Exceptional cardiac anoxia tolerance in tilapia (Oreochromis hybrid)

Anoxic survival requires the matching of cardiac ATP supply (i.e. maximum glycolytic potential, MGP) and demand (i.e. cardiac power output, PO). We examined the idea that the previously observed in vivo downregulation of cardiac function during exposure to severe hypoxia in tilapia (Oreochromis hybrid) represents a physiological strategy to reduce routine PO to within the heart's MGP. The MGP of the ectothermic vertebrate heart has previously been suggested to be ∼70 nmol ATP s(-1) g(-1), sustaining a PO of ∼0.7 mW g(-1) at 15°C. We developed an in situ perfused heart preparation for tilapia (Oreochromis hybrid) and characterized the routine and maximum cardiac performance under both normoxic (>20 kPa O(2)) and severely hypoxic perfusion conditions (<0.20 kPa O(2)) at pH 7.75 and 22°C. The additive effects of acidosis (pH 7.25) and chemical anoxia (1 mmol l(-1) NaCN) on cardiac performance in severe hypoxia were also examined. Under normoxic conditions, cardiac performance and myocardial oxygen consumption rate were comparable to those of other teleosts. The tilapia heart maintained a routine normoxic cardiac output (Q) and PO under all hypoxic conditions, a result that contrasts with the hypoxic cardiac downregulation previously observed in vivo under less severe conditions. Thus, we conclude that the in vivo downregulation of routine cardiac performance in hypoxia is not needed in tilapia to balance cardiac energy supply and demand. Indeed, the MGP of the tilapia heart proved to be quite exceptional. Measurements of myocardial lactate efflux during severe hypoxia were used to calculate the MGP of the tilapia heart. The MGP was estimated to be 172 nmol ATP s(-1) g(-1) at 22°C, and allowed the heart to generate a PO(max) of at least ∼3.1 mW g(-1), which is only 30% lower than the PO(max) observed with normoxia. Even with this MGP, the additional challenge of acidosis during severe hypoxia decreased maximum ATP turnover rate and PO(max) by 30% compared with severe hypoxia alone, suggesting that there are probably direct effects of acidosis on cardiac contractility. We conclude that the high maximum glycolytic ATP turnover rate and levels of PO, which exceed those measured in other ectothermic vertebrate hearts, probably convey a previously unreported anoxia tolerance of the tilapia heart, but a tolerance that may be tempered in vivo by the accumulation of acidotic waste during anoxia.