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

Abstract

Many small animals routinely regulate resting body temperature several degrees below active-phase levels (rest-phase hypothermia), which reduces heat transfer rate and tissue oxygen demand and so may confer energy savings. Small birds that winter at high latitude show limited capacity for rest-phase hypothermia, meaning they cannot avoid upregulating heat production when facing winter cold. Substrates for upholding body temperature are provided by mitochondria in the form of adenosine triphosphate (ATP), but mitochondrial respiration is probably lower during hypothermia because of the temperature-dependence of biological processes (i.e., Q10 effect). Thus, there could be a conflict between increased organismal fuel demand and a lower mitochondrial capacity to provide it during rest-phase hypothermia. We studied this enigma by assessing mitochondrial function in the blood cells of wintering great tits (Parus major) that had spent the preceding night in warm, mild, or cold temperatures, at each of a hypothermic and a normothermic thermal state in vitro. Hypothermia reduced mitochondrial respiration by 13 %. However, this did not affect respiration allocated to oxidative phosphorylation, because hypothermia was also associated with a reduction in non-phosphorylating respiration, from 17 % in normothermia to 4 % in hypothermia. The proportion of non-phosphorylating respiration also decreased in response to colder night temperatures Thus, the coupling efficiency between electron transport and ATP production in maximally stimulated cells increased from 91% in normothermia to 98% in hypothermia. Our study shows that mitochondrial function can be highly plastic on short temporal scales. Thus, functional changes in the electron transport system might safeguard ATP production at lower tissue temperatures and when organismal demand for fuel increases in cold winter temperatures.

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

“…This is achieved by maintaining a specific ratio between contraction kinetics and cycle duration, regardless of if the muscle is activated through a single stimulus or through a burst of stimuli (Askew and Marsh, 2001;Gladman and Askew, 2022;Marsh, 1990). Girgenrath and Marsh (1999) emphasised the close link between muscle operating frequency and twitch duration across a range of taxa and demonstrated…”

“…The flight muscle of many insects performs best at temperatures ≥35°C (Wilmsen and Dzialowski, 2023), 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 ≤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.…”

“…; Mardini et al, 1987), rat (Rattus norvegicus) TA muscle (McMullen and Andrade, 2006), human (Homo sapiens) TA and cricoarytenoid (CA) muscles (D'Antona et al, 2002;Sciote et al, 2002), dog (Canis familiaris) TA, CA and transverse arytenoid (AT) muscles (Alipour and Titze, 1999;Toniolo et al, 2007), and in the tensor chordarum, external and internal oblique trunk muscles of the hylid frogs (Hyla spp.) (Girgenrath and Marsh, 1999;Girgenrath and Marsh, 2003;McLister et al, 1995). However, these muscles are all slower than avian superfast syrinx muscles.…”

A whole blood approach improves speed and accuracy when measuring mitochondrial respiration in intact avian blood cells

“…12,13 Studies on birds have found that this makes it possible to assess mitochondrial function even from small (25-50 μl) blood samples [14][15][16] that can be safely collected in organisms <5 g. 17 This is not possible when measurements are performed using other mitochondria-rich blood cells, as is necessary in mammals. 18,19 Several recent bird studies indicate that blood cell respiration varies predictably in line with organismal-level energy demand over long 16,20 and short 21 time frames, and in the contexts of seasonal adaptation 22 and metabolic senescence. 23 Moreover, blood cell mitochondrial function seems amenable to epigenetic programming during embryonic development, 24,25 much like what is a well-known fact within human medicine.…”

A whole blood approach improves speed and accuracy when measuring mitochondrial respiration in intact avian hematocytes

“…2019; Casagrande et al . 2020) and short (García-Díaz et al 2022) time frames, and in the contexts of seasonal adaptation (Nord et al . 2021) and metabolic senescence (Dawson & Salmón 2020).…”