Changes in lipid profiles in Daphnia magna individuals exposed to low environmental levels of neuroactive pharmaceuticals

Abstract

Disruptive effects of chemicals on lipids in aquatic species are mostly limited to obesogens and vertebrates. Recent studies reported that antidepressants, anxiolytic, antiepileptic and β-adrenergic pharmaceuticals, with putative distinct mechanisms of action at low environmental relevant concentrations, up-regulated common neurological and lipid metabolic pathways and enhanced similarly reproduction in the crustacean Daphnia magna. Conversely CRISPR mutants for the tryptophan hydrolase enzyme gene (TRH) that lack serotonin had the opposed phenotype: the lipid metabolism down-regulated and impaired reproduction. Lipid metabolism is strongly linked to reproduction in D. magna. The aim of this study is to test if the above mentioned neuro-active chemicals disrupted common lipid groups and showed also the opposed lipidomic effects as those individuals lacking serotonin. This study used ultra-high performance liquid chromatography/time-of-flight mass spectrometry (UHPLC/TOFMS) to study how neuro-active chemicals (carbamazepine, diazepam, fluoxetine and propranolol) at low (0.1 μg/L) and higher concentrations (1 μg/L) and three CRISPR TRH mutant clones disrupt the dynamics of glycerophospholipids and glycerolipids in Daphnia adults. Lipidomic analysis identified 267 individual lipids corresponding to three classes of glycerolipids, eleven of glycerophospholipids, one of sterols and one of sphingolipids, of which 132 and 125 changed according to the chemical treatments or across clones, respectively. Most pharmaceutical treatments enhanced reproduction whereas mutated clones lacking serotonin reproduced to a lesser extent. Except for carbamazepine, most of the tested pharmaceuticals increased some triacylglycerol species and decreased monoacylglycerols, lysophospholipids, sphingomyelins and cholesterol esters in exposed females. Opposed lipidomic pattern was observed in mutated clones lacking serotonin. Lipidomic data, thus, indicate a close link between reported transcriptomic and lipidomic changes, which are likely related to serotonin and other neurological signalling pathways.