Cardiovascular oxygen transport and peripheral oxygen extraction capacity contribute to acute heat tolerance in European seabass

Anttila, Katja; Mauduit, Florian; Kanerva, Mirella; Götting, Miriam; Nikinmaa, Mikko; Claireaux, Guy

doi:10.1016/j.cbpa.2022.111340

Cited by 3 publications

(3 citation statements)

References 84 publications

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“…Overall, the patterns of CS and LDH activities are consistent with our expectations given the role of the tissues in ecology of salmon, e.g. high LDH activity in white muscle, high CS activity in the heart, low activities in the liver [23,26]. Considering the small effect sizes from the genotypes and the large among-individual variation in metabolic processes, as also shown here, the genotype effects would not be feasible to detect without a balanced experimental design with a large sample size (still uncommon in physiological investigations).…”

Section: Discussionsupporting

confidence: 88%

“…The advantages of studying CS and LDH activities as proxies of mitochondrial content (and therefore aerobic capacity) and anaerobic capacity, respectively, are that their maximal activities can be measured in high throughput from frozen tissue samples across tissues with different functional roles. For example, glycolysis fuels fast-twitch (white) muscle anaerobically during burst swimming [22], while cardiac muscle typically has high capacity for both anaerobic and aerobic metabolism to maintain energy supply during routine function [23][24][25][26][27]. Although metabolic enzymes can be produced in excess in relation to performance needs [28], maintaining high mitochondrial content and anaerobic capacity is costly, thus among-individual variation in tissue-specific metabolic activities reflects differences in energy allocation [29].…”

Section: Introductionmentioning

confidence: 99%

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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: Discussionsupporting

confidence: 88%

Section: Introductionmentioning

confidence: 99%

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

Self Cite

View full text Add to dashboard Cite

show abstract

“…Furthermore, as TMAO is largely derived from diet (Treberg and Driedzic, 2006), it is reasonable to hypothesize that TMAO acts as a chaperone during chronic heat stress, whereas Hsp70 is a chaperone under acute heat stress. Notably, hsp70 transcript abundance increased in organs whose upper thermal limits are thought to contribute to whole-organism thermal limits: the brain and heart (Andreassen et al, 2022;Anttila et al, 2023). Indeed, a heat shock protein response in these tissues and possibly others (e.g.…”

Section: Discussionmentioning

confidence: 99%

Physiological responses to acute warming at the agitation temperature in a temperate shark

Bouyoucos,

Weinrauch,

Jeffries

et al. 2023

Journal of Experimental Biology

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Thermal tolerance and associated mechanisms are often tested via the critical thermal maximum (CTMax). The agitation temperature is a recently described thermal limit in fishes that has received little mechanistic evaluation. The present study used a temperate elasmobranch fish to test the hypothesis that this thermal tolerance trait is partially set by the onset of declining cardiorespiratory performance and the cellular stress response. Pacific spiny dogfish (Squalus suckleyi) were screened for cardiorespiratory and whole-organism thermal limits to test for associations between thermal performance and tolerance. Then, biochemical markers of secondary stress, aerobic and anaerobic enzyme activities, and molecular markers of cellular stress were determined for various tissues at the agitation temperature, and secondary stress markers were determined at CTMax. In dogfish, the agitation temperature was characterised by increased turning activity within experimental chambers and was equal to the temperature where dogfish exhibited maximum heart rate. Citrate synthase activity increased at the agitation temperature in white muscle relative to unmanipulated dogfish. Further, lactate dehydrogenase activity and accumulated lactate in the plasma and muscle were not affected by acute warming. Cellular stress was apparent in hypothalamus, gill filament, and ventricle, denoted by elevated transcript abundance of hsp70, but not hif1α. Conversely, CTMax was characterised by metabolic acidosis driven by anaerobic lactate production, signifying an increased reliance on anaerobic metabolism between the agitation temperature and CTMax. Together, these data provide partial support for our hypothesis, in that cellular stress, but not declining thermal performance, occurred at the agitation temperature.

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In a marine teleost, the significance of oxygen supply for acute thermal tolerance depends upon the context and the endpoint used

Nati

Blasco

Rodde

et al. 2023

Journal of Experimental Biology

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Eight juvenile European seabass were exposed to two thermal ramping protocols with different levels of aerobic activity and tolerance endpoint: the critical thermal maximum for swimming (CTSmax) while exercising aerobically until fatigue, and the critical thermal maximum (CTmax) under static conditions until loss of equilibrium (LOE). In the CTSmax, warming caused a profound increase in oxygen uptake rate (M˙O2) culminating in a gait transition, from steady aerobic towards unsteady anaerobic swimming, then fatigue at 30.3±0.4°C (mean±SE). Gait transition and fatigue presumably indicate an oxygen limitation, an inability to meet the combined demands of swimming plus warming. The CTmax also elicited an increase in M˙O2, culminating in LOE at 34.0±0.4°C, significantly warmer than fatigue at CTSmax. The maximum M˙O2 achieved in the CTmax was, however, less than 30% of that achieved in the CTSmax. Therefore, the static CTmax did not exploit full cardiorespiratory capacity for oxygen supply, indicating that LOE was not caused by systemic oxygen limitation. Consequently, systemic oxygen supply can be significant for tolerance of acute warming in seabass but this depends upon the physiological context and the endpoint used.

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Cardiovascular oxygen transport and peripheral oxygen extraction capacity contribute to acute heat tolerance in European seabass

Cited by 3 publications

References 84 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

Physiological responses to acute warming at the agitation temperature in a temperate shark

In a marine teleost, the significance of oxygen supply for acute thermal tolerance depends upon the context and the endpoint used

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