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 4 μg/L. Meanwhile, a multi-stage ovarian transcriptome analysis under 4 μg/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 4 μg/L B[a]P significantly decreased GSI and sex steroid levels. Even 0.04 μg/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.
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Abbreviations
- PKA:
-
CAMP-dependent protein kinase
- EGFR:
-
Epidermal growth factor receptor
- GnRHR:
-
Gonadotropin-releasing hormone receptor
- MAPKAPK5:
-
MAP kinase-activated protein kinase 5
- Dax1:
-
Nuclear receptor subfamily 0 group B member 1
- CYP17:
-
Steroid 17-alpha-hydroxylase/17,20 lyase-like
- 3β-HSD:
-
3β-Hydroxysteroid dehydrogenase
- 17β-HSD:
-
17β-Hydroxysteroid dehydrogenase
- Foxl2:
-
Forkhead box protein L2
- HSP70:
-
Heat shock protein 70
- ER:
-
Estrogen receptor
- Vtg:
-
Vitellogenin
- Cav-1:
-
Caveolin-1
- Cav-3:
-
Caveolin-3
- CALM:
-
Calmodulin
- SOD:
-
Superoxide dismutase
- Topo1:
-
Topoisomerase1
- PARP1:
-
Poly [ADP-ribose] polymerase 1
- XRCC1:
-
X-ray repair cross complementing 1
- Polβ:
-
DNA polymerase beta
- LIG4:
-
DNA ligase 4
- CDC25A:
-
M-phase inducer phosphatase
- CDK7:
-
Cyclin-dependent kinase 7
- CCNC:
-
Cyclin C
- FasL:
-
Tumor necrosis factor ligand superfamily member 6
- BIRC2:
-
Inhibitor of apoptosis proteins 2
- FGFR3:
-
Fibroblast growth factor receptor 3
- COL6A3:
-
Collagen alpha 3 chain
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Funding
This work was supported by the Key Research Project of Shandong (2018) (2018GHY115007).
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Ruiyi Xu: conceptualization, methodology, investigation, formal analysis, resources, writing—original draft.
Luqing Pan: conceptualization, methodology, resources, writing—review and editing.
Yueyao Zhou: writing—review and editing, formal analysis.
Zhongyuan Gao: writing—review and editing, investigation.
Jingjing Miao: writing—review and editing.
Yingying Yang: writing—review and editing.
Dongyu Li: writing—review and editing.
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All experimental procedures were conducted in conformity with institutional guidelines for the care and use of laboratory animals, and protocols were approved by the Institutional Animal Care and Use Committee in Ocean University of China, Qingdao, China.
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Xu, R., Pan, L., Zhou, Y. et al. Reproductive toxicity induced by benzo[a]pyrene exposure: first exploration highlighting the multi-stage molecular mechanism in female scallop Chlamys farreri. Environ Sci Pollut Res 29, 48675–48693 (2022). https://doi.org/10.1007/s11356-022-19235-6
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DOI: https://doi.org/10.1007/s11356-022-19235-6