Effects of environmental hypoxia on cardiac energy metabolism and performance in tilapia

Abstract

Speers-Roesch B, Sandblom E, Lau GY, Farrell AP, Richards JG. Effects of environmental hypoxia on cardiac energy metabolism and performance in tilapia. Am J Physiol Regul Integr Comp Physiol 298: R104 -R119, 2010. First published October 28, 2009 doi:10.1152/ajpregu.00418.2009.-The ability of an animal to depress ATP turnover while maintaining metabolic energy balance is important for survival during hypoxia. In the present study, we investigated the responses of cardiac energy metabolism and performance in the hypoxia-tolerant tilapia (Oreochromis hybrid sp.) during exposure to environmental hypoxia. Exposure to graded hypoxia (Ն92% to 2.5% air saturation over 3.6 Ϯ 0.2 h) followed by exposure to 5% air saturation for 8 h caused a depression of whole animal oxygen consumption rate that was accompanied by parallel decreases in heart rate, cardiac output, and cardiac power output (CPO, analogous to ATP demand of the heart). These cardiac parameters remained depressed by 50 -60% compared with normoxic values throughout the 8-h exposure. During a 24-h exposure to 5% air saturation, cardiac ATP concentration was unchanged compared with normoxia and anaerobic glycolysis contributed to ATP supply as evidenced by considerable accumulation of lactate in the heart and plasma. Reductions in the provision of aerobic substrates were apparent from a large and rapid (in Ͻ1 h) decrease in plasma nonesterified fatty acids concentration and a modest decrease in activity of pyruvate dehydrogenase. Depression of cardiac ATP demand via bradycardia and an associated decrease in CPO appears to be an integral component of hypoxia-induced metabolic rate depression in tilapia and likely contributes to hypoxic survival. fish; cardiovascular function; adenosine 5Ј-triphosphate; lipid; pyruvate dehydrogenase DURING PERIODS OF LOW OXYGEN, hypoxia-tolerant animals undergo a profound, rapid, and reversible metabolic rate depression as shown by large decreases in oxygen consumption rate (Ṁ O 2 ) and heat production (44,54). This metabolic rate depression reflects a downregulation of cellular ATP turnover to a level that can be sustained by oxygen-independent ATP production. The ability to balance ATP demand with supply and thus maintain stable cellular ATP concentration ([ATP]) is a key response ensuring hypoxic survival in tolerant animals, including many species of fishes that regularly encounter environmental hypoxia (7).A major component of the hypoxia-induced depression of ATP turnover is a reduction of cellular ATP demand, including the regulated arrest of ion pumping and anabolic pathways such as protein synthesis (30,45,49). Metabolic control analyses demonstrate, however, that ATP turnover in both active and metabolically depressed organisms can be controlled both by regulating ATP demand as well as by modulation of metabolic pathways involved in ATP supply such as mitochondrial substrate oxidation (6, 49). Our knowledge is incomplete as to how processes of ATP demand and ATP supply respond during hypoxia exposure in order to achiev...

Exceptional cardiac anoxia tolerance in tilapia (Oreochromis hybrid)

“…The severe hypoxia exposure (<0.20kPa O 2 , typicallỹ 0.07kPa O 2 , pH7.75) was achieved by gassing the perfusate with compressed medical-grade N 2 (Praxair). The water P O2 achieved for severe hypoxia exposure was 7-fold lower than the haemoglobin-O 2 P 50 of tilapia (1.45kPa) (Speers-Roesch et al, 2010), and below the venous P O2 of tilapia exposed to severe environmental hypoxia of <1kPa O 2 in vivo (B.S.-R., unpublished results). Acidotic perfusate (<0.20kPa O 2 , pH7.25) required altering the ratio of TES acid (to 5.91mmoll -1 ) and TES salt (to 4.09mmoll -1 ) in the saline in accordance with the Henderson-Hasselbalch equation.…”

“…, simulating in vivo Q under resting, normoxic conditions (Speers-Roesch et al, 2010). Q was measured by an inline electromagnetic flow probe in the output line (SWF-4, Zepeda Instruments, Seattle, WA, USA).…”

“…Tilapia lack a coronary circulation (Pieperhoff et al, 2009), and they downregulate routine cardiac activity in hypoxia in vivo (SpeersRoesch et al, 2010). Speers-Roesch and colleagues showed that tilapia (Oreochromis hybrid: Oreochromis niloticus ϫ mossambicus ϫ hornorum) exposed to 8h at a water partial pressure of oxygen (P O2 ) of 1kPa decreased f H , cardiac output (Q) and PO by 50-60% (Speers-Roesch et al, 2010), and affirmed previous claims that bradycardia is an important component of cardiac hypoxia tolerance (Farrell, 2007;Farrell and Stecyk, 2007). Further, they reported that these changes in cardiac function were associated with increases in heart lactate content and decreases in cardiac intracellular pH, and also suggested that depression of PO was necessary to match ATP demand with the limited capacity for ATP supply from anaerobic glycolysis (Speers-Roesch et al, 2010).…”

“…This allowed us to test the hypothesis that the downregulation of cardiac function seen in tilapia during exposure to low oxygen in vivo (Speers-Roesch et al, 2010) is a physiological strategy to reduce routine PO to within the MGP (Farrell and Stecyk, 2007). To accomplish our objective, an in situ perfused heart preparation was developed that generated maximum cardiac performance comparable to in vivo levels, permitting tight control of perfusion conditions and cardiac workload (Farrell et al, 1988;Farrell et al, 1989), and allowing for measurement of lactate efflux and myocardial oxygen consumption rate (V O2 ).…”

Cardiac responses to anoxia in the Pacific hagfish,Eptatretus stoutii

“…the common carp, Cyprinus carpio (Stecyk and Farrell, 2002;Stecyk et al, 2004) and the tilapia, Oreochromis hybrid sp. (Speers-Roesch et al, 2010), but the crucian carp, Carassius carassius, stands out as being tolerant of anoxia for days to weeks at temperatures of 5-8°C (Hyvärinen et al, 1985;Nilsson, 1990;Nilsson, 2001;Shoubridge and Hochachka, 1980;Stecyk et al, 2004;Vornanen and Tuomennoro, 1999). The most hypoxiatolerant elasmobranch appears to be the epaulette shark, Hemiscyllium ocellatum, which can withstand hours of severe hypoxia at 25°C Stenslokken et al, 2004;Wise et al, 1998).…”