The relationships between growth rate and mitochondrial metabolism varies over time

Abstract

Mitochondrial metabolism varies significantly between individuals of the same species and can influence animal performance, such as growth. However, growth rate is usually determined before the mitochondrial assay. The hypothesis that natural variation in mitochondrial metabolic traits is linked to differences in both previous and upcoming growth remains untested. Using biopsies to collect tissue in a non-lethal manner, we tested this hypothesis in a fish model (Dicentrarchus labrax) by monitoring individual growth rate, measuring mitochondrial metabolic traits in the red muscle, and monitoring the growth of the same individuals after the mitochondrial assay. Individual variation in growth rate was consistent before and after the mitochondrial assay; however, the mitochondrial traits that explained growth variation differed between the growth rates determined before and after the mitochondrial assay. While past growth was correlated with the activity of the cytochrome c oxidase, a measure of mitochondrial density, future growth was linked to mitochondrial proton leak respiration. This is the first report of temporal shift in the relationship between growth rate and mitochondrial metabolic traits, suggesting an among-individual variation in temporal changes in mitochondrial traits. Our results emphasize the need to evaluate whether mitochondrial metabolic traits of individuals can change over time.

Figure 1

Experimental design. Juvenile European sea bass (n = 40) were weighted about every four weeks over a 32-week period. At week 20, a biopsy of red muscle was used for mitochondrial assay. Specific growth rates (SGR) were calculated relative to the time of the biopsy. Past growth rate corresponds to SGR calculated before the biopsy, and future growth rate corresponds to SGR calculated after the biopsy.

Figure 2

Future growth rates over 4 weeks was negatively related to the mitochondrial LEAK respiration of red muscle. Future Specific Growth Rates (SGR_future) as a function of variation in Leak respiration in red muscle of juvenile European seabass (n = 40). SGR_future were calculated between body mass measured in the mitochondrial assay and posterior body masses. Continuous lines show significant effect (p < 0.05) and inclusive R² (IR²) were added to illustrate the variance explained by LEAK respiration in the variation of SGR_future. See Table S1 for statistical analyses.

Figure 3

Past growth rates were negatively related to cytochrome c oxydase activity of red muscle mitochondria. Past Specific Growth Rates (SGR_past) as a function of variation in Cytochrome C Oxidase (COX) activity in red muscle of juvenile European seabass (n = 40). SGR_past were calculated between body mass measured before the mitochondrial assay (at 20, 16, 11, and 7 weeks before) and the body mass at the mitochondrial assay. Duration of the growth trials is indicated on the top right of each panel. For 20 weeks period, plotted represent SGR_past since initial body mass has not significant effect on SGR. For 16, 11 and 7 week periods, SGR is plotted as partial residuals of SGR_past evaluated at mean initial body mass (46.6 g, 53.8 g, 60.8 g, respectively) since initial body masses had significant effect on SGR. Continuous lines show significant effect (p < 0.05) and inclusive R² (IR²) were added to illustrate the part of past SGR variation explained by COX activity. See Table S2 for statistical analyses.