skip to main content
US FlagAn official website of the United States government
dot gov icon
Official websites use .gov
A .gov website belongs to an official government organization in the United States.
https lock icon
Secure .gov websites use HTTPS
A lock ( lock ) or https:// means you've safely connected to the .gov website. Share sensitive information only on official, secure websites.


Title: 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)
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.  more » « less
Award ID(s):
2111661
PAR ID:
10513655
Author(s) / Creator(s):
; ; ; ; ; ; ; ;
Publisher / Repository:
Toxins
Date Published:
Journal Name:
Toxins
Volume:
15
Issue:
6
ISSN:
2072-6651
Page Range / eLocation ID:
397
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Ocean acidification is occurring in conjunction with warming and deoxygenation as a result of anthropogenic greenhouse gas emissions. Multistressor experiments are critically needed to better understand the sensitivity of marine organisms to these concurrent changes. Growth and survival responses to acidification have been documented for many marine species, but studies that explore underlying physiological mechanisms of carbon dioxide (CO2) sensitivity are less common. We investigated oxygen consumption rates as proxies for metabolic responses in embryos and newly hatched larvae of an estuarine forage fish (Atlantic silverside, Menidia menidia) to factorial combinations of CO2×temperature or CO2×oxygen. Metabolic rates of embryos and larvae significantly increased with temperature, but partial pressure of CO2 (PCO2) alone did not affect metabolic rates in any experiment. However, there was a significant interaction between PCO2 and partial pressure of oxygen (PO2) in embryos, because metabolic rates were unaffected by PO2 level at ambient PCO2, but decreased with declining PO2 under elevated PCO2. For larvae, however, PCO2 and PO2 had no significant effect on metabolic rates. Our findings suggest high individual variability in metabolic responses to high PCO2, perhaps owing to parental effects and time of spawning. We conclude that early life metabolism is largely resilient to elevated PCO2 in this species, but that acidification likely influences energetic responses and thus vulnerability to hypoxia. 
    more » « less
  2. Anthropogenic climate change is projected to affect marine ecosystems by challenging the environmental tolerance of individuals. Marine fishes may be particularly vulnerable to emergent climate stressors during early life stages. Here we focus on embryos of Pacific herring(Clupea pallasii), an important forage fish species widely distributed across the North Pacific. Embryos were reared under a range of temperatures (10-16°C) crossed with twopCO2levels (600 and 2000μatm) to investigate effects on metabolism and survival. We further tested how elevatedpCO2affects critical thermal tolerance (CTmax) by challenging embryos to short-term temperature fluctuations. Experiments were repeated on embryos collected from winter and spring spawning populations to determine if spawning phenology corresponds with different limits of environmental tolerance in offspring. We found that embryos could withstand acute exposure to 20°C regardless of spawning population or incubation treatment, but that survival was greatly reduced after 2-3 hours at 25°C. We found thatpCO2had limited effects onCTmax. The survival of embryos reared under chronically warm conditions (12°, 14°, or 16°C) was significantly lower relative to 10°C treatments in both populations. Oxygen consumption rates (MO2) were also higher at elevated temperatures andpCO2levels. However, heart contraction measurements made 48 hours afterCTmaxexposure revealed a greater increase in heart rate in embryos reared at 10°C compared to 16°C, suggesting acclimation at higher incubation temperatures. Our results indicate that Pacific herring are generally tolerant ofpCO2but are vulnerable to acute temperature stress. Importantly, spring-spawning embryos did not clearly exhibit a higher tolerance to heat stress compared to winter offspring. 
    more » « less
  3. Polyunsaturated aldehydes (PUAs) are secondary oxylipins produced by some diatoms. PUAs are produced at a greater rate when diatom cells are damaged, suggesting that they may act as chemical grazing deterrents. Past studies showed the deleterious effects of particulate PUAs on diatom consumers like copepods and marine invertebrates. However, to date, very few studies have explored the potential for diatom-derived PUAs to affect marine vertebrates, such as forage fishes. Forage fishes are a foundational functional group in marine ecosystems whose early life history stages are often sympatric with diatoms due to their nearshore spawning behavior and planktivorous diet. In this study, I addressed the question of whether PUAs detrimentally affect a common Salish Sea forage fish, the surf smelt (Hypomesus pretiosus; Girard 1854). The project focused on determining whether PUAs affect the development and physiology of surf smelt embryos and larvae. This was done by measuring survival and hatch success rates, embryonic heart rates, usage of endogenous energy reserves, and morphological features at hatch. Higher concentrations of PUAs resulted in higher mortality and lower hatch success rates of embryonic surf smelt. Embryonic heart rates were equivalent among treatments when embryos were exposed to PUAs soon after fertilization, suggesting that surf smelt embryos can acclimate to PUAs if exposed during early development. However, higher concentrations of PUAs significantly lowered the heart rates of embryos that were exposed to PUAs days after fertilization. Exposure to PUAs diminished the consumption rate of endogenous energy reserves, and the overall size of surf smelt at hatch was reduced. Our results indicate that exposure to dissolved PUAs could impair the fitness of ecologically foundational forage fish early life history stages. Negative effects that manifest into low adult population sizes will have cascading effects on marine ecosystems. 
    more » « less
  4. Abstract Background The teleost fish Fundulus heteroclitus inhabit estuaries heavily polluted with persistent and bioaccumulative chemicals. While embryos of parents from polluted sites are remarkably resistant to toxic sediment and develop normally, embryos of parents from relatively clean estuaries, when treated with polluted sediment extracts, are developmentally delayed, displaying deformities characteristic of pollution-induced embryotoxicity. To gain insight into parental effects on sensitive and resistant phenotypes during late organogenesis, we established sensitive, resistant, and crossed embryo families using five female and five male parents from relatively clean and predominantly PAH-polluted estuaries each, measured heart rates, and quantified individual embryo expression of 179 metabolic genes. Results Pollution-induced embryotoxicity manifested as morphological deformities, significant developmental delays, and altered cardiac physiology was evident among sensitive embryos resulting from crosses between females and males from relatively clean estuaries. Significantly different heart rates among several geographically unrelated populations of sensitive, resistant, and crossed embryo families during late organogenesis and pre-hatching suggest site-specific adaptive cardiac physiology phenotypes relative to pollution exposure. Metabolic gene expression patterns (32 genes, 17.9%, at p < 0.05; 11 genes, 6.1%, at p < 0.01) among the embryo families indicate maternal pollutant deposition in the eggs and parental effects on gene expression and metabolic alterations. Conclusion Heart rate differences among sensitive, resistant, and crossed embryos is a reliable phenotype for further explorations of adaptive mechanisms. While metabolic gene expression patterns among embryo families are suggestive of parental effects on several differentially expressed genes, a definitive adaptive signature and metabolic cost of resistant phenotypes is unclear and shows unexpected sensitive-resistant crossed embryo expression profiles. Our study highlights physiological and metabolic gene expression differences during a critical embryonic stage among pollution sensitive, resistant, and crossed embryo families, which may contribute to underlying resistance mechanisms observed in natural F. heteroclitus populations living in heavily contaminated estuaries. 
    more » « less
  5. Abstract A major challenge in ART is to select high-quality oocytes and embryos. The metabolism of oocytes and embryos has long been linked to their viability, suggesting the potential utility of metabolic measurements to aid in selection. Here, we review recent work on noninvasive metabolic imaging of cumulus cells, oocytes, and embryos. We focus our discussion on fluorescence lifetime imaging microscopy (FLIM) of the autofluorescent coenzymes NAD(P)H and flavine adenine dinucleotide (FAD+), which play central roles in many metabolic pathways. FLIM measurements provide quantitative information on NAD(P)H and FAD+ concentrations and engagement with enzymes, leading to a robust means of characterizing the metabolic state of cells. We argue that FLIM is a promising approach to aid in oocyte and embryo selection. 
    more » « less