Balanced mitochondrial function at low temperature is linked to cold adaptation in Drosophila species

Abstract

The ability of ectothermic animals to live in different thermal environments is closely associated with their capacity to maintain physiological homeostasis across diurnal and seasonal temperature fluctuations. For chill-susceptible insects, such as Drosophila, cold tolerance is tightly linked to ion and water homeostasis obtained through a regulated balance of active and passive transport. Active transport at low temperature requires a constant delivery of ATP and we therefore hypothesize that cold-adapted Drosophila are characterized by superior mitochondrial capacity at low temperature relative cold-sensitive species. To address this, we investigated how experimental temperatures 19-1 {degrees}C affected mitochondrial substrate oxidation in flight muscle of seven tropical and temperate Drosophila species that represent a broad spectrum of cold tolerance. Mitochondrial oxygen consumption rates measured using a substrate-uncoupler-inhibitor-titration protocol showed that cooling generally reduced oxygen consumption of all steps of the electron transport system across species. Complex I is the primary consumer of oxygen at benign temperatures, but low temperature decreases complex I respiration to a much greater extent in cold-sensitive species than in cold-adapted species. Accordingly, cold-induced reduction of complex I correlates strongly with CTmin (the temperature inducing cold coma). The relative contribution of alternative substrates, proline, succinate and glycerol-3-phosphate increased as temperature decreased, particularly in the cold-sensitive species. At present it is unclear whether the oxidation of alternative substrates can be used to offset the effects of the temperature-sensitive complex I, and the potential functional consequences of such a substrate switch are discussed. Summary statementMitochondrial oxygen consumption decreases at low temperature, particularly in cold-sensitive Drosophila species, which turn to oxidation of alternative substrates as complex I-supported respiration is impaired.