Plasticity of mitochondrial function safeguards phosphorylating respiration during in vitro simulation of rest-phase hypothermia

Author:

García-Díaz Carmen C.ORCID,Chamkha ImenORCID,Elmér EskilORCID,Nord AndreasORCID

Abstract

ABSTRACTMany animals downregulate body temperature to save energy when resting (rest-phase hypothermia). Small birds that winter at high latitude have comparatively limited capacity for hypothermia and so pay large energy costs for thermoregulation during cold nights. Available evidence suggests this process is fuelled by adenosine triphosphate (ATP)-dependent mechanisms. Most ATP is produced by oxidative phosphorylation in the mitochondria, but mitochondrial respiration can be lower during hypothermia because of the temperature-dependence of biological processes. This can create conflict between increased organismal ATP demand and a lower mitochondrial capacity to provide it. We studied this in blood cell mitochondria of wild great tits (Parus major) by simulating rest-phase hypothermia via a 6°C reduction in assay temperature in vitro. The birds had spent the night preceding the experiment in thermoneutrality or in temperatures representing mild or very cold winter nights. Night temperature did not affect mitochondrial respiration. Across treatments, endogenous respiration was 14% lower in hypothermia. This did not reflect general thermal suppression because phosphorylating respiration was unaffected by thermal state. Instead, hypothermia was associated with a threefold reduction of leak respiration, from 17% in normothermia to 4% in hypothermia. Thus, coupling of total respiration to ATP production was 96% in hypothermia, compared to 83% in normothermia. Our study shows that thermal insensitivity of phosphorylation combined with short-term plasticity of leak respiration may safeguard ATP production when endogenous respiration is suppressed. This casts new light on the process by which small birds endure harsh winter cold and warrants future tests across tissues in vivo.

Publisher

Cold Spring Harbor Laboratory

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