Loss of mitochondrial performance at high temperatures is correlated with upper thermal tolerance among populations of an intertidal copepod

Healy, Timothy M.; Burton, Ronald S.

doi:10.1016/j.cbpb.2023.110836

Comparative Biochemistry and Physiology Part B: Biochemistry an

2023

DOI: 10.1016/j.cbpb.2023.110836

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Loss of mitochondrial performance at high temperatures is correlated with upper thermal tolerance among populations of an intertidal copepod

Timothy M. Healy

Ronald S. Burton

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Cited by 4 publications

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“…Hence, it has been suggested that mitochondrial thermal sensitivity plays a key role in organismal adaptations to temperature and is involved in setting thermal tolerance of ectotherms [7–12]. Furthermore, it has been shown in several ectotherms that mitochondrial dysfunctions may explain organismal failure at critically high temperatures [10,13–17]. However, the specific mitochondrial process(es) leading to this failure is still unclear.…”

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Succinate oxidation rescues mitochondrial ATP synthesis at high temperature in Drosophila melanogaster

et al. 2023

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Decreased NADH‐induced and increased reduced FADH2‐induced respiration rates at high temperatures are associated with thermal tolerance in Drosophila. Here, we determined whether this change was associated with adjustments of adenosine triphosphate (ATP) production rate and coupling efficiency (ATP/O) in Drosophila melanogaster. We show that decreased pyruvate + malate oxidation at 35°C is associated with a collapse of ATP synthesis and a drop in ATP/O ratio. However, adding succinate triggered a full compensation of both oxygen consumption and ATP synthesis rates at this high temperature. Addition of glycerol‐3‐phosphate (G3P) led to a huge increase in respiration with no further advantage in terms of ATP production. We conclude that succinate is the only alternative substrate able to compensate both oxygen consumption and ATP production rates during oxidative phosphorylation at high temperature, which has important implications for thermal adaptation.

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Succinate oxidation rescues mitochondrial ATP synthesis at high temperature in Drosophila melanogaster

et al. 2023

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Northern copepod mitochondria can't beat the heat

Borowiec

2023

Journal of Experimental Biology

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Disproportionate role of nuclear-encoded proteins in organismal and mitochondrial thermal performance in a copepod

Kayhani,

Barreto

2023

Journal of Experimental Biology

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Determining the mechanisms by which organisms evolve thermal tolerance is crucial to predicting how populations may respond to changes in local temperature regimes. While evidence of relationships between mitochondrial background and thermal adaptation have been found, the presence of both nuclear-encoded and mitochondrial DNA (mtDNA)-encoded proteins warrants experiments aimed at parsing out the relative role of each genome in thermal adaptation. We investigate the relative role of mtDNA-encoded products in thermal tolerance between two divergent populations of Tigriopus californicus using first generation (F1) hybrids that vary in maternally inherited mtDNA but are heterozygous for population-specific alleles across nuclear loci. We tested two measures of thermal tolerance: (1) survivorship to acute thermal stress and (2) thermal stability of mitochondrial performance in Complex I-fueled ATP synthesis, both across a range of increasing temperatures. We found that the southern population (San Diego, California) outperformed the northern population (Strawberry Hill, Oregon) in survivorship, and that both reciprocal F1 hybrid crosses had intermediate survival. Mitochondria from the San Diego population displayed greater stability in ATP synthesis with increasing temperatures compared to those from Strawberry Hill. Interestingly, hybrids from both cross directions had synthesis profiles that were very similar to that of Strawberry Hill. Taken together, these results suggest that the relative role of the mtDNA in these phenotypes is negligible compared to that of elements encoded by nuclear DNA in this system.

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Loss of mitochondrial performance at high temperatures is correlated with upper thermal tolerance among populations of an intertidal copepod

Cited by 4 publications

References 39 publications

Succinate oxidation rescues mitochondrial ATP synthesis at high temperature in Drosophila melanogaster

Succinate oxidation rescues mitochondrial ATP synthesis at high temperature in Drosophila melanogaster

Northern copepod mitochondria can't beat the heat

Disproportionate role of nuclear-encoded proteins in organismal and mitochondrial thermal performance in a copepod

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