Mitochondrial Acclimation Capacities to Ocean Warming and Acidification Are Limited in the Antarctic Nototheniid Fish, Notothenia rossii and Lepidonotothen squamifrons

Mitochondrial performance may play a role in setting whole-animal thermal tolerance limits and their plasticity, but the relative roles of adjustments in mitochondrial performance across different highly aerobic tissues remain poorly understood. We compared heart and brain mitochondrial responses to acute thermal challenges and to thermal acclimation using high-resolution respirometry in two locally adapted subspecies of Atlantic killifish (Fundulus heteroclitus). We predicted that 5°C acclimation would result in compensatory increases in mitochondrial performance, while 33°C acclimation would cause suppression of mitochondrial function to minimize the effects of high temperature on mitochondrial metabolism. In contrast, acclimation to both 33 and 5°C decreased mitochondrial performance compared with fish acclimated to 15°C. These adjustments could represent an energetic cost-saving mechanism at temperature extremes. Acclimation responses were similar in both heart and brain; however, this effect was smaller in the heart, which might indicate its importance in maintaining whole-animal thermal performance. Alternatively, larger acclimation effects in the brain might indicate greater thermal sensitivity compared with the heart. We detected only modest differences between subspecies that were dependent on the tissue assayed. These data demonstrate extensive plasticity in mitochondrial performance following thermal acclimation in killifish, and indicate that the extent of these responses differs between tissues, highlighting the importance and complexity of mitochondrial regulation in thermal acclimation in eurytherms.

Section: Does Acclimation To 33°c Results In a Suppression Of Mitochonsupporting

confidence: 79%

Section: Introductionmentioning

confidence: 99%

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

Chung

Bryant

Schulte

2017

“…Thus, suppression of metabolism with acclimation to high temperature could be interpreted as a benefit of acclimation. Although there are relatively few studies examining this phenomenon, some groups have demonstrated that high-temperature acclimation results in a decrease in mitochondrial membrane fatty acid saturation and a decrease in respiration rate (Guderley and Johnston, 1996;Khan et al, 2014;Strobel et al, 2013).…”

Section: Introductionmentioning

confidence: 99%

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

Chung

Schulte

2015

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.

“…Despite projections that indicate changes in SST and partial pressure of CO 2 (Ṗ CO2 ) in seawater will impact higher latitudes faster and to a greater Is warmer better? Decreased oxidative damage in notothenioid fish after long-term acclimation to multiple stressors Laura A. Enzor and Sean P. Place* extent than temperate regions (Walther et al, 2002;Orr et al, 2005;Turner et al, 2005;McNeil and Matear, 2008;Fabry et al, 2008;Fabry et al, 2009;Halpern et al, 2008;McNeil et al, 2010;Mathis et al, 2011a;Mathis et al, 2011b), only a handful of studies have examined the effects of ecologically relevant increases in seawater Ṗ CO 2 on high latitude marine teleosts (Hurst et al, 2012;Strobel et al, 2012;Enzor et al, 2013;Strobel et al, 2013a;Strobel et al, 2013b). Similar to impacts seen with elevated temperature, ocean acidification may also perturb oxidative stress in marine teleosts (Murphy, 2009;Tomanek et al, 2011) and may even exacerbate the detrimental effects of reactive oxygen species at the cellular level (Ezraty et al, 2011).…”

Section: Introductionmentioning

confidence: 99%

“…Currently, the potential synergistic effects of increased temperature and increased Ṗ CO 2 in fish have only been examined in a small number of studies (Pankhurst and Munday, 2011;Nowicki et al, 2012;Strobel et al, 2012;Enzor et al, 2013;Strobel et al, 2013a;Strobel et al, 2013b;Gräns et al, 2014). We have previously shown that increased temperature and Ṗ CO 2 levels result in a rapid increase in resting metabolic rates in several species of Antarctic fish (Enzor et al, 2013).…”

Section: Introductionmentioning

confidence: 99%

Is warmer better? Decreased oxidative damage in notothenioid fish after long-term acclimation to multiple stressors

Enzor

Place

2014

Antarctic fish of the suborder Notothenioidei have evolved several unique adaptations to deal with subzero temperatures. However, these adaptations may come with physiological trade-offs, such as an increased susceptibility to oxidative damage. As such, the expected environmental perturbations brought on by global climate change have the potential to significantly increase the level of oxidative stress and cellular damage in these endemic fish. Previous single stressor studies of the notothenioids have shown they possess the capacity to acclimate to increased temperatures, but the cellularlevel effects remain largely unknown. Additionally, there is little information on the ability of Antarctic fish to respond to ecologically relevant environmental changes where multiple variables change concomitantly. We have examined the potential synergistic effects that increased temperature and Ṗ CO2 have on the level of protein damage in Trematomus bernacchii, Pagothenia borchgrevinki and Trematomus newnesi, and combined these measurements with changes in total enzymatic activity of catalase (CAT) and superoxide dismutase (SOD) in order to gauge tissue-specific changes in antioxidant capacity. Our findings indicate that total SOD and CAT activity levels displayed only small changes across treatments and tissues. Short-term acclimation to decreased seawater pH and increased temperature resulted in significant increases in oxidative damage. Surprisingly, despite no significant change in antioxidant capacity, cellular damage returned to near-basal levels, and significantly decreased in T. bernacchii, after long-term acclimation. Overall, these data suggest that notothenioid fish currently maintain the antioxidant capacity necessary to offset predicted future ocean conditions, but it remains unclear whether this capacity comes with physiological trade-offs.