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

Abstract

Many animals downregulate body temperature to save energy when resting (rest‐phase hypothermia). Small birds that winter at high latitudes have comparatively limited capacity for hypothermia and so pay large energy costs for thermoregulation during cold nights. Available evidence suggests this process is fueled by adenosine triphosphate (ATP)‐dependent mechanisms. Most ATP is produced by oxidative phosphorylation in the mitochondria, but mitochondrial respiration may 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, but night temperatures never affected mitochondrial respiration. However, across temperature groups, endogenous respiration was 14% lower in hypothermia. This did not reflect general thermal suppression of mitochondrial function 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, the coupling of total respiration to ATP production was 96% in hypothermia, compared to 83% in normothermia. Our study shows that the 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.

Mitochondrial ATP synthesis is essential for efficient gametogenesis inPlasmodium falciparum

“…Potentially, as gametocytes cool from 37°C in the human host to ambient temperature in the mosquito gut, the rate of parasite glycolysis decreases to such an extent that it cannot keep up with demand for ATP. In mammalian systems, a decrease in mitochondrial respiration rates caused by hypothermia is counteracted by an increase in efficiency of respiration thought to be linked to reduction of proton leak across the mitochondrial membrane 31,32 . It is tempting to speculate that such a mitochondrial system could also play a role in optimising ATP production in the parasite under the cooler conditions of the mosquito.…”

Male and female syringeal muscles exhibit superfast shortening velocities in zebra finches

“…High-frequency muscles of birds and bats are likely optimised to operate at similar body temperatures: when operating outside of these temperatures, we see greatly reduced force output, such as with the pectoralis muscle of hummingbirds, where drastic temperature reductions of ≤20°C produce substantially reduced force ( Reiser et al, 2013 ). Even in endotherms, such significant reductions of body temperature are commonly seen and behaviourally relevant: small passerines reduce body temperature 5–10°C during the winter ( Brodin et al, 2017 ; García-Díaz et al, 2023 ; Ruf and Geiser, 2015 ), and hummingbirds and bats reduce body temperature by ≤20°C during daily torpor to reduce energetic costs ( Luo et al, 2021 ; Shankar et al, 2022 ). The underlying muscle mechanics may now affect behavioural performance.…”

Male and female syringeal muscles exhibit superfast shortening velocities in Zebra finches

“…This is also shown e.g in hummingbird pectoralis muscle., where drastic temperature reductions of ≤20°C produce substantially reduced force (Reiser et al, 2013). Even in endotherms, such significant reduction of body temperature are commonly seen and behaviourally relevant: Small passerines reduce body temperature 5-10°C during the winter (Brodin et al, 2017;García-Díaz et al, 2023;Ruf and Geiser, 2015) and hummingbirds and bats reduce body temperature ≤20°C during daily torpor to reduce energetic costs (Luo et al, 2021;Shankar et al, 2022). The underlying muscle mechanics may now affect behavioural performance.…”