Allometry of mitochondrial efficiency is set by metabolic intensity

Abstract

Metabolic activity sets the rates of individual resource uptake from the environment and resource allocations. For this reason, the relationship with body size has been heavily documented from ecosystems to cells. Until now, most of the studies used the fluxes of oxygen as a proxy of energy output without knowledge of the efficiency of biological systems to convert oxygen into ATP. The aim of this study was to examine the allometry of coupling efficiency (ATP/O) of skeletal muscle mitochondria isolated from 12 mammal species ranging from 6 g to 550 kg. Mitochondrial efficiencies were measured at different steady states of phosphorylation. The efficiencies increased sharply at higher metabolic rates. We have shown that body mass dependence of mitochondrial efficiency depends on metabolic intensity in skeletal muscles of mammals. Mitochondrial efficiency positively depends on body mass when mitochondria are close to the basal metabolic rate; however, the efficiency is independent of body mass at the maximum metabolic rate. As a result, it follows that large mammals exhibit a faster dynamic increase in ATP/O than small species when mitochondria shift from basal to maximal activities. Finally, the invariant value of maximal coupling efficiency across mammal species could partly explain why scaling exponent values are very close to 1 at maximal metabolic rates.

Coevolution of body size and metabolic rate in vertebrates: a life‐history perspective

“…However, in resting rats, non‐mitochondrial oxygen consumption accounts for approximately 10% of respiration and ranges from 2 to 21% in different organs (lowest in thymocytes and highest in the liver) (Rolfe & Brown, 1997). Moreover, 15–50% of the resting oxygen consumption is attributed to so‐called proton leak (oxygen consumption uncoupled from ATP generation; a phenomenon termed ‘uncoupling’), and this proportion sharply declines with increasing MR in muscles (Melanie et al ., 2019). Mitochondrial coupling increases with body mass in mammalian muscles, and it increases most steeply for low ATP production and least steeply for the highest ATP production (Melanie et al ., 2019).…”

“…Moreover, 15–50% of the resting oxygen consumption is attributed to so‐called proton leak (oxygen consumption uncoupled from ATP generation; a phenomenon termed ‘uncoupling’), and this proportion sharply declines with increasing MR in muscles (Melanie et al ., 2019). Mitochondrial coupling increases with body mass in mammalian muscles, and it increases most steeply for low ATP production and least steeply for the highest ATP production (Melanie et al ., 2019). The coupling also increases with body mass in frog livers (Roussel et al ., 2015).…”

Positive allometry of sexually selected traits: Do metabolic maintenance costs play an important role?

“…[22,32,33] The hypometric scaling of maintenance MR with body size is often found within and across species. [34] During periods of inactivity organisms must maintain the function of many basic cellular processes: mitochondria continue to consume oxygen when not manufacturing ATP, [35][36][37] maintaining ion gradients across cell membranes requires energy [38] and low-level biosynthesis all contribute to maintenance costs. 22] Yet these energy costs during inactivity are size-dependent-larger individuals almost always pay lower maintenance costs compared to small individuals per unit body size.…”

Cerebral cortical communication overshadows computational energy-use, but these combine to predict synapse number

“…That is, brain tissue has different uncoupling proteins which could potentially alter the amount of ATP produced per mole of glucose. Of course, different species have different issues concerning thermoregulation and thus may differ in amount of leak (see for example (83)). Such studies argue that larger animals are more efficient in regard to mitochondrial production of ATP.…”