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1H-NMR study of the metabolome of a moderately hypoxia-tolerant fish, the common carp (Cyprinus carpio)

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Abstract

All 20.000 different fish species vary greatly in their ability to tolerate and survive fluctuating oxygen concentrations in the water. Especially fish of the genus Carassius, e.g. the crucian carp and the goldfish, exhibit a remarkable tolerance to limited/absent oxygen concentrations. The metabolic changes of anoxia-tolerant crucian carp were recently studied and published. Contrary to crucian carp, the hypoxia-tolerant common carp cannot survive a complete lack of oxygen (anoxia). Therefore, we studied the 1H-NMR-based metabolomics of brain, heart, liver and white muscle extracts of common carp, subjected to anoxia (0 mg O2 l−1) and hypoxia (0.9 mg O2 l−1) at 5 °C. Specifically, fish were exposed to normoxia (i.e. 9 mg O2 l−1; controls 24 h, 1 week and 2 weeks), acute hypoxia (24 h), chronic hypoxia (1 week) and chronic hypoxia (1 week) with normoxic reoxygenation (1 week). Additionally, we also investigated the metabolic responses of fish to anoxia for 2 h. Both anoxia and hypoxia significantly changed the tissue levels of standard energy metabolites as lactate, glycogen, ATP/ADP and phosphocreatine. Remarkably, anoxia induced increased lactate levels in all tissues except for the heart whereas hypoxia resulted in decreased lactate concentrations in all tissues except for brains. Furthermore, hypoxia and anoxia influenced amino acids (alanine, valine/(iso)leucine) and neurotransmitters levels (GABA, glutamate). Lastly, we also detected ‘other’ i.e. previously not reported compounds to play a role in the present context. Scyllo-inositol levels changed significantly in heart, liver and muscle, providing novel insights into the anoxia/hypoxic responses of the common carp.

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Acknowledgments

Isabelle Lardon and Trung Nghia Vu are funded by interdisciplinary scholarships of the University of Antwerp. The 700 MHz NMR spectrometer (Ghent, Belgium) of the interuniversity NMR facility was financed by Ghent University, the Free University of Brussels (VUB) and the University of Antwerp.

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Correspondence to Isabelle Lardon.

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Lardon, I., Eyckmans, M., Vu, T.N. et al. 1H-NMR study of the metabolome of a moderately hypoxia-tolerant fish, the common carp (Cyprinus carpio). Metabolomics 9, 1216–1227 (2013). https://doi.org/10.1007/s11306-013-0540-y

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Keywords

  • Common carp
  • Metabolomics
  • 1H-NMR
  • Hypoxia
  • Anoxia
  • Tissue extracts