Biochemical Genetics

, Volume 24, Issue 1–2, pp 51–69 | Cite as

The effect of dietary ethanol on the composition of lipids of Drosophila melanogaster larvae

  • Billy W. Geer
  • Stephen W. McKechnie
  • Marilyn L. Langevin
Article

Abstract

At a moderate concentration (2.5%, v/v) dietary ethanol reduced the chain length of total fatty acids (FA) and increased the desaturation of short-chain FA in Drosophila melanogaster larvae with a functional alcohol dehydrogenase (ADH). The changes in length in total FA were postulated to be due to the modulation of the termination specificity of fatty acid synthetase. Because the ethanol-stimulated reduction in the length of unsaturated FA was blocked by linoleic acid, it was thought to reflect the properties of FA 9-desaturase. Although the ethanol-stimulated reduction in chain length of unsaturated FA was also observed in ADH-null larvae, ethanol promoted an increase in the length of total FA of the mutant larvae. Thus, the ethanolstimulated change in FA length was ADH dependent but the ethanol effect on FA desaturation was not. Ethanol also stimulated a decrease in the relative amount of phosphatidylcholine and an increase in phosphatidylethanolamine. Because similar ethanol-induced changes have been found in membrane lipids of other animals, ethanol may alter the properties of membranes in larvae. It is proposed that ethanol tolerance in D. melanogaster may be dependent on genes that specify lipids that are resistant to the detrimental effects of ethanol.

Key words

ethanol lipid alcohol dehydrogenase Drosophila nutrition 

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References

  1. Beenakkers, A. M. T. (1969). Carbohydrate and fat as a fuel for insect flight. A comparative study. J. Insect Physiol. 15353.Google Scholar
  2. Bradford, M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein dye binding. Anal. Biochem. 72248.Google Scholar
  3. Bridges, R. G., and Watts, S. G. (1976). Synthesis of fatty acids in vitro by choline-deficient and normal larvae of the housefly, Musca domestica. J. Insect Physiol. 22101.Google Scholar
  4. Buttke, T. M., and Ingram, L. O. (1980). Ethanol-induced changes in lipid composition of Escherichia coli: Inhibition of saturated fatty acid synthesis in vitro. Arch. Biochem. Biophys. 203565.Google Scholar
  5. Carey, E. M., and Dils, R. (1973). Regulation of the chain length of fatty acids synthesized by cell-free preparations of lactating rabbit, rat and guinea pig mammary gland. Comp. Biochem. Physiol. 44B989.Google Scholar
  6. Cavener, D. G., and Clegg, M. T. (1978). Dynamics of correlated genetic systems. IV. Multilocus effects of ethanol stress environments. Genetics 90629.Google Scholar
  7. Cavener, D. G., and Clegg, M. T. (1981). Multigenic response to ethanol in Drosophila melanogaster. Evolution 351.Google Scholar
  8. Church, R. B., and Robertson, F. W. (1966). A biochemical study of the growth of Drosophila melanogaster. J. Exp. Zool. 162337.Google Scholar
  9. Cohan, F. M., and Graf, J. (1985). Latitudinal cline in Drosophila melanogaster for knockdown resistance to ethanol fumes and for rates of response to selection for further resistance. Evolution 39278.Google Scholar
  10. David, J., and Bocquet, C. (1975). Evolution in a cosmopolitan species: Genetic latitudinal clines in Drosophila melanogaster wild populations. Experientia 31164.Google Scholar
  11. David, J. R., Bocquet, C., Arens, M., and Fouillet, P. (1976). Biological role of alcohol dehydrogenase in the tolerance of Drosophila melanogaster to aliphatic alcohols: Utilization of an ADH-null mutant. Biochem. Genet. 14989.Google Scholar
  12. De Schrijver, R., and Privett, O. S. (1983). Hepatic fatty acids and acyl desaturases in rats: Effects of dietary carbohydrate and essential fatty acids. J. Nutr. 1132217.Google Scholar
  13. Folch, J., Lees, M., and Sloane Stanley, G. H. (1957). A simple method for the isolation and purification of total lipids from animal tissues. J. Biol. Chem. 226497.Google Scholar
  14. Geer, B. W., and Downing, B. C. (1972). Changes in lipid and protein syntheses during spermatozoan development and thoracic tissue maturation in Drosophila hydei. Wilhelm Roux Arch. EntwMech. Org. 17083.Google Scholar
  15. Geer, B. W., and Perille, T. T. (1977). Effects of dietary sucrose and environmental temperature on fatty acid synthesis in Drosophila melanogaster. Insect Biochem. 7371.Google Scholar
  16. Geer, B. W., and Vovis, G. F. (1965). The effects of choline and related compounds on the growth and development of Drosophila melanogaster. J. Exp. Zool. 158223.Google Scholar
  17. Geer, B. W., Dolph, W. W., Maguire, J. A., and Dates, R. J. (1971). The metabolism of dietary carnitine in Drosophila melanogaster. J. Exp. Zool. 176445.Google Scholar
  18. Geer, B. W., Kamiak, S. N., Kidd, K. R., Nishimura, R. A., and Yemm, S. J. (1976). Regulation of the oxidative NADP-enzyme tissue levels in Drosophila melanogaster. I. Modulation by dietary carbohydrate and lipid. J. Exp. Zool. 19515.Google Scholar
  19. Geer, B. W., Lindel, D. L., and Lindel, D. M. (1979). The relationship of the oxidative pentose shunt pathway to lipid synthesis in Drosophila melanogaster. Biochem. Genet. 17867.Google Scholar
  20. Geer, B. W., McKechnie, S. W., and Langevin, M. L. (1983). Regulation of sn-glycerol-3-phosphate dehydrogenase in Drosophila melanogaster larvae by dietary ethanol and sucrose. J. Nutr. 1131632.Google Scholar
  21. Geer, B. W., Langevin, M. L., and McKechnie, S. W. (1985). Dietary ethanol and lipid synthesis in Drosophila melanogaster. Biochem. Genet. 23607.Google Scholar
  22. Gibson, J. B., May, T. W., and Wilks, A. V. (1981). Genetic variation at the alcohol dehydrogenase locus in Drosophila melanogaster in relation to environmental variations: Ethanol levels in breeding sites and allozyme frequencies. Oecologia (Berl.) 51191.Google Scholar
  23. Goto, M., Banno, Y., Umeki, S., Kameyama, Y., and Nozawa, Y. (1983). Effects of chronic ethanol exposure on composition and metabolism of Tetrahymena membrane lipids. Biochim. Biophys. Acta 751286.Google Scholar
  24. Green, P. R., and Geer, B. W. (1979). Changes in the fatty acid composition of Drosophila melanogaster during development and ageing. Arch. Int. Physiol. Biochem. 87485.Google Scholar
  25. Grell, E. H., Jacobson, K. B., and Murphy, J. B. (1968). Alterations of genetic material for analysis of alcohol dehydrogenase isozymes of Drosophila melanogaster. Ann. N.Y. Acad. Sci. 151441.Google Scholar
  26. Hayashida, S., Feng, D. D., and Hongo, M. (1974). Function of the high concentration alcohol-producing factor. Agr. Biol. Chem. 382001.Google Scholar
  27. Herrero, A. A., Gomez, R. F., and Roberts, M. F. (1982). Ethanol induced changes in the membrane lipid composition of Clostridium thermocellum. Biochim. Biophys. Acta 693195.Google Scholar
  28. Horie, Y. (1968). The oxidation of NADPH by the soluble fraction of the fat body of the silkworm, Bombyx mori L. J. Insect Physiol. 14417.Google Scholar
  29. Ingram, L. O., Vreeland, N. S., and Eaton, L. C. (1980). Alcohol tolerance in Escherichia coli. Pharmacol. Biochem. Behav. 13191.Google Scholar
  30. Jeffcoat, R., and James, A. T. (1977). Interrelationship between dietary regulation of fatty acid synthesis and the fatty acyl-CoA desaturase. Lipids 12469.Google Scholar
  31. Jeffcoat, R., Roberts, P. A., and James, A. T. (1979). The control of lipogenesis by dietary linoleic acid and its influence on the deposition of fat. Eur. J. Biochem. 101447.Google Scholar
  32. McKechnie, S. W., and Geer, B. W. (1984). Regulation of alcohol dehydrogenase in Drosophila melanogaster by dietary alcohol and carbohydrate. Insect Biochem. 14231.Google Scholar
  33. McKechnie, S. W., and Morgan, P. (1982). Alcohol dehydrogenase polymorphism of Drosophila melanogaster: Aspects of alcohol and temperature variation in the larval environment. Aust. J. Biol. Sci. 3585.Google Scholar
  34. McKenzie, J. A., and McKechnie, S. W. (1978). Ethanol tolerance and the Adh polymorphism in a natural population of Drosophila melanogaster. Nature 27275.Google Scholar
  35. McKenzie, J. A., and Parsons, P. A. (1972). Alcohol tolerance: an ecological parameter in the relative success of Drosophila melanogaster and Drosophila simulans. Oecologia (Berl.) 10373.Google Scholar
  36. McKenzie, J. A., and Parsons, P. A. (1974). Microdifferentiation in a natural population of Drosophila melanogaster to alcohol in the environment. Genetics 77385.Google Scholar
  37. Metcalfe, L. D., Schmitz, A. A., and Pelka, J. R. (1966). Rapid preparation of fatty acid esters from lipids for gas chromatographic analysis. Anal. Chem. 38514.Google Scholar
  38. Nandini-Kishore, S. G., Mattox, S. M., Martin, C. E., and Thompson, G. A. (1979). Membrane change during growth of Tetrahymena in the presence of ethanol. Biochim. Biophys. Acta 551315.Google Scholar
  39. Oakeshott, J. G., Gibson, J. B., and Wilson, S. R. (1984). Selective effects of the genetic background and ethanol on the alcohol dehydrogenase polymorphism in Drosophila melanogaster. Heredity 5351.Google Scholar
  40. Op den Kamp, J. A. F. (1979). Lipid asymmetry in membranes. Annu. Rev. Biochem. 48:47.Google Scholar
  41. Parsons, P. A. (1980). Adaptive strategies in natural populations of Drosophila. Theoret. Appl. Genet. 57257.Google Scholar
  42. Pinter, J. K., Hayashi, J. A., and Watson, J. A. (1967). Enzymatic assay of glycerol, dihydroxyacetone and glyceraldehyde. Arch. Biochem. Biophys. 121404.Google Scholar
  43. Rognstad, R., and Grunnet, N. (1979). Enzymatic pathways of ethanol metabolism. In Majchrowicz, E., and Nobel, E. P. (eds.), Plenum Press, New York, Vol. 1, pp. 65–87.Google Scholar
  44. Schwartz, M., and Sofer, W. H. (1976). Alcohol dehydrogenase negative mutants in Drosophila: Defects at the structural locus? Genetics 83125.Google Scholar
  45. Snedecor, G. W. (1957). Statistical Methods Iowa State College Press, Ames.Google Scholar
  46. Taraschi, T. F., and Rubin, E. (1985). Biology of disease: Effects of ethanol on the chemical and structural properties of biologic membranes. Lab. Invest. 52120.Google Scholar
  47. Thomas, D. S., Hossack, J. A., and Rose, A. H. (1978). Plasma membrane lipid composition and ethanol tolerance in Saccharomyces cerivisiae. Arch. Microbiol. 117239.Google Scholar
  48. Thompson, T. E. (1978). Transmembrane compositional asymmetry of lipids in bilayers and biomembranes. In Solomon, A. K., and Karnovsky, M. (eds.), Molecular Specialization and Symmetry in Membrane Function Harvard University Press, Cambridge, Mass. pp. 78–98.Google Scholar
  49. Tsukagoshi, N., and Fox, C. F. (1973). Transport system assembly and the mobility of membrane lipids in Escherichia coli. Biochemistry 122822.Google Scholar
  50. Van Herrewege, J., and David, J. R. (1980). Alcohol tolerance and alcohol utilisation in Drosophila: Partial independence of two adaptive traits. Heredity 44229.Google Scholar
  51. Williamson, J. H., Krochko, D., and Geer, B. W. (1980). 6-Phosphogluconate dehydrogenase from Drosophila melanogaster. I. Purification and properties of the A isozyme. Biochem. Genet. 1887.Google Scholar
  52. Worchester, N. A., Bruckdorfer, K. R., Halinan, T., Wilks, A. J., and Man, J. A. (1979). The influence of diet and diabetes on stearyl coenzyme A desaturase (EC 1.14.99.5) activity and fatty acid composition in rat tissues. Br. J. Nutr. 41239.Google Scholar

Copyright information

© Plenum Publishing Corporation 1986

Authors and Affiliations

  • Billy W. Geer
    • 1
  • Stephen W. McKechnie
    • 1
  • Marilyn L. Langevin
    • 1
  1. 1.Department of BiologyKnox CollegeGalesburg

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