Links between mitochondrial function, whole-animal metabolic rate, telomere dynamics and swimming performance in minnows.

Abstract

The majority of fish swim by aerobic muscular force, and so there has been considerable interest in the metabolic basis for swimming. Most of this work has measured whole-body oxygen consumption as a metabolic proxy, without any quantification of the actual energy that is produced at the cellular level. In this study, we explored links between organism level metabolic rate [both standard (SMR) and maximal (MMR)], mitochondrial function [the rates of oxygen consumption associated with oxidative phosphorylation (OXPHOS) and offsetting proton leak (i.e. OXPHOS coupling efficiency; OxCE)] and swim performance (Ucrit) using the European minnow (Phoxinus phoxinus). We also measured the relative proportion of aerobic (slow-twitch) and anaerobic (fast-twitch) muscle fibres within the muscle tissue. Lastly, we measured mitochondrial reactive oxygen species (ROS) production rates and the telomere lengths of the minnows (because rates of telomere shortening are known to be influenced by ROS). We found that the critical swimming speed of a fish was unrelated to measures of mitochondrial efficiency (OxCE) or MMR, or to the proportion of aerobic fibres within the muscle mass. However, Ucrit was positively related to individual SMR and OXPHOS capacity, indicating that better swimmers are supported by a higher baseline metabolism and a greater cellular capacity for producing ATP. There was also a significant link between OxCE and rates of mitochondrial ROS production, but this was unrelated to telomere length. This study exemplifies how cellular energy production can influence overall performance.