Temperature-related differences in mitochondrial function among clones of the cladoceran Daphnia pulex

Kake-Guena, Sandrine A.; Touisse, Kamal; Warren, Blair E.; Scott, Katrina Y.; Dufresne, France; Blier, Pierre; Lemieux, Hélène

doi:10.1016/j.jtherbio.2017.05.005

Cited by 12 publications

(6 citation statements)

References 60 publications

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“…This seems to reflect a greater maintenance of CIV function when compared with other complexes. Similar results have already been observed in other aquatic ectotherms (Blier and Lemieux, 2001;Oellermann et al, 2012;Blier et al, 2013;Kake-Guena et al, 2017). Otherwise, in both species, O 2 flux of the leak state was mirrored almost exactly by CI.…”

Section: Discussion Metabolic Depression At Elevated Temperaturessupporting

confidence: 89%

“…Cytochrome c (10 µmol l −1 ) was added to calculate the flux control factor for cytochrome c (FCFc) to determine mitochondrial membrane integrity (an increase in rate following cytochrome c addition is indicative of outer mitochondrial membrane damage) (Gnaiger, 2014). Specifically, values close to 0 represent an undamaged mitochondrial membrane, while values nearing 1 represent a fully damaged mitochondrial membrane (Kake-Guena et al, 2017). Then, succinate (10 mmol l −1 ) was added to stimulate succinate dehydrogenase (complex II, or CII) activity.…”

Section: Mitochondrial Respirationmentioning

confidence: 99%

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Mitochondrial thermo-sensitivity in invasive and native freshwater mussels

Hraoui

Bettinazzi

Gendron

et al. 2020

Journal of Experimental Biology

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Climate change is impacting many, if not all, forms of life. Increases in extreme temperature fluctuations and average temperatures can cause stress, particularly in aquatic sessile ectotherms such as freshwater mussels. However, some species seem to thrive more than others in face of temperature-related stressors. Thermal tolerance may for example explain invasive species success. It is also known that mitochondria can play a key role in setting an ectothermic species’ thermal tolerance. In this study, we aimed to characterize the mitochondrial thermo-tolerance in invasive and endemic freshwater mussels. With the use of high-resolution respirometry, we analyzed the mitochondrial respiration of two freshwater bivalve species exposed to a broad range of temperatures. We noticed that the invasive dreissenid Dreissena bugensis possessed a less thermo-tolerant mitochondrial metabolism than the endemic unionid Elliptio complanata. This lack of tolerance was linked with a more noticeable aerobic metabolic depression at elevated temperatures. This decrease in mitochondrial metabolic activity was also linked with an increase in leak oxygen consumption as well as a stable maintenance of the activity of cytochrome c oxidase in both species. These findings may be associated both with species’ life history characteristics, as D. bugensis is more adapted to unstable habitats, in which selection pressures for resistance adaptations are reduced. Our findings add to the growing body of literature characterizing the mitochondrial metabolism of many aquatic ectotherms in our changing world.

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Section: Discussion Metabolic Depression At Elevated Temperaturessupporting

confidence: 89%

Section: Mitochondrial Respirationmentioning

confidence: 99%

Mitochondrial thermo-sensitivity in invasive and native freshwater mussels

Hraoui

Bettinazzi

Gendron

et al. 2020

Journal of Experimental Biology

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“…B 374: 20180180 plasticity may be important for adaptation to a seasonally more variable environment, and possibly to a climatically more variable future as well (keeping in mind that plasticity in killifish has been shown to differ in response to the cold but not the warm [45]). Plasticity of mitochondrial respiration in response to temperature also differs between clones of Daphnia pulex from temperate and subarctic environments, but without showing a clear latitudinal pattern, although clonal differences in mitochondrial function are again more pronounced when assayed in cold conditions [46]. Among individuals, differential flexibility in metabolic rate among fish is linked to their growth rates: brown trout (Salmo trutta) that either increase or decrease their SMR the most in response to increased or decreased food availability, respectively, grow the fastest relative to their less flexible conspecifics [35].…”

Section: Evidence For Plasticity In Metabolic Ratesmentioning

confidence: 97%

Ecological and evolutionary consequences of metabolic rate plasticity in response to environmental change

Norin

Metcalfe

2019

Phil. Trans. R. Soc. B

174

172

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One contribution of 13 to a theme issue 'The role of plasticity in phenotypic adaptation to rapid environmental change'.Basal or standard metabolic rate reflects the minimum amount of energy required to maintain body processes, while the maximum metabolic rate sets the ceiling for aerobic work. There is typically up to three-fold intraspecific variation in both minimal and maximal rates of metabolism, even after controlling for size, sex and age; these differences are consistent over time within a given context, but both minimal and maximal metabolic rates are plastic and can vary in response to changing environments. Here we explore the causes of intraspecific and phenotypic variation at the organ, tissue and mitochondrial levels. We highlight the growing evidence that individuals differ predictably in the flexibility of their metabolic rates and in the extent to which they can suppress minimal metabolism when food is limiting but increase the capacity for aerobic metabolism when a high work rate is beneficial. It is unclear why this intraspecific variation in metabolic flexibility persists-possibly because of trade-offs with the flexibility of other traits-but it has consequences for the ability of populations to respond to a changing world. It is clear that metabolic rates are targets of selection, but more research is needed on the fitness consequences of rates of metabolism and their plasticity at different life stages, especially in natural conditions. This article is part of the theme issue 'The role of plasticity in phenotypic adaptation to rapid environmental change'.

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“…Metabolic demand increases with temperature and to maintain cellular homeostasis the rate of mitochondrial aerobic respiration must keep pace (Blier et al, 2014;Schulte, 2015). Accordingly, thermal sensitivity of mitochondria has been suggested to be important for thermal tolerance and thermal adaptations of mitochondrial functions have been observed in several ectothermic phyla (Chung et al, 2018;Ekström et al, 2017;Fangue et al, 2009;Harada et al, 2019;Havird et al, 2020;Hraoui et al, 2020;Hunter-Manseau et al, 2019;Iftikar et al, 2010;Iftikar et al, 2014;Kake-Guena et al, 2017;Martinez et al, 2016, see also Chung and Schulte, 2020). Most mitochondrial studies addressing the effects of high temperature in ectotherms have focused on aquatic invertebrates or fish, while only a few studies have used insects, even though they comprise > 70% of all animal species (Stork, 2018) and have the most rapidly contracting muscles in nature (Beenakkers et al, 1984;Candy et al, 1997) (but see Chamberlin (2004), Pichaud et al (2010;2011; and references below for studies on insect mitochondrial function).…”

Section: Introductionmentioning

confidence: 99%

Dramatic changes in mitochondrial substrate use at critically high temperatures: a comparative study usingDrosophila

Jørgensen

Overgaard

Hunter-Manseau

et al. 2021

Journal of Experimental Biology

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Ectotherm thermal tolerance is critical to species distribution, but at present the physiological underpinnings of heat tolerance remain poorly understood. Mitochondrial function is perturbed at critically high temperatures in some ectotherms, including insects, suggesting that heat tolerance of these animals is linked to failure of oxidative phosphorylation (OXPHOS) and/or ATP production. To test this hypothesis we measured mitochondrial oxygen consumption rates in six Drosophila species with different heat tolerance using high-resolution respirometry. Using a substrate-uncoupler-inhibitor titration protocol we examined specific steps of the electron transport system to study how temperatures below, bracketing and above organismal heat limits affected mitochondrial function and substrate oxidation. At benign temperatures (19 and 30°C), complex I-supported respiration (CI-OXPHOS) was the most significant contributor to maximal OXPHOS. At higher temperatures (34, 38, 42 and 46°C), CI-OXPHOS decreased considerably, ultimately to very low levels at 42 and 46°C. The enzymatic catalytic capacity of complex I was intact across all temperatures and accordingly the decreased CI-OXPHOS is unlikely to be caused directly by hyperthermic denaturation/inactivation of complex I. Despite the reduction in CI-OXPHOS, maximal OXPHOS capacities were maintained in all species, through oxidation of alternative substrates; proline, succinate and, particularly, glycerol-3-phosphate, suggesting important mitochondrial flexibility at temperatures exceeding the organismal heat limit. Interestingly, this failure of CI-OXPHOS and compensatory oxidation of alternative substrates occurred at temperatures that tended to correlate with species heat tolerance, such that heat-tolerant species could defend “normal” mitochondrial function at higher temperatures than sensitive species. Future studies should investigate why CI-OXPHOS is perturbed and how this potentially affects ATP production rates.

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Temperature-related differences in mitochondrial function among clones of the cladoceran Daphnia pulex

Cited by 12 publications

References 60 publications

Mitochondrial thermo-sensitivity in invasive and native freshwater mussels

Mitochondrial thermo-sensitivity in invasive and native freshwater mussels

Ecological and evolutionary consequences of metabolic rate plasticity in response to environmental change

Dramatic changes in mitochondrial substrate use at critically high temperatures: a comparative study usingDrosophila

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