Energy metabolism during insect flight: Biochemical design and physiological performance

Flying insects achieve the highest known mass-specific rates of O-2 consump tion in the animal kingdom. Because the flight muscles account for >90% of the organismal O2 uptake, accurate estimates of metabolic flux rates (J) in the muscles can be made. In steady state, these are equal to the net forwa rd flux rates (v) at individual steps and can be compared with flux capacit ies (V-max) measured in vitro. In flying honeybees, hexokinase and phosphof ructokinase, both nonequilibrium reactions in glycolysis, operate at large fractions of their maximum capacities (i. e., they operate at high v/V-max) . Phosphoglucoisomerase is a reversible reaction that operates near equilib rium. Despite Vmax values more than 20-fold greater than the net forward fl ux rates during flight, a close match is found between the V-max required i n vivo (estimated using the Haldane relationship) to maintain near equilibr ium and this net forward flux rate and the V-max measured in vitro under si mulated physiological conditions. Rates of organismal O-2 consumption and d ifference spectroscopy were used to estimate electron transfer rates per mo lecule of respiratory chain enzyme during flight. These are much higher tha n those estimated in mammalian muscles. Current evidence indicates that met abolic enzymes in honeybees do not display higher catalytic efficiencies th an the homologous enzymes in mammals, and the high electron transfer rates do not appear to be the result of higher enzyme densities per unit cristae surface area. A number of possible mechanistic explanations for the higher rates of electron transfer are proposed.