Metabolic rate increases with acclimation temperature and is associated with mitochondrial function in some tissues of threespine stickleback

Cominassi, Louise; Ressel, Kirsten N.; Brooking, Allison A; Marbacher, Patrick; Ransdell-Green, Eleanor C; O’Brien, Kristin M.

doi:10.1242/jeb.244659

Cited by 6 publications

(5 citation statements)

References 73 publications

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“…Heart and intestine are not commonly explored for their association to organismal SMR, but variation in cardiac performance explains variation in MMR [69,70]. Previous studies have found evidence that mitochondrial efficiency or cytochrome C oxidase enzyme activity in muscle and liver is correlated with variation in SMR in fish [12,14,71], yet these were not supported by our measures of mitochondrial density (CS activity). By contrast, there was a positive relationship between mitochondrial density in the heart and SMR in the high food treatment.…”

Section: Discussionmentioning

confidence: 73%

Tissue-specific metabolic enzyme levels covary with whole-animal metabolic rates and life-history loci via epistatic effects

Prokkola,

Chew,

Anttila

et al. 2024

Phil. Trans. R. Soc. B

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Metabolic rates, including standard (SMR) and maximum (MMR) metabolic rate have often been linked with life-history strategies. Variation in context- and tissue-level metabolism underlying SMR and MMR may thus provide a physiological basis for life-history variation. This raises a hypothesis that tissue-specific metabolism covaries with whole-animal metabolic rates and is genetically linked to life history. In Atlantic salmon ( Salmo salar ), variation in two loci, vgll3 and six6 , affects life history via age-at-maturity as well as MMR. Here, using individuals with known SMR and MMR with different vgll3 and six6 genotype combinations, we measured proxies of mitochondrial density and anaerobic metabolism, i.e. maximal activities of the mitochondrial citrate synthase (CS) and lactate dehydrogenase (LDH) enzymes, in four tissues (heart, intestine, liver, white muscle) across low- and high-food regimes. We found enzymatic activities were related to metabolic rates, mainly SMR, in the intestine and heart. Individual loci were not associated with the enzymatic activities, but we found epistatic effects and genotype-by-environment interactions in CS activity in the heart and epistasis in LDH activity in the intestine. These effects suggest that mitochondrial density and anaerobic capacity in the heart and intestine may partly mediate variation in metabolic rates and life history via age-at-maturity. This article is part of the theme issue ‘The evolutionary significance of variation in metabolic rates’.

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Section: Discussionmentioning

confidence: 73%

Tissue-specific metabolic enzyme levels covary with whole-animal metabolic rates and life-history loci via epistatic effects

Prokkola,

Chew,

Anttila

et al. 2024

Phil. Trans. R. Soc. B

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“…Changes in mitochondria number, structure, and function represent an important part of animal development, and it has been demonstrated that adaption occurs as a result of aging [7], increased exercise [4], change in dietary composition [9], exposure to environmental stressors and temperature changes [6]. Thermal changes in the ambient environment can induce mitochondrial metabolic adaptation, and it can occur via different mechanisms that could include the adaption of mitochondrial phosphorylation respiration rate, mitochondrial complex II/I activity, or cytochrome c oxidase activity [28]. For this study we only measured mitochondrial DNA quantity and used this as a proxy for mitochondria number.…”

Section: Discussionmentioning

confidence: 99%

Using qPCR to Identify Potential Effects of Thermal Conditions during Embryogenesis on Mitochondrial DNA Copy Number in Juvenile Brown Trout Salmo trutta

Erlandsson,

Ašmonaitė,

Jonsson

et al. 2024

Fishes

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Changes in the number, structure, and function of mitochondria during the early life stages of animals can play an important role for an organism’s metabolic rate, growth, and health. Previous studies have shown that juvenile brown trout (Salmo trutta) subjected to elevated temperatures during the embryonic stage respond phenotypically with a reduced metabolic rate. The aim of this study was to explore if embryonic temperature affects the mitochondria content of young brown trout and as such explains the previously found differences in metabolic rates. Here, we optimize a quantitative PCR (qPCR) method for the mitochondria cytochrome c oxidase subunit I gene, and then use the method as a proxy for mitochondrial DNA content. We hypothesize that young trout subjected to elevated temperatures during the embryonic stage respond phenotypically with a reduced mitochondrial DNA content. To test this hypothesis, we subjected brown trout to either control ambient (4.4 ± 1.5 °C) or elevated temperatures (7.1 ± 0.6 °C) during embryogenesis. Subsequently, we extracted DNA from liver and white muscle tissue of juvenile brown trout from the two different incubation temperature treatments and successively optimized qPCR for mitochondrial DNA. We found that the amount of mitochondria DNA in liver tissue was 18 times higher than in white muscle tissue, but there was no significant difference in mitochondria content in liver or muscle tissue between brown trout exposed to elevated and ambient control temperatures during embryogenesis. We conclude that reduced metabolic rate is not likely associated with mitochondria DNA content. We also suggest that qPCR is a simple and cost-effective method to quantify mitochondria DNA in frozen and partly degraded tissue from different treatment groups and a useful proxy for identification of differences in mitochondria number.

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“…Investigating variation in mitochondrial metabolism provides an opportunity for integrating how mechanisms at the cellular level constrain whole-organism traits [6][7][8][9]. For example, individual variation in SMR and MMR were positively associated with proton leak respiration in hepatic mitochondria (i.e.…”

Section: Introductionmentioning

confidence: 99%

Non-lethal sampling for assessment of mitochondrial function does not affect metabolic rate and swimming performance

Thoral,

Dargère,

Medina-Suárez

et al. 2024

Phil. Trans. R. Soc. B

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A fundamental issue in the metabolic field is whether it is possible to understand underlying mechanisms that characterize individual variation. Whole-animal performance relies on mitochondrial function as it produces energy for cellular processes. However, our lack of longitudinal measures to evaluate how mitochondrial function can change within and among individuals and with environmental context makes it difficult to assess individual variation in mitochondrial traits. The aims of this study were to test the repeatability of muscle mitochondrial metabolism by performing two biopsies of red muscle, and to evaluate the effects of biopsies on whole-animal performance in goldfish Carassius auratus . Our results show that basal mitochondrial respiration and net phosphorylation efficiency are repeatable at 14-day intervals. We also show that swimming performance (optimal cost of transport and critical swimming speed) was repeatable in biopsied fish, whereas the repeatability of individual oxygen consumption (standard and maximal metabolic rates) seemed unstable over time. However, we noted that the means of individual and mitochondrial traits did not change over time in biopsied fish. This study shows that muscle biopsies allow the measurement of mitochondrial metabolism without sacrificing animals and that two muscle biopsies 14 days apart affect the intraspecific variation in fish performance without affecting average performance of individuals. This article is part of the theme issue ‘The evolutionary significance of variation in metabolic rates’.

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Metabolic rate increases with acclimation temperature and is associated with mitochondrial function in some tissues of threespine stickleback

Cited by 6 publications

References 73 publications

Tissue-specific metabolic enzyme levels covary with whole-animal metabolic rates and life-history loci via epistatic effects

Tissue-specific metabolic enzyme levels covary with whole-animal metabolic rates and life-history loci via epistatic effects

Using qPCR to Identify Potential Effects of Thermal Conditions during Embryogenesis on Mitochondrial DNA Copy Number in Juvenile Brown Trout Salmo trutta

Non-lethal sampling for assessment of mitochondrial function does not affect metabolic rate and swimming performance

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