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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Benjamini, Y., & Hochberg, Y. (1995). Controlling the false discovery rate: A practical and powerful approach to multiple testing. Journal of the Royal Statistical Society - Series B (Methodological), 57(1), 289–300.
Bickler, P. E., & Buck, L. T. (2007). Hypoxia tolerance in reptiles, amphibians, and fishes: Life with variable oxygen availability. Annual Review of Physiology, 69, 145–170.
Chatham, J. C. (2002). Lactate—The forgotten fuel! Journal of Physiology, 542(2), 333.
Coen, M., Lenz, E. M., Nicholson, J. K., et al. (2003). An integrated metabonomic investigation of acetaminophen toxicity in the mouse using NMR spectroscopy. Chemical Research in Toxicology, 16(3), 295–303.
Ekman, D. R., Teng, Q. N., Villeneuve, D. L., Kahl, M. D., Jensen, K. M., Durhan, E. J., et al. (2009). Profiling lipid metabolites yields unique information on sex- and time-dependent responses of fathead minnows (Pimephales promelas) exposed to 17 alpha-ethynylestradiol. Metabolomics, 5(1), 22–32.
Griffith, H. R., den Hollander, J. A., Stewart, C. C., Evanochko, W. T., Buchthal, S. D., Harrell, L. E., et al. (2007). Elevated brain scyllo-inositol concentrations in patients with Alzheimer’s disease. NMR in Biomedicine, 8, 709–716.
Hallman, T. M., Rojas-Vargas, A. C., Jones, D. R., & Richards, J. G. (2008). Differential recovery from exercise and hypoxia exposure measured using (31)P- and (1)H-NMR in white muscle of the common carp Cyprinus carpio. Journal of Experimental Biology, 211(20), 3237–3248.
Hylland, P., & Nilsson, G. E. (1999). Extracellular levels of amino acid neurotransmitters during anoxia and forced energy deficiency in crucian carp brain. Brain Research, 823, 49–58.
Jobling, M. (1994). Book of fish bioenergetics- fish and fisheries series 13 (1st edition). London: Chapman & Hall.
Karakach, T. K., Huenupi, E. C., Soo, E. C., Walter, J. A., & Afonso, L. O. B. (2009). (1)H-NMR and mass spectrometric characterization of the metabolic response of juvenile Atlantic salmon (Salmo salar) to long-term handling stress. Metabolomics, 5(1), 123–137.
Kemppainen, J., Fujimoto, T., Kalliokoski, K. K., Viljanen, T., Nuutila, P., & Knuuti, J. (2002). Myocardial and skeletal muscle glucose uptake during exercise in humans. Journal of Physiology, 542(2), 403–412.
Kullgren, A., Samuelsson, L. M., & Forlin, L. (2010). A metabolomics approach to elucidate effects of food deprivation in juvenile rainbow trout (Oncorhynchus mykiss). American Journal of Physiology-Regulatory Integrative and Comparative Physiology, 299(6), R1440–R1448.
Lardon, I., Nilsson, G. E., Stecyk, J. A. W., Vu, N. T., Laukens, K., Dommisse, R., et al. (2012). 1H-NMR study of the metabolome of an exceptionally anoxia tolerant vertebrate, the crucian carp (Carassius carassius). Metabolomics,. doi:10.1007/s11306-012-0448-y.
Lin, C. Y., Wu, H. F., Tjeerdema, R. S., & Viant, M. R. (2007). Evaluation of metabolite extraction strategies from tissue samples using NMR metabolomics. Metabolomics, 3(1), 55–67.
Milligan, L. C., & Pagnotta, A. (1991). The role of blood glucose in the restoration of muscle glycogen during recovery from exhaustive exercise in rainbow trout (Oncorhynchus mykiss) and winter flounder (Pseudopleuronectes americanus). Journal of Experimental Biology, 161, 489–508.
Neely, J. R., & Morgan, H. E. (1974). Relationship between carbohydrate and lipid metabolism and the energy balance of heart muscle. Annual Review of Physiology, 36, 413–459.
Nilsson, G. E. (1990). Long term anoxia in crucian carp: Changes in the levels of amino acid and monoamine neurotransmitters in the brain, catecholamines in chromaffin tissue, and liver glycogen. Journal of Experimental Biology, 150, 295–320.
Podrabsky, J. E., Lopez, J. P., Fan, T. W. M., Higashi, R., & Somero, G. N. (2007). Extreme anoxia tolerance in embryos of the annual killifish Austrofundulus limnaeus: Insights from a metabolomics analysis. Journal of Experimental Biology, 210(13), 2253–2266.
Prentice, H. M. (2009). The major contribution of brain GABAergic function to anoxic survival. Physiological Genomics, 36, 59–60.
Segner, H., Dolle, A., & Bohm, R. (1997). Ketone body metabolism in the carp Cyprinus carpio: Biochemical and H-1 NMR spectroscopical analysis. Comparative Biochemistry and Physiology B-Biochemistry & Molecular Biology, 116(2), 257–262.
Stecyk, J. A. W., Stenlocken, K. O., Farrell, A. P., & Nilsson, G. E. (2004). Maintained cardiac pumping in anoxic crucian carp. Science, 306, 77.
Stentiford, G. D., Viant, M. R., Ward, D. G., et al. (2005). Liver tumors in wild flatfish: A histopathological, proteomic, and metabolomic study. OMICS: A Journal of Integrative Biology, 9(3), 281–299.
Sumner, L. W., Amberg, A., Barrett, D., Beale, M. H., Beger, R., Daykin, C. A., et al. (2007). Proposed minimum reporting standards for chemical analysis. Metabolomics, 3, 211–221.
Tang, Y., & Boutilier, R. G. (1991). White muscle intracellular acid-base and lactate status following exhaustive exercise: A comparison between freshwater- and seawater-adapted rainbow trout. Journal of Experimental Biology, 156, 153–171.
Tota, B., Angelone, T., Mancardi, D., & Cerra, M. C. (2011). Hypoxia and anoxia tolerance of vertebrate hearts: An evolutionary perspective. Antioxidants & Redox Signaling, 14(5), 851–862.
Voet, D., & Voet, J. (1995). Biochemistry (2nd ed.). New York: Wiley.
Wang, Y., Haipeng, S., Lu, G., Ren, S., & Chen, J. (2011). Catabolism of branched-chain amino acids in heart failure: Insights from genetic models. Pediatric Cardiology, 32, 305–310.
Wu, H. F., Southam, A. D., Hines, A., & Viant, M. R. (2008). High-throughput tissue extraction protocol for NMR and MS-based metabolomics. Journal of Analytical Biochemistry, 372(2), 204–212.
Zhou, B. S., Wu, R. S. S., Randall, D. J., Lam, P. K. S., Ip, Y. K., & Chew, S. F. (2000). Metabolic adjustments in the common carp during prolonged hypoxia. Journal of Fish Biology, 57, 1160–1171.
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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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
- Common carp
- Tissue extracts