Skip to main content

Seasonal variations of trimethylamine oxide and urea in the blood of a cold-adapted marine teleost, the rainbow smelt

Fish Physiology and Biochemistry volume 13, pages 13–22 (1994)Cite this article

Abstract

Trimethylamine oxide (TMAO), which has previously not been known to occur in significant amounts in the blood of marine teleosts, rose to concentrations of approximately 50 mM in the blood of winter-acclimatized rainbow smelt, Osmerus mordax. Urea also increased in the blood of cold-acclimatized smelt, and, with TMAO, contributed significantly to the winter freezing point depression. TMAO and urea also varied seasonally in muscle and liver tissues. TMAO and urea appeared to be reabsorbed from the urine. Losses of TMAO and urea from the head region of the fish, where most of the losses appeared to occur, were approximately 9 μmol and 8 μmol 100 g−1 h−1, respectively. Despite the effluxes, TMAO and urea levels in both the blood and muscle either increased or were maintained in starved, cold-acclimated fish, suggesting that they were synthesized in response to cold temperature. TMAO was also found in the blood of some other cold-hardy teleosts.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

References cited

  • Augustsson, I. and Strom, A.R. 1981. Biosynthesis and turnover of trimethylamine oxide in the teleost cod, Gadus morhua. J. Biol. Chem. 256: 8045–8049.

    Google Scholar 

  • Baker, R.J., Struempler, A. and Chaykin, S. 1963. A comparative study of trimethylamine N-oxide biosynthesis. Biochim. Biophys. Acta 71: 58–64.

    PubMed  CAS  Article  Google Scholar 

  • Boylan, J.W. 1967. Gill permeability in Squalus acanthias. In Sharks, Skates and Rays. pp 197–206. Edited by P.M. Gilbert, R.F. Mathewson and D.P. Rall. The Johns Hopkins Press, Baltimore.

    Google Scholar 

  • Brull, L. and Nizet, E. 1953. Blood and urine constituents of Lophius piscatorius L. J. Mar. Biol. Ass. U.K. 32: 321–328.

    CAS  Article  Google Scholar 

  • Charest, R.P., Chenoweth, M. and Dunn, A. 1988. Metabolism of trimethylamines in kelp bass (Paralabrax clathratus) and marine and freshwater pink salmon (Oncorhynchus gorbuscha). J. Comp. Physiol. B. 158: 609–619.

    PubMed  CAS  Article  Google Scholar 

  • Cohen, J.J., Krupp, M.A. and Chidsey, C.A. 1958. Renal conservation of trimethylamine oxide by spiny dogfish. Am. J. Physiol. 194: 229–235.

    PubMed  CAS  Google Scholar 

  • Curtis, B.J. and Wood, C.M. 1991. The function of the urinary bladder in vivo in the freshwater rainbow trout. J. Exp. Biol. 155: 567–583.

    Google Scholar 

  • DeVries, A.L. and Wohlschlag, D.E. 1969. Freezing resistance in some Antarctic fishes. Science 163: 1073–1075.

    PubMed  CAS  Google Scholar 

  • Daikoku, T. 1980. Changes in osmotic and ionic concentrations of various tissues of the guppy, Poecilia reticulata, with adaptation to sea water and the effect of dietary trimethylamine on these changes. Comp. Biochem. Physiol. 66A: 189–195.

    Article  Google Scholar 

  • Daikoku, T. and Sakaguchi, M. 1983. Effects of dietary trimethylamine on free amino acid and nonprotein nitrogen levels in muscle of the guppy, Poecilia reticulata, in relation to seawater adaptation. Comp. Biochem Physiol. 75A: 343–346.

    CAS  Google Scholar 

  • Duman, J.G. and DeVries, A.L. 1974. The effects of temperature and photoperiod on antifreeze production in cold water fishes. J. Exp. Zool. 190: 89–98.

    PubMed  CAS  Article  Google Scholar 

  • Dyer, W.J. 1952. Amines in fish muscle. VI. Trimethylamine oxide content of fish and marine invertebrates. J. Fish. Res. Bd. Can. 8: 314–324.

    CAS  Google Scholar 

  • Ewart, K.V., Rubinsky, B. and Fletcher, G.L. 1992. Structural and functional similarity between fish antifreeze proteins and calcium-dependent lectins. Biochem. Biophys. Res. Comm. 185: 335–340.

    PubMed  CAS  Google Scholar 

  • Forster, R.P., Berglund, F. and Rennick, B.R. 1958. Tubular secretion of creatine, trimethylamine oxide, and other organic bases by the aglomerular kidney of Lophius americanus. J. Gen. Physiol. 42: 319–327.

    PubMed  CAS  Article  Google Scholar 

  • Forster, R.P. and Goldstein, L. 1976. Intracellular osmoregulatory role of amino acids and urea in marine elasmobranchs. Am. J. Physiol. 230: 925–931.

    PubMed  CAS  Google Scholar 

  • Forster, R.P. and Goldstein, L. 1965. Formation of excretory products. In Fish Physiology. Vol 1, pp. 313–350. Edited by W.S. Hoar and D.J. Randall. Academic Press, New York.

  • Goldstein, L. and Palatt, P.J. 1974. Trimethylamine oxide excretion rates in elasmobranchs. Am. J. Physiol. 227: 1268–1272.

    PubMed  CAS  Google Scholar 

  • Gordon, M.S., Amdur, B.H. and Scholander, P.F. 1962. Freezing resistance in some northern fishes. Biol. Bull. 122: 52–62.

    Google Scholar 

  • Hebard, C.E., Flick, G.J. and Martin, R.E. 1982. Occurrence and significance of trimethylamine oxide and its derivatives in fish and shellfish. In Chemistry and Biochemistry of Marine Food Products. pp. 149–304. Edited by R.E. Martin, G.J. Flick, C.E. Hebard and D.R. Ward. AVI Publishing Co., Westport.

    Google Scholar 

  • Henderson, I.W., O'Toole, L.B. and Hazon, N. 1988. Kidney function. In Physiology of Elasmobranch Fishes. pp. 201–214. Edited by T.J. Shuttleworth. Springer-Verlag, Berlin.

    Google Scholar 

  • Holliday, F.G.T. and Blaxter, J.H.S. 1963. The behavior and physiology of herring and other clupeids. In Advances in Marine Biology. Vol. 1, pp. 262–393. Edited by F.S. Russell. Academic Press, London.

  • Holmes, W.N. and Donaldson, E.M. 1969. The body compartments and the distribution of electrolytes. In Fish Physiology. Vol. 1, pp. 1–90. Edited by W.S. Hoar and D.J. Randall. Academic Press, New York.

  • Hughes, R.B. 1959. Chemical studies on the herring (Clupea harengus). 1. Trimethylamine oxide and volatile amines in fresh, spoiling and cooked herring. J. Sci. Food. Agric. 10: 431–436.

    CAS  Google Scholar 

  • Kakuta, I. 1988. The role of non-protein nitrogenous compounds in osmotic regulation of Tridentiger obscurus and T. brevispinis. Comp. Biochem. Physiol. 90A: 109–113.

    Google Scholar 

  • Lange, R. and Fugelli, K. 1965. The osmotic adjustments in the euryhaline teleosts, the flounder, Pseudopleuronectes flesus L. and the three-spined stickleback, Gasterosteus aculeatus L. Comp. Biochem. Physiol. 15: 283–292.

    PubMed  CAS  Article  Google Scholar 

  • Norris, E.R. and Benoit, G.J. 1945. Studies on trimethylamine oxide. 1. Occurrence of trimethylamine oxide in marine organisms. J. Biol. Chem. 158: 433–438.

    CAS  Google Scholar 

  • O'Grady, S.M. and DeVries, A.L. 1992. Osmotic and ionic regulation in polar fishes. J. Exp. Mar. Biol. Ecol. 57: 219–228.

    Article  Google Scholar 

  • Parry, G. 1961. Osmotic and ionic changes in blood and muscle of migrating salmonids. J. Exp. Biol. 38: 411–427.

    CAS  Google Scholar 

  • Prosser, C.L., MacKay, W. and Kato, K. 1970. Osmotic and ionic concentrations in some Alaskan fish and goldfish from different temperatures. Physiol. Zool. 43: 81–89.

    CAS  Google Scholar 

  • Raymond, J.A. and DeVries, A.L. 1977. Adsorption inhibition as a mechanism of freezing resistance in polar fishes. Proc. Natl. Acad. Sci. U.S.A. 74: 2589–2593.

    PubMed  CAS  Article  Google Scholar 

  • Raymond, J.A. 1989. Freezing resistance in some northern populations of Pacific herring, Clupea harengus pallasi. Can. J. Fish. Aquat. Sci. 46: 2104–2107.

    Article  Google Scholar 

  • Raymond, J.A. 1992. Glycerol is a colligative antifreeze in some northern fishes. J. Exp. Zool. 262: 347–352.

    CAS  Article  Google Scholar 

  • Raymond, J.A. 1993. Glycerol and water balance in a nearisosmotic teleost, winter-acclimatized rainbow smelt. Can. J. Zool. 71: 1849–1854.

    CAS  Article  Google Scholar 

  • Robertson, J.D. 1975. Osmotic constituents of the blood plasma and parietal muscle of Squalus acanthias L. Biol. Bull. 148: 303–319.

    PubMed  CAS  Google Scholar 

  • Sakaguchi, M. and Murata, M. 1986. Distribution of free amino acids, creatine and trimethylamine oxide in mackerel and yellowtail. Bull. Jap. Soc. Sci. Fish. 52: 685–689.

    CAS  Google Scholar 

  • Sayer, M.D.J. and Davenport, J. 1987. The relative importance of the gills to ammonia and urea excretion in five seawater and one freshwater teleost species. J. Fish Biol. 31: 561–570.

    Article  Google Scholar 

  • Shewan, J.M. 1951. The chemistry and metabolism of the nitrogenous extractives in fish. Biochem. Soc. Symp. 6: 28–48.

    Google Scholar 

  • Smith, R.N. 1972. The freezing resistance of antarctic fish: l. Serum composition and its relation to freezing resistance. Bull. Brit. Antarctic Surv. 28: 1–10.

    Google Scholar 

  • Somero, G.N. 1992. Adapting to water stress: convergence on common solutions. In Water and Life. Comparative Analysis of Water Relationships at the Organismic, Cellular and Molecular Levels. pp. 3–18. Edited by G.N. Somero, C.B. Osmond and C.L. Bolis. Springer-Verlag, Berlin.

    Google Scholar 

  • Suyama, M. and Tokuhiro, T. 1954. Urea content and ammonia formation of the muscle of cartilaginous fishes. III. The distribution of urea and trimethylamine oxide in different parts of the body. Bull. Jap. Soc. Sci. Fish. 19: 1003–1006.

    CAS  Google Scholar 

  • Timasheff, S.N. 1992. A physicochemical basis for the selection of osmolytes by Nature. In Water and Life. Comparative Analysis of Water Relationships at the Organismic, Cellular and Molecular Levels. pp. 70–84. Edited by G.N. Somero, C.B. Osmond and C.L. Bolis. Springer-Verlag, Berlin.

    Google Scholar 

  • Van Waarde, A. 1988. Biochemistry of non-protein nitrogenous compounds in fish including the use of amino acids for anaerobic energy production. Comp. Biochem Physiol. 91B: 207–228.

    Article  Google Scholar 

  • Wekell, J.C. and Barnett, H. 1991. New method for analysis of trimethylamine oxide using ferrous sulfate and EDTA. J. Food Sci. 56: 132–138.

    CAS  Google Scholar 

  • Wright, P.A., Iwama, G.K. and Wood, C.M. 1993. Ammonia and urea excretion in Lahontan cutthroat trout (Oncorhynchus clarki henshawi) adapted to the highly alkaline Pyramid Lake (pH 9.4). J. Exp. Biol. 175: 153–172.

    CAS  Google Scholar 

  • Yamada, K. 1967. Occurrence and origin of trimethylamine oxide in fishes and marine invertebrates. Bull. Jap. Soc. Sci. Fish. 33: 591–603.

    Google Scholar 

  • Yancey, P.H., Clark, M.E., Hand, S.C., Bowlus, R.D. and Somero, G.N. 1982. Living with water stress: evolution of osmolyte systems. Science 217: 1214–1222.

    PubMed  CAS  Google Scholar 

Download references

Author information

Affiliations

  1. Department of Biological Sciences, University of South Alabama, Mobile, AL, 36688, U.S.A.

    James A. Raymond

Authors
  1. James A. Raymond
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Raymond, J.A. Seasonal variations of trimethylamine oxide and urea in the blood of a cold-adapted marine teleost, the rainbow smelt. Fish Physiol Biochem 13, 13–22 (1994). https://doi.org/10.1007/BF00004115

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00004115

Keywords

  • serum trimethylamine oxide
  • serum urea
  • marine teleost
  • freezing resistance
  • Osmerus mordax