Mechanisms and costs of mitochondrial thermal acclimation in a eurythermal killifish (Fundulus heteroclitus)

Abstract

Processes acting at the level of the mitochondria have been suggested to affect the thermal limits of organisms. To determine whether changes in mitochondrial properties could underlie shifts in thermal limits, we examined how mitochondrial properties are affected by thermal acclimation in the eurythermal killifish, Fundulus heteroclitus -a species with substantial plasticity in whole-organism thermal limits. We hypothesized that thermal acclimation would result in functional changes in the mitochondria that could result in trade-offs in function during acute thermal shifts. We measured the mitochondrial respiration rate (V O2 ) through multiple complexes of the electron transport system following thermal acclimation (to 5, 15, 33°C) and assessed maintenance of mitochondrial membrane potential (Δp) and rates of reactive oxygen species (ROS) production as an estimate of costs. Acclimation to 5°C resulted in a modest compensation of mitochondrial respiration at low temperatures, but these mitochondria were able to maintain Δp with acute exposure to high temperatures, and ROS production did not differ between acclimation groups, suggesting that these increases in mitochondrial capacity do not alter mitochondrial thermal sensitivity. Acclimation to 33°C suppressed mitochondrial respiration as a result of effects on NADH dehydrogenase (complex I). These high-temperature acclimated fish nonetheless maintained levels of Δp and ROS production similar to those of the other acclimation groups. This work demonstrates that killifish mitochondria can successfully acclimate to a wide range of temperatures without incurring major functional trade-offs during acute thermal shifts and that high-temperature acclimation results in a suppression of metabolism, consistent with patterns observed at the organismal level.

Thermal acclimation and subspecies-specific effects on heart and brain mitochondrial performance in a eurythermal teleost (Fundulus heteroclitus)

“…Our observed decline in heart and brain mitochondrial capacity supports the prediction of decreased mitochondrial capacity at high temperatures (Figs 2-7). Similar declines in mitochondrial function have been observed previously in heart and liver mitochondria in F. heteroclitus (Baris et al, 2016a;Chung and Schulte, 2015) and in other ectotherms (Khan et al, 2014;Guderley and Johnston, 1996;Strobel et al, 2013). Acclimation to 33°C results in a decline in routine oxygen consumption in F. heteroclitus, suggesting that this temperature causes a collapse of aerobic metabolism or that active metabolic suppression is taking place (Healy and Schulte, 2012).…”

“…Declines in whole-animal and tissue mass (Fig. 1) following 33°C acclimation may be indicative of an energetic mismatch induced by insufficient food supply and high energetic demands (Chung and Schulte, 2015). These data provide support for a mismatch of organism-level energetic supply and demand with increasing temperature and potential sub-lethal costs associated with high-temperature acclimation; this may account for our observed mitochondrial suppression with potential consequences for the fitness of these animals (Salin et al, 2016;Lemoine and Burkepile, 2012;Iles, 2014).…”

“…Low-temperature acclimation is associated with increased mitochondrial oxidative phosphorylation (OXPHOS) capacity, mitochondrial volume density and alterations in mitochondrial membrane composition (Chung and Schulte, 2015;Egginton and Johnston, 1984;Grim et al, 2010;Fangue et al, 2009;Kraffe et al, 2007;Dhillon and Schulte, 2011;Schnell and Seebacher, 2008). In contrast, hightemperature acclimation has been associated with changes in mitochondrial membrane fatty acid saturation and lowered mitochondrial respiratory capacity (Chung and Schulte, 2015;Guderley and Johnston, 1996;Khan et al, 2014;Strobel et al, 2013;Baris et al, 2016a;Fangue et al, 2009). These changes may induce trade-offs causing mitochondrial function to decline at temperatures that were not previously harmful, which may account for shifts in whole-animal thermal tolerance following acclimation (Fangue et al, 2009;Chung and Schulte, 2015).…”

“…In contrast, hightemperature acclimation has been associated with changes in mitochondrial membrane fatty acid saturation and lowered mitochondrial respiratory capacity (Chung and Schulte, 2015;Guderley and Johnston, 1996;Khan et al, 2014;Strobel et al, 2013;Baris et al, 2016a;Fangue et al, 2009). These changes may induce trade-offs causing mitochondrial function to decline at temperatures that were not previously harmful, which may account for shifts in whole-animal thermal tolerance following acclimation (Fangue et al, 2009;Chung and Schulte, 2015).…”

“…In these estuarine habitats they experience large diel and seasonal fluctuations in T a . Their ability to survive [critical thermal (CT) limits=−1 to 41°C] and acclimate (acclimation limits=2 to 35°C) over a large thermal range may be due to a thermally robust mitochondrial physiology (Fangue et al, 2009;Chung and Schulte, 2015) and acclimation capacity (Chung and Schulte, 2015;Fangue et al, 2009;Baris et al, 2016a). In addition, northern and southern subspecies of F. heteroclitus have undergone local adaptation to their thermal environments and have diverged for a number of traits such as whole-animal metabolic rates and thermal tolerance (Schulte, 2001;Fangue et al, 2006Fangue et al, , 2009.…”