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Potential pathway and mechanisms underlining the immunotoxicity of benzo[a]pyrene to Chlamys farreri

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Abstract

The long-distance migration of polycyclic aromatic hydrocarbons (PAHs) promotes their release into the marine environment, posing a serious threat to marine life. Studies have shown that PAHs have significant immunotoxicity effects on bivalves, but the exact mechanism of immunotoxicity remains unclear. This paper aims to investigate the effects of exposure to 0.4, 2, and 10 μg/L of benzo(a)pyrene (B[a]P) on the immunity of Chlamys farreri under environmental conditions, as well as the potential molecular mechanism. Multiple biomarkers, including phagocytosis rate, metabolites, neurotoxicity, oxidative stress, DNA damage, and apoptosis, were adopted to assess these effects. After exposure to 0.4, 2, and 10 μg/L B[a]P, obvious concentration-dependent immunotoxicity was observed, indicated by a decrease in the hemocyte index (total hemocyte count, phagocytosis rate, antibacterial and bacteriolytic activity). Analysis of the detoxification metabolic system in C. farreri revealed that B[a]P produced B[a]P-7,8-diol-9,10-epoxide (BPDE) through metabolism, which led to an increase in the expression of protein tyrosine kinase (PTK). In addition, the increased content of neurotransmitters (including acetylcholine, γ -aminobutyric acid, enkephalin, norepinephrine, dopamine, and serotonin) and related receptors implied that B[a]P might affect immunity through neuroendocrine system. The changes in signal pathway factors involved in immune regulation indicated that B[a]P interfered with Ca2+ and cAMP signal transduction via the BPDE-PTK pathway or neuroendocrine pathway, resulting in immunosuppression. Additionally, B[a]P induced the increase in reactive oxygen species (ROS) content and DNA damage, as well as an upregulation of key genes in the mitochondrial pathway and death receptor pathway, leading to the increase of apoptosis rate. Taken together, this study comprehensively investigated the detoxification metabolic system, neuroendocrine system, and cell apoptosis to explore the toxic mechanism of bivalves under B[a]P stress.

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All data generated or analyzed during this study are included in this published article.

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Funding

This work was supported by the General Program of National Natural Science Foundation of China (32273106) and the Shandong Agricultural Major Applied Technology Innovation Project (2017-10) and supported by the Fundamental Research Funds for the Central Universities (202262009).

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Authors and Affiliations

  1. The Key Laboratory of Mariculture, Ministry of Education, Ocean University of China, Qingdao, 266003, China

    Fengjun Lei, Ning Zhang, Jingjing Miao, Ruixue Tong, Yaobing Li & Luqing Pan

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  1. Fengjun Lei
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  2. Ning Zhang
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Contributions

Fengjun Lei: conceptualization, investigation, formal analysis, resources, writing—original draft. Ning Zhang: investigation. Jingjing Miao: supervision. Ruixue Tong: investigation, resources. Yueyao Zhou: conceptualization, writing—review. Luqing Pan: conceptualization, resources, writing—review and editing.

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Correspondence to Luqing Pan.

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Lei, ., Zhang, N., Miao, J. et al. Potential pathway and mechanisms underlining the immunotoxicity of benzo[a]pyrene to Chlamys farreri. Environ Sci Pollut Res 30, 97128–97146 (2023). https://doi.org/10.1007/s11356-023-29016-4

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