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Mechanisms of pH-Dependent Uptake of Ionizable Organic Chemicals by Fish from Oil Sands Process-Affected Water (OSPW)

  • Markus Brinkmann*
    Markus Brinkmann
    School of Environment and Sustainability (SENS), University of Saskatchewan, 44 Campus Drive, Saskatoon S7N 5C8, Canada
    Toxicology Centre, University of Saskatchewan, Saskatoon S7N 5B3, Canada
    Global Institutes for Water Security (GIWS), University of Saskatchewan, Saskatoon S7N 3H5, Canada
    *Email: [email protected]. Tel: +1 (306) 966 1204. Fax: +1 (306) 931 1664.
  • Hattan Alharbi
    Hattan Alharbi
    Department of Plant Protection, College of Food and Agriculture Sciences, King Saud University, Riyadh 11451, Saudi Arabia
  • Ulyana Fuchylo
    Ulyana Fuchylo
    Toxicology Centre, University of Saskatchewan, Saskatoon S7N 5B3, Canada
  • Steve Wiseman
    Steve Wiseman
    Department of Biological Sciences, University of Lethbridge, Lethbridge T1K 3M4, Canada
  • Garrett Morandi
    Garrett Morandi
    Toxicology Centre, University of Saskatchewan, Saskatoon S7N 5B3, Canada
  • Hui Peng
    Hui Peng
    Toxicology Centre, University of Saskatchewan, Saskatoon S7N 5B3, Canada
    Department of Chemistry, University of Toronto, Toronto M5S 3H6, Canada
    More by Hui Peng
  • John P. Giesy
    John P. Giesy
    Toxicology Centre, University of Saskatchewan, Saskatoon S7N 5B3, Canada
    Department of Veterinary Biomedical Sciences, University of Saskatchewan, Saskatoon S7N 5B4, Canada
    Department of Zoology and Center for Integrative Toxicology, Michigan State University, East Lansing, Michigan 48824, United States
    Department of Environmental Sciences, Baylor University, Waco, Texas 76706, United States
  • Paul D. Jones
    Paul D. Jones
    School of Environment and Sustainability (SENS), University of Saskatchewan, 44 Campus Drive, Saskatoon S7N 5C8, Canada
    Toxicology Centre, University of Saskatchewan, Saskatoon S7N 5B3, Canada
  • , and 
  • Markus Hecker
    Markus Hecker
    School of Environment and Sustainability (SENS), University of Saskatchewan, 44 Campus Drive, Saskatoon S7N 5C8, Canada
    Toxicology Centre, University of Saskatchewan, Saskatoon S7N 5B3, Canada
Cite this: Environ. Sci. Technol. 2020, 54, 15, 9547–9555
Publication Date (Web):July 8, 2020
https://doi.org/10.1021/acs.est.0c02522
Copyright © 2020 American Chemical Society

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    Abstract

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    Uptake and effects of ionizable organic chemicals (IOCs) that are weak acids in aqueous solution by fish can differ as a function of pH. While the pH-dependent behavior of select IOCs is well-understood, complex mixtures of IOCs, e.g., from oil sands process-affected water (OSPW), have not yet been studied systematically. Here, we established an in vitro screening method using the rainbow trout gill cell line, RTgill-W1, to investigate pH-dependent cytotoxicity and permeation of IOCs across cultured epithelia using ultra-high-performance liquid chromatography with high-resolution mass spectrometry (UPLC-HRMS). The assay was benchmarked using model chemicals and technical mixtures, and then used to characterize fractions and reconstituted extracts of field-collected OSPW. Significant pH-dependent cytotoxicity of individual IOCs, acidic fractions, and reconstituted extracts of OSPW was observed. In vitro data were in good agreement with data from a 96 h in vivo exposure experiment with juvenile rainbow trout. Permeation of some IOCs from OSPW was mediated by active transport, as revealed by studies in which inhibitors of these active transport mechanisms were applied. We conclude that the RTgill-W1 in vitro assay is useful for the screening of pH-dependent uptake of IOCs in fish, and has applications for in vitroin vivo extrapolation, and prioritization of chemicals in nontarget screenings.

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    The Supporting Information is available free of charge at https://pubs.acs.org/doi/10.1021/acs.est.0c02522.

    • Cytotoxicity and epithelial permeability of other ionizable organic chemicals, as well as changes in transepithelial electric resistance over time; cytotoxicities of six ionizable organic chemicals in the cell line RTgill-W1 (Figure S1); changes in transepithelial electrical resistance (TEER) after changing the pH of exposure media in the apical chamber of culture inserts containing established RTgill-W1 epithelia (Figure S2); relative permeabilities of dicyclohexylacetic acid (A) and nonylphenol technical mixture of isomers (B) at different pHs of exposure media in the apical chamber (Figure S3) (PDF)

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    Cited By

    This article is cited by 8 publications.

    1. Timothy M. C. Leshuk, Zachary W. Young, Brad Wilson, Zi Qi Chen, Danielle A. Smith, Greg Lazaris, Mary Gopanchuk, Sean McLay, Corin A. Seelemann, Theo Paradis, Asfaw Bekele, Rodney Guest, Hafez Massara, Todd White, Warren Zubot, Daniel J. Letinski, Aaron D. Redman, D. Grant Allen, Frank Gu. A Light Touch: Solar Photocatalysis Detoxifies Oil Sands Process-Affected Waters Prior to Significant Treatment of Naphthenic Acids. ACS ES&T Water 2024, 4 (4) , 1483-1497. https://doi.org/10.1021/acsestwater.3c00616
    2. Fabian Balk, Bastian Hüsser, Juliane Hollender, Kristin Schirmer. Bioconcentration Assessment of Three Cationic Surfactants in Permanent Fish Cell Lines. Environmental Science & Technology 2024, 58 (3) , 1452-1461. https://doi.org/10.1021/acs.est.3c05360
    3. Ling Zhang, Bryan W. Brooks, Fen Liu, Zhimin Zhou, Huizhen Li, Jing You. Human Apparent Volume of Distribution Predicts Bioaccumulation of Ionizable Organic Chemicals in Zebrafish Embryos. Environmental Science & Technology 2022, 56 (16) , 11547-11558. https://doi.org/10.1021/acs.est.2c03421
    4. Ulyana Fuchylo, Hattan A. Alharbi, Alper James Alcaraz, Paul D. Jones, John P. Giesy, Markus Hecker, Markus Brinkmann. Inflammation of Gill Epithelia in Fish Causes Increased Permeation of Petrogenic Polar Organic Chemicals via Disruption of Tight Junctions. Environmental Science & Technology 2022, 56 (3) , 1820-1829. https://doi.org/10.1021/acs.est.1c05839
    5. Elisabeth Dohmann Chang, Raewyn M. Town, Stewart F. Owen, Christer Hogstrand, Nic R. Bury. Effect of Water pH on the Uptake of Acidic (Ibuprofen) and Basic (Propranolol) Drugs in a Fish Gill Cell Culture Model. Environmental Science & Technology 2021, 55 (10) , 6848-6856. https://doi.org/10.1021/acs.est.0c06803
    6. Justin Scott, Matteo Minghetti. Characterization of RTgill-W1 cells epithelial development on transwell inserts: Evaluation of osmotic and toxic challenges. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology 2023, 270 , 109638. https://doi.org/10.1016/j.cbpc.2023.109638
    7. Lei Hu, Wenbin Jiang, Xuesong Xu, Huiyao Wang, Kenneth C. Carroll, Pei Xu, Yanyan Zhang. Toxicological characterization of produced water from the Permian Basin. Science of The Total Environment 2022, 815 , 152943. https://doi.org/10.1016/j.scitotenv.2022.152943
    8. Ana Sharelys Cardenas Perez, Jonathan K. Challis, Xiaowen Ji, John Giesy, Markus Brinkmann. Impacts of Wastewater Effluents and Seasonal Trends on Levels of Antipsychotic Pharmaceuticals in Water and Sediments from Two Cold-Region Rivers. SSRN Electronic Journal 2022, 599 https://doi.org/10.2139/ssrn.4145441