An integrated omic analysis of hepatic alteration in medaka fish chronically exposed to cyanotoxins with possible mechanisms of reproductive toxicity. (December 2016)

• Record Type: Journal Article
• Authors: Qiao, Qin; Le Manach, Séverine; Huet, Hélène; Duvernois-Berthet, Evelyne; Chaouch, Soraya; Duval, Charlotte; Sotton, Benoit; Ponger, Loïc; Marie, Arul; Mathéron, Lucrèce; Lennon, Sarah; Bolbach, Gérard; Djediat, Chakib; Bernard, Cécile; Edery, Marc; Marie, Benjamin
• Is Part Of: Environmental pollution. Volume 219(2016)
• Page Start: 119
• Page End: 131
• Publication Date: 2016-12
• Subjects: Microcystins -- Microcystis aeruginosa PCC 7820 -- Transcriptomics -- Proteomics -- Ingenuity pathway analysis -- Hepatic circadian rhythm perturbation; Pollution -- Periodicals; Pollution -- Environmental aspects -- Periodicals; Environmental Pollution -- Periodicals; Pollution -- Périodiques; Pollution -- Aspect de l'environnement -- Périodiques; Pollution -- Effets physiologiques -- Périodiques; Pollution; Pollution -- Environmental aspects; Periodicals; Electronic journals; 363.73
• DOI: 10.1016/j.envpol.2016.10.029
• Languages: English
• ISSNs: 0269-7491

Abstract

Abstract: Cyanobacterial blooms threaten human health as well as the population of other living organisms in the aquatic environment, particularly due to the production of natural toxic components, the cyanotoxin. So far, the most studied cyanotoxins are microcystins (MCs). In this study, the hepatic alterations at histological, proteome and transcriptome levels were evaluated in female and male medaka fish chronically exposed to 1 and 5 μg L −1 microcystin-LR (MC-LR) and to the extract of MC-producing Microcystis aeruginosa PCC 7820 (5 μg L −1 of equivalent MC-LR) by balneation for 28 days, aiming at enhancing our understanding of the potential reproductive toxicity of cyanotoxins in aquatic vertebrate models. Indeed, both MC and Microcystis extract adversely affect reproductive parameters including fecundity and egg hatchability. The liver of toxin treated female fish present glycogen storage loss and cellular damages. The quantitative proteomics analysis revealed that the quantities of 225 hepatic proteins are dysregulated. In particular, a notable decrease in protein quantities of vitellogenin and choriogenin was observed, which could explain the decrease in reproductive output. Liver transcriptome analysis through Illumina RNA-seq reveals that over 100–400 genes are differentially expressed under 5 μg L −1 MC-LR and Microcystis extract treatments, respectively. Ingenuity pathway analysis of the omic data attests that various metabolic pathways, such as energy production, protein biosynthesis and lipid metabolism, are disturbed by both MC-LR and the Microcystis extract, which could provoke the observed reproductive impairment. The transcriptomics analysis also constitutes the first report of the impairment of circadian rhythm-related gene induced by MCs. This study contributes to a better understanding of the potential consequences of chronic exposure of fish to environmental concentrations of cyanotoxins, suggesting that Microcystis extract could impact a wider range of biological pathways, compared with pure MC-LR, and even 1 μg L −1 MC-LR potentially induces a health risk for aquatic organisms. Graphical abstract: Highlights: Impaired overall protein translation process cause down-regulation of vtg and chg. Neither of MC nor the Microcystis extract causes noticeable estrogenic effects. Female fish appear to be more responsive to cyanotoxin exposures. Microcystis extract impacts more biological pathways compared with MC-LR. Hepatic circadian rhythm related genes are dysregulated by MC-containing exposures. Abstract : Hepatic alterations are responsible for reproduction impairments induced by MCs by affecting energy supply, lipid metabolism, oocyte-specific protein and circadian cycle.