feed actively and can accumulate up to 50% of their body mass as lipids, through consumption of seal blubber during the ringed seal (Pusa hispida) pupping and moulting periods[24] These energy stores are metabolized during periods of food scarcity or reproductive fasting. The biomarkers of energy metabolism included targeted analyses (i.e. gene transcription and FA metabolism in adipose tissue, and concentrations of lipid related variables in plasma), and non-targeted end-points such as plasma metabolome and lipidome, which are considered as final downstream products of gene transcription
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