Abstract
Reproductive toxicity induced by benzo[a]pyrene (B[a]P) exposure has received great ecotoxicological concerns. However, huge gaps on the molecular mechanism still exist in bivalves. In this study, reproduction-related indicators were investigated in female scallops Chlamys farreri during life cycle of proliferative, growth, mature, and spawn stages, under gradient concentrations of B[a]P at 0, 0.04, 0.4, and 4μg/L. Meanwhile, a multi-stage ovarian transcriptome analysis under 4μg/L B[a]P exposure was also conducted to elucidate the potential molecular mechanisms. The results indicated that life-cycle exposure to 0.4 and 4μg/L B[a]P significantly decreased GSI and sex steroid levels. Even 0.04μg/L B[a]P could play the adverse role in DNA integrity at the mature and spawn stages. Ovarian histological sections showed that B[a]P inhibited the maturation and release of oocytes. Through the functional enrichment analysis of differentially expressed genes (DEGs) from transcriptome data, 18 genes involved in endocrine disruption effects, DNA damage and repair, and oogenesis were selected and further determined by qRT-PCR. The downregulation of genes involved in steroidogenic and estrogen signaling pathways indicated that B[a]P could cause endocrine disruption through both receptor-dependent and receptor-independent pathways. The variations of gene expressions involved in DNA single-strand break and repair implied the presence of toxic mechanisms similar with vertebrates. Additionally, the changes of gene expressions of cell cycle, apoptosis, and cell adhesion suggested that exposure to B[a]P possibly caused the reproductive toxicity effects by affecting oogenesis. Taken together, this study was a pioneer in combining genome-wide transcriptomic analysis with its corresponding reproductive indicators (GSI, sex steroid levels, DNA single-strand break, and histological sections) to explore the bivalves' toxic mechanisms under B[a]P exposure. Meanwhile, some genes involved in estrogen signaling pathway and DNA damage were firstly analyzed in bivalves, and the expression data might be useful in establishing new hypotheses and discovering new biomarkers for marine biomonitoring.
Highlights
With the rapid pace of industrialization and frequent occurrence of marine oil spill accidents, persistent organic pollutants (POPs) are globally detectable in terrestrial and marine environment (Heskett et al 2012; Wurl and Obbard et al 2004)
Gene expression data involved in cell cycle, apoptosis and cell adhesion exhibited the possibly toxic mechanisms of oogenesis caused by B[a]P
The trends of the three sex steroids variation were similar throughout the whole experiment, that all of them continued to increase during gonadal maturation but decreased when reaching spawn stage
Summary
With the rapid pace of industrialization and frequent occurrence of marine oil spill accidents, persistent organic pollutants (POPs) are globally detectable in terrestrial and marine environment (Heskett et al 2012; Wurl and Obbard et al 2004). Polycyclic aromatic hydrocarbons (PAHs) are one of the most widespread POPs in marine ecosystem, which represent a potential health hazard to aquatic organisms (Ankley et al 2003; Kim et al 2013). Numerous studies have observed that PAHs pollution could induce adverse effects on reproduction of marine organisms, including sex reversal, delaying gonadal development and spawn probability (Chikae et al 2004; Rochman et al 2014; Vignet et al 2016). Reduction in the successful rate of reproduction as well as survival rate of outputs were observed in maternal oyster Crassostrea gigas exposed to a kind of model PAHs, benzo[a]pyrene (B[a]P), during ovarian development (Choy et al 2007). The phenomenon has attracted great concerns due to the strong evidences that PAHs possess high potential to be reproductive toxicants towards marine organisms
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