Abstract
Heat production serves as the standard measurement for the determination of energy expenditure and efficiency in animals. Estimations of metabolic heat production have traditionally focused on gas exchange (oxygen uptake and carbon dioxide production) although direct heat measurements may include an anaerobic component particularly when carbohydrate is oxidized. Stoichiometric interpretations of the ratio of carbon dioxide production to oxygen uptake suggest that both anaerobic and aerobic heat production and, by inference, all energy expenditure – can be accounted for with a measurement of oxygen uptake as 21.1 kJ per liter of oxygen. This manuscript incorporates contemporary bioenergetic interpretations of anaerobic and aerobic ATP turnover to promote the independence of these disparate types of metabolic energy transfer: each has different reactants and products, uses dissimilar enzymes, involves different types of biochemical reactions, takes place in separate cellular compartments, exploits different types of gradients and ultimately each operates with distinct efficiency. The 21.1 kJ per liter of oxygen for carbohydrate oxidation includes a small anaerobic heat component as part of anaerobic energy transfer. Faster rates of ATP turnover that exceed mitochondrial respiration and that are supported by rapid glycolytic phosphorylation with lactate production result in heat production that is independent of oxygen uptake. Simultaneous direct and indirect calorimetry has revealed that this anaerobic heat does not disappear when lactate is later oxidized and so oxygen uptake does not adequately measure anaerobic efficiency or energy expenditure (as was suggested by the "oxygen debt" hypothesis). An estimate of anaerobic energy transfer supplements the measurement of oxygen uptake and may improve the interpretation of whole-body energy expenditure.
Highlights
"...(animals) take up oxygen and complex compounds made by plants, discharge these compounds largely in the form of carbonic acid (CO2)and water as the products of combustion and partly as simpler reduced products, consuming a certain quantity of chemical potential energy, and generate thereby heat and mechanical energy"
The focus on oxygen uptake follows from the extensive involvement of mitochondria in ATP re-synthesis accompanied by concomitant heat production [5,6,7,8]
If heat serves as the standard measure of energy expenditure anaerobic energy transfer, rapid glycolysis and glycogenolysis with lactate production has the potential to make significant contributions to cellular energy expenditure
Summary
"...(animals) take up oxygen and complex compounds made by plants, discharge these compounds largely in the form of carbonic acid (CO2)and water as the products of combustion and partly as simpler reduced products, consuming a certain quantity of chemical potential energy, and generate thereby heat and mechanical energy" The application of energy conservation as expressed in Hess's law (reactions that start and end with the same reactants and products produce the same amount of enthalpy regardless of path) led to the idea that anaerobic energy expenditure during exercise could be measured via subsequent oxygen uptake during the recovery from exercise, as part of the so-called "oxygen debt" [37] This hypothesis proposes that all ATP re-synthesized via glycolytic phosphorylation is included in the net aerobic ATP yield when pyruvate undergoes subsequent aerobic oxidation (36 ATP; 21.1 kJ per l O2), even if it passes transiently through lactate. Rapid glycolytic ATP re-synthesis with lactate production can exceed mitochondrial rates and under these conditions the efficiency of anaerobic energy transfer can not be interpreted using gas exchange stoichiometry. The interpretation of efficiency and energy expenditure may be improved if a separate estimate of anaerobic ATP turnover is provided along with a measure of oxygen uptake
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