Benzo(a)pyrene exposure in early life suppresses spermatogenesis in adult male zebrafish and association with the methylation of germ cell-specific genes

Abstract

Polycyclic aromatic hydrocarbons (PAHs) are environmental contaminants that are widely present in aquatic ecosystems. To assess the impact of early-life exposure to benzo[a]pyrene (BaP), a representative PAH, on reproductive ability in adult male zebrafish (Danio rerio), fertilized embryos were exposed to 0.05, 0.5, 5 and 50 nM of BaP for 96 h, and then the hatched larvae were raised to adulthood in clean water. In one-year-old male fish, the percentage of spermatozoa in testis was significantly reduced in the 0.5, 5 and 50 nM treatments. When the treated fish were mated with untreated fish, significantly decreased rate of egg fertilization and hatching success and significantly elevated malformation rate the F1 larvae were observed in the 0.5, 5 and 50 nM treatments. The transcriptional levels of genes along the brain-pituitary-gonadal axis, involving gnrh3, gnrhr3, fshβ, lhβ, lhγ, lhrγ and ar, were downregulated. In addition, embryonic BaP exposure upregulated the promotor methylation of germ cell-specific genes in the testis of adult fish. The upregulated methylation of ddx4, dnd1, nanos2 in the testis might be associated with the downregulated mRNA levels of these genes, which could be another reason for the inhibition of spermatogenesis. These results indicate that early-life exposure to BaP suppress the reproductive capability of adult male fish, which would cause a decrease in fish population.