Exchange of polar lipids from adults to neonates in Daphnia magna: Perturbations in sphingomyelin allocation by dietary lipids and environmental toxicants

• Published in: PloS one 2017-05, Vol.12 (5), p.e0178131
• Main Authors: Sengupta, Namrata, Reardon, Delaney C, Gerard, Patrick D, Baldwin, William S
• Format: Article
• Language: English
• Subjects: Algae; Animals; Atrazine; Atrazine - toxicity; Bioaccumulation; Biology and Life Sciences; Cholesterol; Contaminants; Daphnia - drug effects; Daphnia - growth & development; Daphnia - metabolism; Daphnia magna; Daphniidae; Diet; Dietary Fats - metabolism; Docosahexaenoic acid; Environmental toxicology; Exposure; Fatty acids; Fatty Acids, Unsaturated - metabolism; Fertility - drug effects; Fluorouracil - analogs & derivatives; Fluorouracil - toxicity; Food; Gene expression; Gene Expression Regulation; Genes; Genetic aspects; Homeostasis; Insects; Lipid metabolism; Lipid Metabolism - drug effects; Lipid Metabolism - genetics; Lipids; Liver diseases; Maturation; Medicine and Health Sciences; Metabolism; Metabolites; Newborn babies; Perturbation; Phosphatidylcholines - metabolism; Physiological aspects; Retention; Sphingomyelins - metabolism; Studies; Survival; Toxicants; Toxicology; Triclosan - toxicity; Water Pollutants, Chemical - toxicity
• ISSN: 1932-6203; 1932-6203
• DOI: 10.1371/journal.pone.0178131

Because xenosensing nuclear receptors are also lipid sensors that regulate lipid allocation, we hypothesized that toxicant-induced modulation of HR96 activity would alter lipid profiles and the balance between adult survival and neonate production following exposure in Daphnia magna. Adult daphnids were exposed to unsaturated fatty acid- and toxicant- activators or inhibitors of HR96 and later starved to test whether chemical exposure altered allocation toward survival or reproduction. The HR96 activators, linoleic acid and atrazine, decreased reproduction as expected with concomitant changes in the expression of HR96 regulated genes such as magro. The HR96 inhibitors, docosahexaenoic acid (DHA) and triclosan, increased reproduction or neonate starvation survival, respectively. However, pre-exposure to triclosan increased in neonate survival at the expense of reproductive maturation. Lipidomic analysis revealed that sphingomyelins (SM) are predominantly found in neonates and therefore we propose are important in development. DHA and triclosan increased neonatal SM, consistent with HR96's regulation of Niemann-Pick genes. While DHA altered expression of magro, Niemann-Pick 1b, mannosidase, and other HR96-regulated genes as expected, triclosan primarily perturbed sphingomyelinase and mannosidase expression indicating different but potentially overlapping mechanisms for perturbing SM. Overall, SM appears to be a key lipid in Daphnia maturation and further support was provided by carmofur, which inhibits sphingomyelin/ceramide metabolism and in turn severely represses Daphnia maturation and initial brood production. In conclusion, toxicants can perturb lipid allocation and in turn impair development and reproduction.