Thermal plasticity of skeletal muscle mitochondrial activity and whole animal respiration in a common intertidal triplefin fish, Forsterygion lapillum (Family: Tripterygiidae)

Abstract

Oxygen demand generally increases in ectotherms as temperature rises in order to sustain oxidative phosphorylation by mitochondria. The thermal plasticity of ectotherm metabolism, such as that of fishes, dictates a species survival and is of importance to understand within an era of warming climates. Within this study the whole animal O2 consumption rate of a common New Zealand intertidal triplefin fish, Forsterygion lapillum, was investigated at different acclimation temperatures (15, 18, 21, 24 or 25 °C) as a commonly used indicator of metabolic performance. In addition, the mitochondria within permeabilised skeletal muscle fibres of fish acclimated to a moderate temperature (18 °C Cool acclimation group-CA) and a warm temperature (24 °C. Warm acclimation group-WA) were also tested at 18, 24 and 25 °C in different states of coupling and with different substrates. These two levels of analysis were carried out to test whether any peak in whole animal metabolism reflected the respiratory performance of mitochondria from skeletal muscle representing the bulk of metabolic tissue. While standard metabolic rate (SMR- an indicator of total maintenance metabolism) and maximal metabolic rate ([Formula: see text]O2 max) both generally increased with temperature, aerobic metabolic scope (AMS) was maximal at 24 °C, giving the impression that whole animal (metabolic) performance was optimised at a surprisingly high temperature. Mitochondrial oxygen flux also increased with increasing assay temperature but WA fish showed a lowered response to temperature in high flux states, such as those of oxidative phosphorylation and in chemically uncoupled states of respiration. The thermal stability of mitochondria from WA fish was also noticeably greater than CA fish at 25 °C. However, the predicted contribution of respirational flux to ATP synthesis remained the same in both groups and WA fish showed higher anaerobic activity as a result of high muscle lactate loads in both rested and exhausted states. CA fish had a comparably lower level of resting lactate and took 30 % longer to fatigue than WA fish. Despite some apparent acclimation capacity of skeletal muscle mitochondria, the ATP synthesis capacity of this species is constrained at high temperatures, and that a greater fraction of metabolism in skeletal muscle appears to be supported anaerobically at higher temperatures. The AMS peak at 24 °C does not therefore represent utilisation efficiency of oxygen but, rather, the temperature where scope for oxygen flow is greatest.

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).…”

“…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).…”

The effects of temperature on aerobic metabolism: towards a mechanistic understanding of the responses of ectotherms to a changing environment

“…4D, there is little evidence of a limitation by oxygen supply as temperature increases, nor is there a clear link between the position of the aerobic scope curve and the temperatures that maximize fitnessrelated traits such as growth (Healy and Schulte, 2012;Donelson et al, 2014;Khan et al, 2014;Norin et al, 2014;Gräns et al, 2014). Instead, growth and development have thermal optima well below the upper end of the aerobic scope T opt window in these species.…”

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

“…Intraspecific variability in LEAK and OXPHOS can be considerable and is positively related to SMR and BMR (Brown et al 2012;Salin et al 2012;Monternier et al 2014) and MMR (Coen et al 2012;Jacobs et al 2012;Schlagowski et al 2013). These investigations into the effects of these mitochondrial properties on minimum or maximum metabolic rate have generally focused on comparisons of mean values between treatment groups or life stages (Brown et al 2012;Coen et al 2012;Jacobs et al 2012;Khan et al 2014;Monternier et al 2014). However, accounting for individual heterogeneity within a population is critical for understanding properties affecting fitness, since individual variation is what natural selection acts on (Careau and Garland 2012;Vindenes and Langangen 2015).…”