High-Resolution Magic Angle Spinning (HRMAS) NMR Identifies Oxidative Stress and Impairment of Energy Metabolism by Zearalenone in Embryonic Stages of Zebrafish (Danio rerio), Olive Flounder (Paralichthys olivaceus) and Yellowtail Snapper (Ocyurus chrysurus)

Toxins (Basel). 2023 Jun 15;15(6):397. doi: 10.3390/toxins15060397.

Abstract

Zearalenone (ZEA) is a mycotoxin, commonly found in agricultural products, linked to adverse health impacts in humans and livestock. However, less is known regarding effects on fish as both ecological receptors and economically relevant "receptors" through contamination of aquaculture feeds. In the present study, a metabolomics approach utilizing high-resolution magic angle spinning nuclear magnetic resonance (HRMAS NMR) was applied to intact embryos of zebrafish (Danio rerio), and two marine fish species, olive flounder (Paralichthys olivaceus) and yellowtail snapper (Ocyurus chrysurus), to investigate the biochemical pathways altered by ZEA exposure. Following the assessment of embryotoxicity, metabolic profiling of embryos exposed to sub-lethal concentrations showed significant overlap between the three species and, specifically, identified metabolites linked to hepatocytes, oxidative stress, membrane disruption, mitochondrial dysfunction, and impaired energy metabolism. These findings were further supported by analyses of tissue-specific production of reactive oxygen species (ROS) and lipidomics profiling and enabled an integrated model of ZEA toxicity in the early life stages of marine and freshwater fish species. The metabolic pathways and targets identified may, furthermore, serve as potential biomarkers for monitoring ZEA exposure and effects in fish in relation to ecotoxicology and aquaculture.

Keywords: fish; metabolomics; mycotoxins; nuclear magnetic resonance (NMR); zearalenone; zebrafish.

Publication types

  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Animals
  • Flounder* / metabolism
  • Humans
  • Magnetic Resonance Spectroscopy
  • Oxidative Stress
  • Zearalenone* / toxicity
  • Zebrafish

Substances

  • Zearalenone

Grants and funding

Aspects of this research related to yellowtail snapper were prepared by the co-authors under Award Number NA20NMF4270195 to the University of Miami from the National Oceanic and Atmospheric Administration (NOAA) Saltonstall-Kennedy Grant Program, National Marine Fisheries Service (NMFS), U.S. Department of Commerce. The statements, findings, conclusions, and recommendations are those of the authors and do not necessarily reflect the views of NOAA, NMFS, or the U.S. Department of Commerce. Research-related travel and other support for Annunziato, Lawson, and Berry was funded, in part, by a grant from the U.S. Department of Agriculture (USDA; Grant number NIFA-2017-67018-26229). The material in the present work was additionally supported by the National Science Foundation under Grant No. HRD-1547798 and Grant No. HRD-2111661. These NSF Grants were awarded to Florida International University as part of the Centers for Research Excellence in Science and Technology (CREST) Program.