Oil-induced responses of cardiac and red muscle mitochondria in red drum (Sciaenops ocellatus)

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Acute exposure to crude oil and polycyclic aromatic hydrocarbons (PAH) can severely impair cardiorespiratory function and swim performance of larval, juvenile and adult fish. Interestingly, recent work has documented an oil induced decoupling of swim performance (Ucrit) and maximum metabolic rate (MMR) whereby oil causes a decline in Ucrit without a parallel reduction in MMR. We hypothesize that this uncoupling is due to impaired mitochondrial function in swimming muscles that results in increased proton leak, and thus less ATP generated per unit oxygen. Using high resolution mitochondrial respirometry, we assessed 11 metrics of mitochondrial performance in red and cardiac muscle from permeabilized fibers isolated from red drum following control or 24 h crude oil (high energy water accommodated fractions) exposure. Two experimental series were performed, a Deepwater Horizon relevant low dose (29.6 ± 7.4 μg L−1 ∑PAH50) and a proof-of-concept high dose (64.5 ± 8.9 μg L−1 ∑PAH50). No effects were observed on any mitochondrial parameter in either tissue at the low oil dose; however, high dose exposure provided evidence of impairment in the OXPHOS respiratory control ratio and OXPHOS spare capacity in red muscle following oil exposure, as well as a shift from Complex I to Complex II during OXPHOS respiration. No effects of the high dose oil treatment were observed in cardiac muscle. As such, mitochondrial dysfunction is unlikely to be the underlying mechanism for decoupling of Ucrit and MMR following acute oil exposure in red drum. Furthermore, mitochondrial dysfunction does not appear to be a relevant toxicological impairment in juvenile red drum with respect to the Deepwater Horizon oil spill, although impairments may be observed under higher dose exposure scenarios.