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1H-NMR study of the metabolome of an exceptionally anoxia tolerant vertebrate, the crucian carp (Carassius carassius)

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Abstract

The crucian carp (Carassius carassius) can tolerate anoxia for days to months, depending on the temperature. In this study, we applied 1H-NMR-based metabolomics to polar extracts of crucian carp brain, heart, muscle and liver samples obtained from fish exposed to either control normoxic conditions, acute anoxia (24 h), chronic anoxia (1 week) or reoxygenation (for 1 week following chronic anoxia) at 5 °C. Spectra of the examined tissues revealed changes in several energy-related compounds. In particular, anoxic stress resulted in decreased concentrations of phosphocreatine (muscle, liver) and glycogen (liver) and ATP/ADP (liver, heart and muscle) and increased concentrations of lactate (brain, heart, muscle) and beta-hydroxybutyric acid (all tissues). Likewise, increased concentrations of inhibitory compounds (glycine, gamma-amino butyric acid or GABA) and decreased concentrations of excitatory metabolites (glutamate, glutamine) were confirmed in the anoxic brain extracts. Additionally, a decrease of N-acetylaspartate (NAA), an important neuronal marker, was also observed in anoxic brains. The branched-chain amino acids (BCAA) valine/isoleucine/leucine increased in all anoxic tissues. Possibly, this general tissue increase can be due to an inhibited mitochondrial function or due to protein degradation/protein synthesis inhibition. In this study, the potential and strength of the 1H-NMR is highlighted by the detection of previously unrecognized changes in metabolites. Specifically, myo-inositol substantially decreased in the heart of anoxic crucian carp and anoxic muscle tissue displayed a decreased concentration of taurine, providing novel insights into the anoxia responses of the crucian carp.

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Acknowledgments

Isabelle Lardon and Trung Nghia Vu are funded by interdisciplinar scholarships of the University of Antwerp.

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Authors and Affiliations

  1. Departments of Chemistry and Biology, University of Antwerp, Groenenborgerlaan 171, 2020, Antwerp, Belgium

    Isabelle Lardon, Roger Dommisse & Gudrun De Boeck

  2. Department of Molecular Biosciences, University of Oslo, Blindernveien 31, 0316, Oslo, Norway

    Göran E. Nilsson & Jonathan A. W. Stecyk

  3. Department of Mathematics and Computer Science, University of Antwerp, Middelheimlaan 1, 2020, Antwerp, Belgium

    Trung Nghia Vu & Kris Laukens

  4. Biomina-Biomedical Informatics Research Center Antwerp, Wilrijkstraat 10, 2650 Edegem, Antwerp, Belgium

    Trung Nghia Vu & Kris Laukens

  5. Department of Applied NMR and Laboratory for Systemic Physiological and Ecotoxicological Research (SPHERE), University of Antwerp, Groenenborgerlaan 171, 2020, Antwerp, Belgium

    Isabelle Lardon

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  1. Isabelle Lardon
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  2. Göran E. Nilsson
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  3. Jonathan A. W. Stecyk
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  4. Trung Nghia Vu
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  5. Kris Laukens
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Correspondence to Isabelle Lardon.

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Lardon, I., Nilsson, G.E., Stecyk, J.A.W. et al. 1H-NMR study of the metabolome of an exceptionally anoxia tolerant vertebrate, the crucian carp (Carassius carassius). Metabolomics 9, 311–323 (2013). https://doi.org/10.1007/s11306-012-0448-y

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