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Cyanotoxins within and Outside of Microcystis aeruginosa Cause Adverse Effects in Rainbow Trout (Oncorhynchus mykiss)
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    Contaminants in Aquatic and Terrestrial Environments

    Cyanotoxins within and Outside of Microcystis aeruginosa Cause Adverse Effects in Rainbow Trout (Oncorhynchus mykiss)
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    • René S. Shahmohamadloo*
      René S. Shahmohamadloo
      School of Environmental Sciences, University of Guelph, Guelph, Ontario N1G 2W1, Canada
      Department of Integrative Biology, University of Guelph, Guelph, Ontario N1G 2W1, Canada
      *Email: [email protected]
    • Xavier Ortiz Almirall
      Xavier Ortiz Almirall
      Ministry of the Environment, Conservation and Parks, Toronto, Ontario M9P 3V6, Canada
      School of Environmental Studies, Queen’s University, Kingston, Ontario K7L 3N6, Canada
    • Denina B. D. Simmons
      Denina B. D. Simmons
      Faculty of Science, Ontario Tech University, Oshawa, Ontario L1G 0C5, Canada
    • John S. Lumsden
      John S. Lumsden
      Department of Pathobiology, University of Guelph, Guelph, Ontario N1G 2W1, Canada
    • Satyendra P. Bhavsar
      Satyendra P. Bhavsar
      Ministry of the Environment, Conservation and Parks, Toronto, Ontario M9P 3V6, Canada
      Department of Physical & Environmental Sciences, University of Toronto, Toronto, Ontario M1C 1A4, Canada
    • Trudy Watson-Leung
      Trudy Watson-Leung
      Ministry of the Environment, Conservation and Parks, Toronto, Ontario M9P 3V6, Canada
    • Angela Vander Eyken
      Angela Vander Eyken
      School of Environmental Sciences, University of Guelph, Guelph, Ontario N1G 2W1, Canada
    • Gabrielle Hankins
      Gabrielle Hankins
      School of Environmental Sciences, University of Guelph, Guelph, Ontario N1G 2W1, Canada
    • Kate Hubbs
      Kate Hubbs
      School of Environmental Sciences, University of Guelph, Guelph, Ontario N1G 2W1, Canada
      More by Kate Hubbs
    • Polina Konopelko
      Polina Konopelko
      School of Environmental Sciences, University of Guelph, Guelph, Ontario N1G 2W1, Canada
    • Michael Sarnacki
      Michael Sarnacki
      School of Environmental Sciences, University of Guelph, Guelph, Ontario N1G 2W1, Canada
    • Damon Strong
      Damon Strong
      School of Environmental Sciences, University of Guelph, Guelph, Ontario N1G 2W1, Canada
      More by Damon Strong
    • Paul K. Sibley
      Paul K. Sibley
      School of Environmental Sciences, University of Guelph, Guelph, Ontario N1G 2W1, Canada
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    Environmental Science & Technology

    Cite this: Environ. Sci. Technol. 2021, 55, 15, 10422–10431
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    https://doi.org/10.1021/acs.est.1c01501
    Published July 15, 2021
    Copyright © 2021 American Chemical Society

    Abstract

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    The global expansion of toxic Microcystis blooms, and production of cyanotoxins including microcystins, are an increasing risk to freshwater fish. Differentiating intracellular and extracellular microcystin toxicity pathways (i.e., within and outside of cyanobacterial cells) in fish is necessary to assess the severity of risks to populations that encounter harmful algal blooms in pre-to-postsenescent stages. To address this, adult and juvenile Rainbow Trout (Oncorhynchus mykiss) were, respectively, exposed for 96 h to intracellular and extracellular microcystins (0, 20, and 100 μg L–1) produced by Microcystis aeruginosa. Fish were dissected at 24 h intervals for histopathology, targeted microcystin quantification, and nontargeted proteomics. Rainbow Trout accumulated intracellular and extracellular microcystins in all tissues within 24 h, with greater accumulation in the extracellular state. Proteomics revealed intracellular and extracellular microcystins caused sublethal toxicity by significantly dysregulating proteins linked to the cytoskeletal structure, stress responses, and DNA repair in all tissues. Pyruvate metabolism in livers, anion binding in kidneys, and myopathy in muscles were also significantly impacted. Histopathology corroborated these findings with evidence of necrosis, apoptosis, and hemorrhage at similar severity in both microcystin treatments. We demonstrate that sublethal concentrations of intracellular and extracellular microcystins cause adverse effects in Rainbow Trout after short-term exposure.

    Copyright © 2021 American Chemical Society

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    Supporting Information

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    The Supporting Information is available free of charge at https://pubs.acs.org/doi/10.1021/acs.est.1c01501.

    • M. aeruginosa CPCC 300 culturing methodology; microcystin water analysis methodology; microcystin fish tissue analysis methodology; database searches and analysis of identified proteins methodology; statistical analyses; physicochemical properties of the dechlorinated tap water used in all toxicity tests; growth parameters of Rainbow Trout used during toxicity tests; physicochemical properties of the solution during toxicity tests; method variables used for separation and detection by LC-QTOF MS; two-way analysis of variance measuring the interaction between time and treatment; histopathology scoring for liver of adult Rainbow Trout; correlations between microcystins in water (MCwater) and microcystins in liver (MCliver), kidney (MCkidney), and muscle (MCmuscle), and liver somatic index (LSI) and kidney somatic index (KSI); label-free proteins with differential abundance in Rainbow Trout adults’ livers; label-free proteins with differential abundance in Rainbow Trout adults’ kidneys; label-free proteins with differential abundance in Rainbow Trout adults’ muscles; GO enrichment analysis for label-free proteins; total microcystins measured in water (μg L–1) of intracellular and extracellular treatments; and heat maps of peak areas from key functions in GO enrichment analysis (PDF)

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    Environmental Science & Technology

    Cite this: Environ. Sci. Technol. 2021, 55, 15, 10422–10431
    Click to copy citationCitation copied!
    https://doi.org/10.1021/acs.est.1c01501
    Published July 15, 2021
    Copyright © 2021 American Chemical Society

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