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Embryonic benzophenone-3 exposure inhibited fertility in later-life female zebrafish and altered developmental morphology in offspring embryos

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Abstract

Benzophenone-3 (BP3), an organic UV filter widely used in personal care products, is ubiquitous in aquatic environments. Previous studies have shown that BP3 can interfere with oocytes development in the ovary. The current study was conducted to evaluate the effects of embryonic BP3 exposure on reproductive outcomes in later life. Zebrafish embryos were exposed to different concentrations of BP3 (0, 1, 10, 100 μg/L) for 5 days in the developmental stage and subsequently fed for 4 months without any toxins. The body length, body weight, and ovary weight in F0 female adult zebrafish and morphology indices in F1 offspring embryos were measured. The reproductive behaviors of adult zebrafish were recorded by a digital camera. HE staining was used to estimate the development of oocytes and the proportion of different phases was calculated. qPCR was used to detect the expression levels of reproduction-related genes of the hypothalamic-pituitary-gonadal (HPG) axis. Our findings revealed that the body length and body weight were not changed with embryonic BP3 exposure, but BP3 exposure inhibited the development and maturation of ovaries in later-life female zebrafish, accompanied by an increased proportion of follicles in the primary growth and early vitellogenic stages, and a decline in the full-growth stage in ovaries. Meanwhile, reduced egg production, delayed hatching rate, altered somite count and increased mortality rate were observed at 100 μg/L in offspring embryos. Behavioral results showed that BP3 exposure reduced the frequency of chasing, touching, entering the spawning area, and the duration of fish entering the spawning area later in life, qPCR analysis showed that the expression levels of reproduction-related genes of the HPG axis were downregulated in females, following a decreasing trend in plasma E2 and 11-KT levels. These results suggested that embryonic BP3 exposure negatively affected the fertility of fish and the development of their offspring embryos, which may cause potential risks to aquatic ecosystems and human health.

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The data for this study are included in this article and available from the corresponding author upon reasonable request.

Funding

This work was supported by funding from the National Natural Science Foundation of China (No. 22166014) and the Guizhou Education Department Youth Science and Technology Talents Growth Project (KY [2021]175).

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Authors and Affiliations

  1. School of Public Health, the Key Laboratory of Environmental Pollution Monitoring and Disease Control, Ministry of Education, Guizhou Medical University, Guiyang, 550025, China

    Junyan Tao, Qinyuan Yang, Min Jing, Xiaowei Sun, Linxuan Tian, Xin Huang, Xiaoli Huang, Wenlu Wan, Hui Ye, Ting Zhang & Feng Hong

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  1. Junyan Tao
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Contributions

Junyan Tao: conceptualization, investigation, data curation, formal analysis, writing—original draft, funding acquisition. Qinyuan Yang: investigation, data curation, formal analysis, writing—original draft. Min Jing: writing—review and editing. Xiaowei Sun: methodology, data curation, formal analysis. Linxuan Tian: methodology, data curation, formal analysis. Xin Huang: methodology, data curation. Xiaoli Huang: methodology, data curation. Wenlu Wan: methodology, data curation. Hui Ye: methodology. Ting Zhang: methodology. Feng Hong: conceptualization, funding acquisition, supervision, writing—review and editing.

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Correspondence to Feng Hong.

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Junyan Tao and Qinyuan Yang contributed equally to this work.

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Tao, J., Yang, Q., Jing, M. et al. Embryonic benzophenone-3 exposure inhibited fertility in later-life female zebrafish and altered developmental morphology in offspring embryos. Environ Sci Pollut Res 30, 49226–49236 (2023). https://doi.org/10.1007/s11356-023-25843-7

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