Publisher Summary Actively flying insects achieve the highest metabolic rates known, and they do so in the fraction of a second required to shift from quiescence to flight. This chapter focuses on the various adaptations that make possible the high metabolic rates necessary for flight. Flight depends on the biochemical and mechanical work done by the flight muscles, which must be continually supplied with oxygen and fuel. The work of the muscles is under neural control and therefore the metabolic rate is also under neural control. Hormones participate as part of the biochemical mechanisms by which the neural commands are executed and also as part of the internal milieu supportive of flight. In larger insects, high metabolic rates and the associated heat production result in elevated body temperatures; temperature effects and temperature regulation are thus closely related to flight. Control of flight metabolism is accomplished by a complicated meshwork of neural, hormonal, and biochemical mechanisms. Control of the rate of metabolism is primarily neural, since the frequency of excitation of the flight muscles provides the primary control on the demand for metabolic performance. The metabolic machinery of the muscle is also influenced by these neural signals, since Ca ++ released by excitation modulates enzyme activity. Hormones that control the uptake of substrates and perhaps other biochemical reactions in the muscles also influence muscle metabolism.

Insect Flight Metabolism

https://dspace.library.uu.nl/bitstream/handle/1874/25136/horst_84_insect%20flight%20muscle%20metabolism.pdf;sequence=1

Insect flight muscle metabolism

Bioenergetics in aging

Amino acids have long been recognized to be prominent constituents of the hemolymph and tissue fluids of insects, accounting for more than 30% of the total osmotic activity in advanced orders (Sutcliffe, 1963). Details of the amino acid pattern have been elucidated for many species, and the results have been widely reviewed (Florkin, 1958; Wyatt, 1961; Chen, 1966; Schoffeniels and Gilles, 1970; Jeuniaux, 1971), to reveal a situation of bewildering, but seemingly controlled (Collett, 1976a), complexity. The only feature that stands out as a general, though by no means universal, characteristic of insect hemolymph is the predominance of proline and/ or of glutamate and its amide glutamine (see also more recent investigations of Barrett, 1974; Nurmi and Birt, 1974; Bailey, 1975; Barrett and Friend, 1975; Collett, 1976b; de Kort and Kramer, 1976.) The early work of Winteringham with radioactively labeled substrates indicated a high rate of turnover in amino acid pools (Winteringham and Harrison, 1956; Winteringham, 1958) and suggested that hemolymph amino acids in general, and proline and glutamate in particular, could serve as important sources of substrate for the Krebs cycle (see also reviews by Sacktor, 1961, 1974). Support for this view was provided by later work, which showed a significant depletion of proline during activity in a number of different insects (Bursell, 1963; Corrigan and Kearns, 1963; Kirsten et al, 1963; Ray, 1964; Sacktor and Wormser-Shavit, 1966; Barker and Lehner, 1972; Brouwers and de Kort, 1979). Since then, proline metabolism has been under intensive investigation, and its importance in energy metabolism has become firmly established.

The Role of Proline in Energy Metabolism

Proline can be utilized as an energy substrate during flight of Aedes aegypti females.

The only exogenous substrates oxidized by mitochondria isolated from the flight muscle of the Japanese beetle (Popillia japonica) are proline, pyruvate and glycerol 3-phosphate. The highest rate of oxygen consumption is obtained with proline. The oxidation of proline leads to the production of more NH3 than alanine, indicating a functioning glutamate dehydrogenase (EC 1.4.1.2). Studies of mitochondrial extracts confirm the presence of a very active glutamate dehydrogenase, and this enzyme is found to be activated by ADP and inhibited by ATP. These extracts also show high alanine aminotransferase activity (EC 2.6.1.2) and a uniquely active "malic' enzyme (EC 1.1.1.39). The "malic' enzyme is activated by succinate and inhibited by ATP and by pyruvate. It is suggested that the input of tricarboxylate-cycle intermediate from proline oxidation is balanced by the formation of pyruvate from malate, and the complete oxidation of the majority of the pyruvate. Studies of the steady-state concentrations of mitochondrial CoASH and CoA thioesters during proline oxidation show a high succinyl (3-carboxypropionyl)-CoA content which falls on activating respiration with ADP. There is a concomitant rise in CoASH. However, the reverse transition, from state-3 to state-4 respiration, causes only very slight changes in acylation. The reasons for this are discussed. Studies of the mitochondrial content of glutamate, 2-oxoglutarate, malate, pyruvate, citrate and isocitrate during the same phases of proline oxidation give results consistent with control at the level of glutamate dehydrogenase and isocitrate dehydrogenase during proline oxidation, with the possibility of further control at "malic' enzyme. During the oxidation of pyruvate all of the tricarboxylate-cycle intermediates and NAD(P)H follow the pattern of changes described in the blowfly (Johnson & Hansford, 1975; Hansford, 1974) and isocitrate dehydrogenase is identified as the primary site of control.?2OAuthor

R N Johnson

Papers

The nature and control of the tricarboxylate cycle in beetle flight muscle.