Abstract
Energy requirements of tissues vary greatly and exhibit different mitochondrial respiratory activities with variable participation of both substrates and oxidative phosphorylation. The present study aimed to (1) compare the substrate preferences of mitochondria from different tissues and fish species with different ecological characteristics, (2) identify an appropriate substrate for comparing metabolism by mitochondria from different tissues and species, and (3) explore the relationship between mitochondrial metabolism mechanisms and ecological energetic strategies. Respiration rates and cytochrome c oxidase (CCO) activities of mitochondria isolated from heart, brain, kidney, and other tissues from Silurus meridionalis, Carassius auratus, and Megalobrama amblycephala were measured using succinate (complex II-linked substrate), pyruvate (complex I-linked), glutamate (complex I-linked), or combinations. Mitochondria from all tissues and species exhibited substrate preferences. Mitochondria exhibited greater coupling efficiencies and lower leakage rates using either complex I-linked substrates, whereas an opposite trend was observed for succinate (complex II-linked). Furthermore, maximum mitochondrial respiration rates were higher with the substrate combinations than with individual substrates; therefore, state III respiration rates measured with substrate combinations could be effective indicators of maximum mitochondrial metabolic capacity. Regardless of fish species, both state III respiration rates and CCO activities were the highest in heart mitochondria, followed by red muscle mitochondria. However, differences in substrate preferences were not associated with species feeding habit. The maximum respiration rates of heart mitochondria with substrate combinations could indicate differences in locomotor performances, with higher metabolic rates being associated with greater capacity for sustained swimming.
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The data that support the findings of this study are available from the corresponding author upon request.
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Abbreviations
- ANOVA:
-
Analysis of variance
- ADP:
-
Adenosine diphosphate
- ATP:
-
Adenosine triphosphate
- CCO:
-
Cytochrome c oxidase
- CS:
-
Citrate synthase
- FADH2:
-
Flavine adenine dinucleotide
- G:
-
Glutamate
- P:
-
Pyruvate
- M:
-
Malate
- NADH:
-
Reduced nicotinamide adenine dinucleotide
- OXPHOS:
-
Oxidative phosphorylation
- RCR:
-
Respiration control ratio
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Acknowledgements
We are grateful to Daofu Ming, Qinzhu Dai, and Nan Wu, for their experimental assistance.
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This study was supported by the Natural Science Foundation of China (No. 31300338) and the Fundamental Research Funds for the Central Universities (No. XDJK2016C156).
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Jing Long, Xiaojun Xie, Yulian Yan conceived and designed the experiments. Jing Long, Yiguo Xia and Hanxun Qiu performed all the experiments and analyzed the data. Jing Long and Yulian Yan drafted manuscript and all authors discussed and revised the manuscript.
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Long, J., Xia, Y., Qiu, H. et al. Respiratory substrate preferences in mitochondria isolated from different tissues of three fish species. Fish Physiol Biochem 48, 1555–1567 (2022). https://doi.org/10.1007/s10695-022-01137-6
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DOI: https://doi.org/10.1007/s10695-022-01137-6