Mitochondrial Function in Antarctic Nototheniids with ND6 Translocation

Mark, Felix Christopher; Lucassen, Magnus; Strobel, Anneli; Barrera-Oro, Esteban; Koschnick, Nils; Zane, Lorenzo; Patarnello, Tomaso; Pörtner, Hans‐Otto; Papetti, Chiara

doi:10.1371/journal.pone.0031860

Cited by 34 publications

(53 citation statements)

References 101 publications

(145 reference statements)

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“…Complex-specific variability among species has also been documented in two other notothenioids (Mark et al 2012), but the state III rates reported for N coriiceps in our study are significantly higher than those found by Mark and coworkers (2012). In addition, our values are in close agreement to the variation in complex-specific contributions found in triplefin blennies (Hilton et al 2010).…”

Section: Antarctic Teleostscontrasting

confidence: 66%

“…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.…”

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%

“…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%

“…Moyes and colleagues (1989) performed a variety of assays in which mitochondrial isolations from Cyprinus carpio were exposed to single substrate titrations. Since then, studies in notothenioids combining up to three substrates have been conducted (Weinstein and Somero 1998;Hardewig et al 1999b;Mark et al 2012). Recent advances in mitochondrial physiology have provided insights into the use of substrate combinations for maximally engaging electron carriers and substrate transporters for measurements of OXPHOS capacity in mammals (Gnaiger 2010a;Gnaiger 2010b).…”

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: Antarctic Teleostscontrasting

confidence: 66%

Section: Antarctic Teleostsmentioning

confidence: 96%

Section: Introductionmentioning

confidence: 92%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Mitochondrial energetics of benthic and pelagic Antarctic teleosts

2013

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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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Copper Alters the Effect of Temperature on Mitochondrial Bioenergetics in Rainbow Trout, Oncorhynchus mykiss

Sappal

MacDougald

Stevens

et al. 2013

Arch Environ Contam Toxicol

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We investigated the interaction of temperature and copper (Cu) on mitochondrial bioenergetics to gain insight into how temperature fluctuations imposed by natural phenomena or anthropogenic activities would modulate the effects of Cu on cellular energy homeostasis. Mitochondria were isolated from rainbow trout livers and, in the first set of experiments, exposed to Cu (0-2.5 mM) at 5, 11, and 25 °C with measurement of mitochondrial complex II (mtCII)-driven respiration. In the second set of experiments, unenergized mitochondria were incubated for 30 or 60 min with lower concentrations (0-160 μM) of Cu to measure the effects on mtCII enzyme activity. Whereas maximal (state 3) respiration was inhibited by high Cu exposure, low Cu doses stimulated and high Cu doses inhibited resting (state 4) and 4ol (proton leak) respirations. High temperature alone increased mitochondrial respiration in all states. The Q10 values for state 3, state 4, and proton leak respirations suggested active processes with state 4 respiration and proton leak exhibiting greater thermal sensitivity than state 3 respiration. The differential thermal sensitivity of resting relative to phosphorylating mitochondrial state led to uncoupling and limitation of mitochondrial oxidative capacity at both high temperature and doses of Cu. Moreover, exposure to high Cu caused loss of thermal dependence of the mitochondrial bioenergetics culminating in Q10 values well below unity and decreased activation energies (E a) for both maximal and resting respiration rates. In addition, mtCII activity was increased by low and decreased by high doses of Cu indicating that direct effects on this enzyme contribute to Cu-induced mitochondrial dysfunction. Taken together, it appears that the substrate oxidation (electron transport chain and tricarboxylic acid cycle) and proton leak subsystems are targets of the deleterious effects of Cu and increased temperature on mitochondrial bioenergetics. However, mitochondrial effects of Cu and temperature may not be easily distinguished because they are generally qualitatively similar.

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Mitochondrial Function in Antarctic Nototheniids with ND6 Translocation

Cited by 34 publications

References 101 publications

Mitochondrial energetics of benthic and pelagic Antarctic teleosts

Mitochondrial energetics of benthic and pelagic Antarctic teleosts

Mitochondrial Bioenergetics

Copper Alters the Effect of Temperature on Mitochondrial Bioenergetics in Rainbow Trout, Oncorhynchus mykiss

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