Embryonic Crude Oil Exposure Impairs Growth and Lipid Allocation in a Keystone Arctic Forage Fish

Laurel, Benjamin J.; Copeman, Louise A.; Iseri, Paul; Spencer, Mara L.; Hutchinson, Greg; Nordtug, Trond; Donald, Carey E.; Meier, Sonnich; Allan, Sarah; Boyd, Daryle; Ylitalo, Gina M.; Cameron, James; French, Barbara L.; Linbo, Tiffany L.; Scholz, Nathaniel L.; Incardona, John P.

doi:10.1016/j.isci.2019.08.051

Cited by 51 publications

(41 citation statements)

References 47 publications

(55 reference statements)

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“…The latter may be linked to the high molecular weight PAHs which were not present in the H WSF. Enhanced toxicity after direct contact with oil and accumulation on the chorion have also been observed in medaka (Oryzias latipes) (Gonzalez-Doncel et al, 2008) and polar cod (Laurel et al, 2019), together with our results it highlight the importance of including dispersed oil in experimental exposure designs and risk assessment models (Nordtug et al, 2011).…”

Section: Oil Droplet Foulingsupporting

confidence: 84%

“…Severe oil-induced aberrations lead to early larval mortality, yet even the smaller developmental impacts can affect survival later in life (Heintz et al, 2000;Hicken et al, 2011). Recently, a study linked oil-induced changes in lipid composition and dynamics to reduced growth and survival in polar cod (Boreogadus saida) (Laurel et al, 2019). Consistently, impacts on lipid metabolism pathways have been reported in several RNAseq studies (Sørhus et al, 2017;Xu et al, 2017).…”

Section: Introductionmentioning

confidence: 70%

“…Consistently, impacts on lipid metabolism pathways have been reported in several RNAseq studies (Sørhus et al, 2017;Xu et al, 2017). Several gene expression studies have started to unravel initiating events and key events of adverse outcome pathways of crude oil (Laurel et al, 2019;Lie et al, 2019;McGruer et al, 2019;Sørhus et al, 2017), but there are still knowledge gaps in understanding the underlying mechanisms of crude oil toxicity.…”

Section: Introductionmentioning

confidence: 72%

“…Circulatory defects may also affect distribution of lipids from the yolk which in turn may affect growth in later stages. Polar cod exposed to transient low levels of oil induced dysregulation of lipid metabolism and reduced growth in morphologically normal juveniles (Laurel et al, 2019).…”

Section: Cardiac Functional Defectsmentioning

confidence: 99%

“…The disruption of ionic signaling leads to defects in cardiac rhythm and contractility Incardona et al, 2009;Sørhus et al, 2016b) as well as calcium regulated cardiomyocyte proliferation (Ebert et al, 2005;Huang et al, 2012;Rottbauer et al, 2001;Sørhus et al, 2017). Beyond these circulatory defects that affect cardiac development (Andres-Delgado and Mercader, 2016), other extra-cardiac abnormalities can be secondary to circulatory defects, including craniofacial and eye development, and osmoregulatory and lipid metabolism deficiencies (Incardona et al, 2004;Incardona and Scholz, 2016;Laurel et al, 2019;Sørhus et al, 2017;Sun et al, 2019) Numerous other pathways/endpoints have also been reported beyond the effects downstream of circulatory defects described above. PAH-related disruption of retinoid signaling interrupts eye development (Lie et al, 2019).…”

Section: Introductionmentioning

confidence: 99%

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Untangling mechanisms of crude oil toxicity: linking gene expression, morphology and PAHs at two developmental stages in a cold-water fish

Sørhus¹,

Donald²,

Dasilva

et al. 2020

Preprint

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Early life stages of fish are highly sensitive to crude oil exposure and thus, short term exposures during critical developmental periods could have detrimental consequences for juvenile survival. To obtain a broader understanding of the mechanisms behind crude oil toxicity, we administered crude oil to Atlantic haddock (Melanogrammus aeglefinus) in short term (3-day) exposures at two developmental time-points, before and after onset of heartbeat. A frequent sampling regime enabled us to determine and link immediate PAH uptake, metabolite formation and gene expression changes (cyp1a,b,c,d, bmp10, abcb1 and rhag). In general, the embryotoxic consequences were more severe in the earliest exposure, and oil droplet fouling enhanced the toxicity. This study detected circulation-independent, oil-induced gene expression changes and separated phenotypes linked to proliferation, growth and disruption of formation events at early and late developmental stages. A greater understanding of crude oil toxicity is essential for predicting the consequences of oil spills.Graphic abstractHighlightsOil droplet fouling occurred in the whole water column and increased the oil toxicity.Early exposure resulted in higher PAH uptake due to lower metabolism resulting in more severe abnormalities.A rapid and circulation-indepenent regulation of bmp10 suggested a direct oil-induced effect on calcium homeostasis.Expression of rhag indicated a direct oil-induced effect on osmoregulatory cells and osmoregulation.Severe eye abnormalities especially in the late exposure was linked to inappropriate overexpression of cyp1b in the eyes.

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Section: Oil Droplet Foulingsupporting

confidence: 84%

Section: Introductionmentioning

confidence: 70%

Section: Introductionmentioning

confidence: 72%

Section: Cardiac Functional Defectsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Untangling mechanisms of crude oil toxicity: linking gene expression, morphology and PAHs at two developmental stages in a cold-water fish

Sørhus¹,

Donald²,

Dasilva

et al. 2020

Preprint

Self Cite

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Effects of Phenanthrene Exposure on Cholesterol Homeostasis and Cardiotoxicity in Zebrafish Embryos

McGruer

Tanabe

Vliet

et al. 2021

Enviro Toxic and Chemistry

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Polycyclic aromatic hydrocarbons (PAHs) are pervasive pollutants in aquatic ecosystems, and developing fish embryos are especially sensitive to PAH exposure. Exposure to crude oil or phenanthrene (a reference PAH found in oil) produces an array of gross morphological abnormalities in developing fish embryos, including cardiotoxicity. Recently, studies utilizing transcriptomic analyses in several oil-exposed fish embryos found significant changes in the abundance of transcripts involved in cholesterol biosynthesis. Given the vital role of cholesterol availability in embryonic heart development, we hypothesized that cholesterol dysregulation in early development contributes to phenanthrene-induced cardiotoxicity. We exposed zebrafish embryos to 12 or 15 µM phenanthrene from 6 to 72 h post fertilization (hpf) and demonstrated that, in conjunction with pericardial edema and bradycardia, several genes (fdft1 and hmgcra) in the cholesterol biosynthetic pathway were significantly altered. When embryos were pretreated with a cholesterol solution from 6 to 24 hpf followed by exposure to phenanthrene from 24 to 48 hpf, the effects of phenanthrene on heart rate were partially mitigated. Despite changes in gene expression, whole-mount in situ staining of cholesterol was not significantly affected in embryos exposed to phenanthrene ranging in stage from 24 to 72 hpf. However, the 2-dimensional yolk area was significantly increased with phenanthrene exposure at 72 hpf, suggesting that lipid transport from the yolk to the developing embryo was impaired.

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Diluted Bitumen Affects Multiple Physiological Systems in Sockeye Salmon (Oncorhynchus nerka) Embryo to Juvenile Life Stages

Lin

Alderman

Gillis

et al. 2022

Enviro Toxic and Chemistry

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An understanding of the risks associated with diluted bitumen (dilbit) transport through Pacific salmon habitat necessitates the identification and quantification of hazards posed to early life stages. Sockeye from the embryo to juvenile stage (8 months old) were exposed to four concentrations of the water‐soluble fraction of Cold Lake dilbit (summer blend; concentrations of 0, 13.7, 34.7, and 124.5 μg/L total polycyclic aromatic compounds). Significant mortality (up to 18% over controls) only occurred in the embryo to swim‐up fry stage. Impaired growth was seen in the alevin, swim‐up, and juvenile stages (maximum reduction 15% in mass but not fork length). Reductions in both critical (maximum 24% reductions) and burst (maximum 47% reductions) swimming speed in swim‐up fry and juveniles were seen. Alterations in energy substrate reserves (reductions in soluble protein and glycogen content, elevations in whole‐body lipid and triglyceride levels) at all stages may underlie the effects seen in swimming and growth. Dilbit exposure induced a preexercise physiological stress response that affected the recovery of postexercise biochemistry (cortisol, glycogen, lactate, triglyceride concentrations). The transcript abundance of the cytochrome P450 1A gene (cyp1a) was quantified in alevin head regions (containing the heart) and in the hearts of swim‐up fry and juveniles and showed a concentration‐dependent increase in the expression of cyp1a at all life stages. Environ Toxicol Chem 2022;41:1937–1949. © 2022 SETAC

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Embryonic Crude Oil Exposure Impairs Growth and Lipid Allocation in a Keystone Arctic Forage Fish

Cited by 51 publications

References 47 publications

Untangling mechanisms of crude oil toxicity: linking gene expression, morphology and PAHs at two developmental stages in a cold-water fish

Untangling mechanisms of crude oil toxicity: linking gene expression, morphology and PAHs at two developmental stages in a cold-water fish

Effects of Phenanthrene Exposure on Cholesterol Homeostasis and Cardiotoxicity in Zebrafish Embryos

Diluted Bitumen Affects Multiple Physiological Systems in Sockeye Salmon (Oncorhynchus nerka) Embryo to Juvenile Life Stages

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