Variation in the link between oxygen consumption and ATP production, and its relevance for animal performance

Abstract

It is often assumed that an animal's metabolic rate can be estimated through measuring the whole-organism oxygen consumption rate. However, oxygen consumption alone is unlikely to be a sufficient marker of energy metabolism in many situations. This is due to the inherent variability in the link between oxidation and phosphorylation; that is, the amount of adenosine triphosphate (ATP) generated per molecule of oxygen consumed by mitochondria (P/O ratio). In this article, we describe how the P/O ratio can vary within and among individuals, and in response to a number of environmental parameters, including diet and temperature. As the P/O ratio affects the efficiency of cellular energy production, its variability may have significant consequences for animal performance, such as growth rate and reproductive output. We explore the adaptive significance of such variability and hypothesize that while a reduction in the P/O ratio is energetically costly, it may be associated with advantages in terms of somatic maintenance through reduced production of reactive oxygen species. Finally, we discuss how considering variation in mitochondrial efficiency, together with whole-organism oxygen consumption, can permit a better understanding of the relationship between energy metabolism and life history for studies in evolutionary ecology.

Living in flowing water increases resistance to ultraviolet B radiation

“…Our results showing that U crit increased in the absence of an increase in maximal metabolic rate and metabolic scope indicate that sustained performance is relatively independent from mitochondrial ATP supply. Exercise can also increase locomotor performance by improving muscle efficiency -that is, the amount of oxygen used for a given amount of force produced (Joyner and Coyle, 2007;Lichtwark and Wilson, 2005;Salin et al, 2015). Additionally, exercise can alter contractile properties and fatigue resistance by modulating calcium cycling dynamics and fibre-type composition (Anttila et al, 2008;Gundersen, 2011;Place et al, 2015).…”

Variation in Metabolic Rate among Individuals Is Related to Tissue-Specific Differences in Mitochondrial Leak Respiration

“…However, they may also benefit from a lower production of reactive oxygen species (ROS; Salin et al 2015b). Such a physiological trade-off between ATP and ROS may help explain the persistence of variation in metabolic rates among individuals; metabolic phenotypes can have differential effects on fitness (Burton et al 2011;Salin et al 2015a). For example, we have shown that individual brown trout with relatively higher SMR perform worse under conditions of low food availability, which may be explained by a reduced capacity to generate ATP above baseline energetic needs (Auer et al 2015c).…”

Osmoregulation, bioenergetics and oxidative stress in coastal marine invertebrates: raising the questions for future research

“…Current research on fundamental mitochondrial functioning indicates the need to analyze mitochondrial efficiency -that is, the amount of ATP generated per molecule of O 2 consumed by mitochondria -in order to correctly address energetic studies (Salin et al, 2015a). In fact, much of the O 2 consumption by mitochondria can be explained through H + pumping and leaking across internal membranes, a subject that has received much attention in the field of biomedical research.…”