Thermal sensitivity of mitochondrial function in the Antarctic Notothenioid Lepidonotothen nudifrons

Hardewig, I.; Pörtner, Hans-O.; Peck, Lloyd S.

doi:10.1007/s003600050260

Cited by 76 publications

(90 citation statements)

References 37 publications

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“…The oxidation system was highly coupled with the phosphorylation system in Pleuragramma antarcticum at temperatures of 5°C and 10°C, where RCR values reached 12.35 ± 0.79 (n = 10, ± SE) and 12.66 ± 1.26 (n = 8, ± SE), respectively (Figure 1). These values are among the highest reported for notothenioid liver mitochondria (Hardewig et al 1999a). No significant differences were found among RCR values obtained between 5°C and 15°C (one-way ANOVA, P > 0.05).…”

Section: Thermal Tolerance In Mitochondria Of Pleuragramma Antarcticummentioning

confidence: 47%

“…When extrapolated to 0°C, N. coriiceps liver mitochondria exhibited lower state III rates than observed in red muscle tissue of N. coriiceps and livers mitochondria of other notothenioids (Johnston et al 1994;Johnston et al 1998;Mark et al 2012). However, state III rates of the conspecifics L. squamifrons and L. nudifrons (Hardewig et al 1999a) were found to be significantly different. These differences were expected due to differences in the titration protocol: values for L. nudifrons corresponded to state III rates in the presence of only succinate, ADP and the complex I inhibitor rotenone.…”

Section: Antarctic Teleostsmentioning

confidence: 96%

“…Weinstein and Somero (1998) found an Arrhenius breakpoint in the state III respiration rate at 20.3°C for Trematomus bernacchii liver mitochondria, several degrees higher than its upper lethal temperature of around 5°C (Somero and DeVries 1967). Similar Arrhenius plots have been employed to describe the thermal sensitivity of OXPHOS in notothenioids, where breakpoints in state III respiration have been observed at various temperatures between 9°C and 31.5°C (Hardewig et al 1999a;Urschel and O'Brien 2008;Mark et al 2012). …”

Section: Introductionmentioning

confidence: 92%

“…In previous studies, the use of individual substrates to understand substrate preferences resulted in the use of pyruvate as the major substrate in similar assays (Moyes et al 1989;Moyes et al 1992;Johnston et al 1994). More recent studies utilized titrations including PM to activate complex I, PMS to activate both complexes I and II and others have used rotenone as a complex I inhibitor in the presence of S to activate solely complex II (Weinstein and Somero 1998;Hardewig et al 1999a;Lannig et al 2005). The addition of glutamate and the overall combination of PMGS in a single run has been utilized in snappers recently (Cook et al 2013), and our study constitutes the first attempt in notothenioids.…”

Section: Antarctic Teleostsmentioning

confidence: 99%

“…More recently, various studies described the thermal-tolerance window of the mitochondrial oxidative phosphorylation (OXPHOS) system in Antarctic teleosts. Those studies provide valuable information of the thermal tolerance of the moderately active, benthic species Trematomus bernacchii (Weinstein and Somero 1998), Lepidonotothen nudifrons (Hardewig et al 1999a), and the less active Notothenia coriiceps (Johnston et al 1994;Mark et al 2012) and Notothenia rossii (Mark et al 2012). In addition, the thermal sensitivity of ADP-stimulated (state III) respiration based on Arrhenius breakpoints in temperature (ABT) of the red blooded notothenioid Gobionotothen gibberifrons and the hemoglobinless Chaenocephalus aceratus have shown similar levels of thermal plasticity in notothenioid mitochondria (Urschel and O'Brien 2009).…”

Section: Introductionmentioning

confidence: 99%

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Mitochondrial energetics of benthic and pelagic Antarctic teleosts

2013

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Antarctic fauna are highly adapted to the frigid waters of the Southern Ocean. This study describes the in vitro temperature sensitivity of oxygen consumption rates measured in liver mitochondria from the pelagic nototheniid Pleuragramma antarcticum between 5°C and 35°C. Oxygen fluxes were measured after the addition of milimolar levels of pyruvate, malate, succinate and glutamate (State II, LEAK) and saturating levels of ADP (State III, OXPHOS). State III respiration significantly decreased above 18.7°C. A comparison of the oxidative capacities among P. antarcticum and other notothenioids showed significant differences in state III respiration, where benthic species exhibited about 50% lower rates than P. antarcticum. In addition, state III respiration rates normalized per milligram of mitochondrial protein of P. antarcticum were up to eight times higher than state III rates reported in the literature for other notothenioids. The comparatively high respiration rates measured in this study may be explained by our approach, which engaged both complex I and II under conditions of oxidative phosphorylation. State III rates of independently activated complexes I and II were found to range from 42 to 100% of rates obtained when both complexes were activated simultaneously in the same species. The remarkable tolerance of P.antarcticum OXPHOS toward warmer temperatures was unexpected for an Antarctic stenotherm, and may indicate that thermal sensitivity of their mitochondria is not the driving force behind their stenothermy.3

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Section: Thermal Tolerance In Mitochondria Of Pleuragramma Antarcticummentioning

confidence: 47%

Section: Antarctic Teleostsmentioning

confidence: 96%

Section: Introductionmentioning

confidence: 92%

Section: Antarctic Teleostsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Mitochondrial energetics of benthic and pelagic Antarctic teleosts

2013

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Mechanisms Defining Thermal Limits and Adaptation in Marine Ectotherms: An Integrative View

Pörtner¹,

Peck²,

Somero³

2012

Antarctic Ecosystems

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Mitochondrial Bioenergetics

2012

Methods in Molecular Biology

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Animals must expend energy to deal with a wide array of stressors associated with environmental change. Because mitochondria produce >90% of the energy requirement of the cell, they are likely the fundamental drivers of responses to environmental change. The primary goal of my thesis was to explore the interactions of three common stressors in aquatic systemstemperature, metals (copper: Cu) and hypoxia-on mitochondrial bioenergetics. To achieve this, I first performed a series of in vitro experiments using rainbow trout, Oncorhynchus mykiss liver mitochondria energized with complex I and II substrates to characterize the acute interactive responses of temperature and Cu on mitochondrial function. These studies revealed that Cu altered the basal and maximal mitochondrial oxidation rates differently depending on the metal dose and temperature. Mechanistically, I showed that Cu impairs oxidative phosphorylation in part by inhibiting the electron transport system (ETS) enzymes, stimulating proton leak, inducing mitochondrial permeability transition pore and dissipating inner membrane potential. Importantly, temperature exacerbated the effects of Cu suggesting that environmental warming, e.g., due to climate change, may sensitize fish to Cu toxicity. The next study combined in vitro and in vivo approaches to shed light on how persistent elevated temperature (warm acclimation) modulates the effects of acute temperature increase, hypoxiareoxygenation (HRO) and/or Cu on mitochondrial function. Sequential inhibition and activation of mitochondrial ETS enzyme complexes permitted the measurement of respiratory activities supported by ETS complexes I-IV in one run and allowed me to identify segments/components of the ETS that are resilient or susceptible to single and combined effects of temperature, Cu and HRO. This study also revealed that warm acclimation blunted the sensitivity of the ETS to acute temperature rise and, together with HRO, sensitized the ETS to Cu. v My fourth study examined how warm acclimation influences the ability of fish to handle individual and joint effects of subsequent acute temperature shifts, hypoxia and Cu stress by exposing fish in vivo to the three stressors. Here I measured mitochondrial oxidation and apical endpoints indicative of stress and organismal energy status to assess the relevance of energy metabolism endpoints in vivo. I showed that warm acclimation reduced fish condition, promoted anaerobic metabolism, decelerated the ETS and altered the responses of fish to acute temperature shifts, hypoxia and Cu. Moreover, Cu and hypoxia showed reciprocal antagonistic interaction on the ETS and plasma metabolites, with modest additive actions limited to proton leak. The final study highlighted the functional-biochemical and transcriptional responses of fish to warm acclimation and short-term exposures to Cu and hypoxia. In this in vivo study, activities of ETS enzyme complexes and targeted analyses of transcripts encoding for proteins involved in mitochondrial oxidation, metals detoxification/...

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Thermal sensitivity of mitochondrial function in the Antarctic Notothenioid Lepidonotothen nudifrons

Cited by 76 publications

References 37 publications

Mitochondrial energetics of benthic and pelagic Antarctic teleosts

Mitochondrial energetics of benthic and pelagic Antarctic teleosts

Mechanisms Defining Thermal Limits and Adaptation in Marine Ectotherms: An Integrative View

Mitochondrial Bioenergetics

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