Acute crude oil exposure alters mitochondrial function and ADP affinity in cardiac muscle fibers of young adult Mahi-mahi (Coryphaena hippurus)

Amanda Reynolds Kirby, Georgina K. Cox, Derek Nelson, Rachael M. Heuer, John Stieglitz, Daniel D Benetti, Martin Grosell, Dane A. Crossley

Research output: Contribution to journalArticle

3 Citations (Scopus)

Abstract

Mitochondrial function is critical to support aerobic metabolism through the production of ATP, and deficiencies in mitochondrial bioenergetics will directly impact the performance capacity of highly aerobic tissues such as the myocardium. Cardiac function in fish has been shown to be negatively affected by crude oil exposure, however, the mechanism for this adverse response is largely unexplored. We hypothesized that lipophilic polycyclic aromatic hydrocarbons (PAHs) found in crude oil disrupt the electron transport system (ETS) ultimately leading to mitochondrial dysfunction. In this study, mitochondrial respiration and ADP affinity we measured using high resolution respirometery in permeabilized cardiac muscle fibers of young adult Mahi-mahi (Coryphaena hippurus) after an acute (24 h) whole animal crude oil exposure. Oil exposure reduced both complex I-fueled ADP stimulated respiration (OXPHOSCI) and complex I,II-fueled ADP stimulated respiration (OXPHOSCI, CII) by 33%,while complex II-fueled ADP stimulated respiration (OXPHOSCII) was reduced by 25%. These changes were found without changes in enzyme activity or mitochondrial density between control and oil exposed Mahi. Additionally, mitochondrial affinity for ADP was decreased three-fold after acute exposure to crude oil. We purpose that acute crude oil exposure selectively impairs mitochondrial complexes of the electron transport system and ATP supply to the cell. This limited ATP supply could present several challenges to a predatory animal like the mahi; including a reliance on anaerobic metabolism and ultimately cell or tissue death as metabolic substrates are rapidly depleted. However, the impact of this impairment may only be evident under periods of increased aerobic metabolic demand.

Original languageEnglish (US)
Pages (from-to)88-95
Number of pages8
JournalComparative Biochemistry and Physiology Part - C: Toxicology and Pharmacology
Volume218
DOIs
StatePublished - Apr 1 2019

Fingerprint

Perciformes
Petroleum
Adenosine Diphosphate
Muscle
Young Adult
Myocardium
Respiration
Fibers
Adenosine Triphosphate
Electron Transport
Metabolism
Oils
Animals
Tissue
Anaerobiosis
Polycyclic Aromatic Hydrocarbons
Enzyme activity
Fish
Energy Metabolism
Fishes

Keywords

  • Enzyme kinetics
  • Mitochondrial respiration
  • Oil exposure

ASJC Scopus subject areas

  • Biochemistry
  • Physiology
  • Toxicology
  • Cell Biology
  • Health, Toxicology and Mutagenesis

Cite this

Acute crude oil exposure alters mitochondrial function and ADP affinity in cardiac muscle fibers of young adult Mahi-mahi (Coryphaena hippurus). / Kirby, Amanda Reynolds; Cox, Georgina K.; Nelson, Derek; Heuer, Rachael M.; Stieglitz, John; Benetti, Daniel D; Grosell, Martin; Crossley, Dane A.

In: Comparative Biochemistry and Physiology Part - C: Toxicology and Pharmacology, Vol. 218, 01.04.2019, p. 88-95.

Research output: Contribution to journalArticle

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abstract = "Mitochondrial function is critical to support aerobic metabolism through the production of ATP, and deficiencies in mitochondrial bioenergetics will directly impact the performance capacity of highly aerobic tissues such as the myocardium. Cardiac function in fish has been shown to be negatively affected by crude oil exposure, however, the mechanism for this adverse response is largely unexplored. We hypothesized that lipophilic polycyclic aromatic hydrocarbons (PAHs) found in crude oil disrupt the electron transport system (ETS) ultimately leading to mitochondrial dysfunction. In this study, mitochondrial respiration and ADP affinity we measured using high resolution respirometery in permeabilized cardiac muscle fibers of young adult Mahi-mahi (Coryphaena hippurus) after an acute (24 h) whole animal crude oil exposure. Oil exposure reduced both complex I-fueled ADP stimulated respiration (OXPHOSCI) and complex I,II-fueled ADP stimulated respiration (OXPHOSCI, CII) by 33{\%},while complex II-fueled ADP stimulated respiration (OXPHOSCII) was reduced by 25{\%}. These changes were found without changes in enzyme activity or mitochondrial density between control and oil exposed Mahi. Additionally, mitochondrial affinity for ADP was decreased three-fold after acute exposure to crude oil. We purpose that acute crude oil exposure selectively impairs mitochondrial complexes of the electron transport system and ATP supply to the cell. This limited ATP supply could present several challenges to a predatory animal like the mahi; including a reliance on anaerobic metabolism and ultimately cell or tissue death as metabolic substrates are rapidly depleted. However, the impact of this impairment may only be evident under periods of increased aerobic metabolic demand.",
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