Metabolic shifts in the Antarctic fish Notothenia rossii in response to rising temperature and PCO2

Abstract

IntroductionOngoing ocean warming and acidification increasingly affect marine ecosystems, in particular around the Antarctic Peninsula. Yet little is known about the capability of Antarctic notothenioid fish to cope with rising temperature in acidifying seawater. While the whole animal level is expected to be more sensitive towards hypercapnia and temperature, the basis of thermal tolerance is set at the cellular level, with a putative key role for mitochondria. This study therefore investigates the physiological responses of the Antarctic Notothenia rossii after long-term acclimation to increased temperatures (7°C) and elevated PCO2 (0.2 kPa CO2) at different levels of physiological organisation.ResultsFor an integrated picture, we analysed the acclimation capacities of N. rossii by measuring routine metabolic rate (RMR), mitochondrial capacities (state III respiration) as well as intra- and extracellular acid–base status during acute thermal challenges and after long-term acclimation to changing temperature and hypercapnia. RMR was partially compensated during warm- acclimation (decreased below the rate observed after acute warming), while elevated PCO2 had no effect on cold or warm acclimated RMR. Mitochondrial state III respiration was unaffected by temperature acclimation but depressed in cold and warm hypercapnia-acclimated fish. In both cold- and warm-exposed N. rossii, hypercapnia acclimation resulted in a shift of extracellular pH (pHe) towards more alkaline values. A similar overcompensation was visible in muscle intracellular pH (pHi). pHi in liver displayed a slight acidosis after warm normo- or hypercapnia acclimation, nevertheless, long-term exposure to higher PCO2 was compensated for by intracellular bicarbonate accumulation.ConclusionThe partial warm compensation in whole animal metabolic rate indicates beginning limitations in tissue oxygen supply after warm-acclimation of N. rossii. Compensatory mechanisms of the reduced mitochondrial capacities under chronic hypercapnia may include a new metabolic equilibrium to meet the elevated energy demand for acid–base regulation. New set points of acid–base regulation under hypercapnia, visible at the systemic and intracellular level, indicate that N. rossii can at least in part acclimate to ocean warming and acidification. It remains open whether the reduced capacities of mitochondrial energy metabolism are adaptive or would impair population fitness over longer timescales under chronically elevated temperature and PCO2.

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

“…Although temperature increases have long been known to impact oxidative stress in organisms (Lesser, 2006), ocean acidification has recently emerged as a potentially more pressing issue in the world's oceans, and to date, we still have a poor understanding of the cellular-level impact that ecologically relevant increases in seawater Ṗ CO 2 will have on cellular homeostasis. Increases in Ṗ CO2 are specifically hypothesized to exacerbate oxidative stress by directly affecting mitochondrial function (Murphy, 2009;Tomanek et al, 2011), and recent studies have indeed shown that hypercapnia can negatively affect mitochondrial capacities in Antarctic fish (Strobel et al, 2012;Strobel et al, 2013b). We found that oxidative damage was most apparent within the first 7 days of acclimation to the treatment conditions, which coincides with a spike in the resting metabolic rate (RMR) of all three species under these same acclimation conditions (Enzor et al, 2013).…”

“…The initial spike in oxidative damage observed in this study along with the increased metabolic rates previously observed within the first week of acclimation (Robinson and Davison, 2008a;Robinson and Davison, 2008b;Strobel et al, 2012;Enzor et al, 2013) may signal a surge in protein synthesis and turnover as the cellular environment is restructured. The slow decline of metabolic rates seen in previous studies, connected with the precipitous drop-off in damaged proteins seen in this study, may in turn signal that the initial energy expenditure has led to a more stable cellular environment.…”

“…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).…”

“…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).…”

Acclimation and thermal tolerance in Antarctic marine ectotherms

“…Robinson and Davison (Robinson and Davison, 2008) showed that oxygen consumption (Ṁ O 2 ) acclimated to 4°C in P. borchgrevinki after 1 month such that resting Ṁ O 2 was the same as that at −1°C and recovery from exhaustive exercise was the same in warm-or cold-acclimated fish. More recently, metabolic rate stabilisation, mitochondrial function and acid-base regulation have all been used to measure acclimation state in the fish Notothenia rosii, where partial acclimation of metabolic rate was observed after 29-36 days at 7°C (Strobel et al, 2012). At the whole-animal level, Bilyk and DeVries (Bilyk and DeVries, 2011) used the change in CT max to demonstrate that a range of fish from both the high Antarctic at McMurdo Sound and the maritime Antarctic on the Antarctic Peninsula were capable of acclimating to 4°C (Fig.…”