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Life Cycle Exposure to Environmentally Relevant Concentrations of Diphenyl Phosphate (DPhP) Inhibits Growth and Energy Metabolism of Zebrafish in a Sex-Specific Manner

  • Qiliang Chen
    Qiliang Chen
    Chongqing Key Laboratory of Animal Biology, School of Life Sciences, Chongqing Normal University, Chongqing 401331, China
    More by Qiliang Chen
  • Xiaolong Lian
    Xiaolong Lian
    Chongqing Key Laboratory of Animal Biology, School of Life Sciences, Chongqing Normal University, Chongqing 401331, China
  • Jingjing An
    Jingjing An
    Chongqing Key Laboratory of Animal Biology, School of Life Sciences, Chongqing Normal University, Chongqing 401331, China
    More by Jingjing An
  • Ningbo Geng*
    Ningbo Geng
    CAS Key Laboratory of Separation Sciences for Analytical Chemistry, Dalian Institute of Chemical Physics, Chinese Academy of Sciences, Dalian 116023, Liaoning, China
    *Email: [email protected]
    More by Ningbo Geng
  • Haijun Zhang
    Haijun Zhang
    CAS Key Laboratory of Separation Sciences for Analytical Chemistry, Dalian Institute of Chemical Physics, Chinese Academy of Sciences, Dalian 116023, Liaoning, China
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  • Jonathan K. Challis
    Jonathan K. Challis
    Toxicology Centre, University of Saskatchewan, Saskatoon S7N 5B3, SK, Canada
  • Yun Luo
    Yun Luo
    CAS Key Laboratory of Separation Sciences for Analytical Chemistry, Dalian Institute of Chemical Physics, Chinese Academy of Sciences, Dalian 116023, Liaoning, China
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  • Yaxin Liu
    Yaxin Liu
    School of Environmental and Biological Engineering, Nanjing University of Science and Technology, Nanjing 210094, Jiangsu, China
    More by Yaxin Liu
  • Guanyong Su
    Guanyong Su
    School of Environmental and Biological Engineering, Nanjing University of Science and Technology, Nanjing 210094, Jiangsu, China
    More by Guanyong Su
  • Yuwei Xie
    Yuwei Xie
    Toxicology Centre, University of Saskatchewan, Saskatoon S7N 5B3, SK, Canada
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  • Yingwen Li
    Yingwen Li
    Chongqing Key Laboratory of Animal Biology, School of Life Sciences, Chongqing Normal University, Chongqing 401331, China
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  • Zhihao Liu
    Zhihao Liu
    Chongqing Key Laboratory of Animal Biology, School of Life Sciences, Chongqing Normal University, Chongqing 401331, China
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  • Yanjun Shen
    Yanjun Shen
    Chongqing Key Laboratory of Animal Biology, School of Life Sciences, Chongqing Normal University, Chongqing 401331, China
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  • John P. Giesy
    John P. Giesy
    Toxicology Centre, University of Saskatchewan, Saskatoon S7N 5B3, SK, Canada
    Department of Veterinary Biomedical Sciences, University of Saskatchewan, Saskatoon S7N 5B4, SK, Canada
    Department of Environmental Sciences, Baylor University, Waco, Texas 76798-7266, United States
    State Key Laboratory of Pollution Control and Resource Reuse, School of the Environment, Nanjing University, Nanjing 210023, Jiangsu, China
  • , and 
  • Yufeng Gong*
    Yufeng Gong
    Toxicology Centre, University of Saskatchewan, Saskatoon S7N 5B3, SK, Canada
    *Email: [email protected]
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Cite this: Environ. Sci. Technol. 2021, 55, 19, 13122–13131
Publication Date (Web):September 15, 2021
https://doi.org/10.1021/acs.est.1c03948
Copyright © 2021 American Chemical Society

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    Abstract

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    Due to commercial uses and environmental degradation of aryl phosphate esters, diphenyl phosphate (DPhP) is frequently detected in environmental matrices and is thus of growing concern worldwide. However, information on potential adverse effects of chronic exposure to DPhP at environmentally realistic concentrations was lacking. Here, we investigated the effects of life cycle exposure to DPhP on zebrafish at environmentally relevant concentrations of 0.8, 3.9, or 35.6 μg/L and employed a dual-omics approach (metabolomics and transcriptomics) to characterize potential modes of action. Exposure to DPhP at 35.6 μg/L for 120 days resulted in significant reductions in body mass and length of male zebrafish, but did not cause those same effects to females. Predominant toxicological mechanisms, including inhibition of oxidative phosphorylation, down-regulation of fatty acid oxidation, and up-regulation of phosphatidylcholine degradation, were revealed by integrated dual-omics analysis and successfully linked to adverse outcomes. Activity of succinate dehydrogenase and protein content of carnitine O-palmitoyltransferase 1 were significantly decreased in livers of male fish exposed to DPhP, which further confirmed the proposed toxicological mechanisms. This study is the first to demonstrate that chronic, low-level exposure to DPhP can retard growth via inhibiting energy output in male zebrafish.

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    The Supporting Information is available free of charge at https://pubs.acs.org/doi/10.1021/acs.est.1c03948.

    • Detailed description on zebrafish maintenance, quantification of DPhP in water, sample preparation and instrumental analysis for pseudotargeted metabolomics, RNA isolation and sequencing, quantitative real time PCR (qRT-PCR), and a number of supporting tables and figures (PDF)

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    Cited By

    This article is cited by 6 publications.

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