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Temperature-related kinetic differentiation of glucosephosphate isomerase alleloenzymes isolated from the blue mussel,Mytilus edulis

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Two glucosephosphate isomerase (GPI;D-glucose-6-phosphate ketolisomerase; EC alleloenzymes from the blue mussel,Mytilus edulis, were purified to homogeneity. The steady-state kinetic properties of GPI1.00 and GPI.96, which exhibit latitudinal clines in frequency along the Atlantic coast of North America, were determined in both the glycolytic and the gluconeogenic reaction directions at physiological temperatures and pH levels. The two alleloenzymes are catalytically similar at low temperatures (5–10°C), while GPI1.00 diverges to become more efficient at higher physiological temperatures (15–25°C). This pattern of differentiation is consistent with the latitudinal distributions of the alleloenzymes and is due to the greater temperature sensitivities of GPI1.00 V max /K m values of the two alleloenzymes are virtually the same over the physiological range of temperatures. The observed pattern of catalytic differentiation is similar to that seen for interspecific GPI variants.

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  1. Albery, W. J., and Knowles, J. R. (1976). Evolution of enzyme function and the development of catalytic efficiency.Biochemistry 155631.

  2. Anderson, S. M., and MacDonald, J. F. (1983). Biochemical and molecular analysis of naturally occurring Adh variants inDrosophila melanogaster.Proc. Natl. Acad. Sci. USA 804798.

  3. Anonymous (1972). Mean surface water temperature and salinity readings for the east coast of North and South America. U.S. Coastal and Geodetic Survey, Publ. 31-1, U.S. Government Printing Office, Washington, D.C.

  4. Atkins, G. L., and Nimmo, I. A. (1981). A comment on the design of experiments to estimate the Michaelis-Menten parameters of enzyme-catalyzed reactions.Experientia 37122.

  5. Atkinson, D. E. (1977).Cellular Energy Metabolism and Its Regulation Academic Press, New York.

  6. Ayala, F. J. (ed.) (1976).Molecular Evolution Sinauer Associates, Sunderland, Mass.

  7. Bayne, B. L., Thompson, R. J., and Widdows, J. (1973). Some effects of temperature and food on the rate of oxygen consumption byMytilus edulis L. In Wieser, W. (ed.),Effects of Temperature on Ectothermic Organisms Springer-Verlag, Heidelberg, pp. 181–193.

  8. Beis, I., and Newsholme, E. A. (1975). The contents of adenine nucleotides, phosphagens, and some glycolytic intermediates in resting muscles from vertebrates and invertebrates.Biochem. J. 15223.

  9. Bradford, M. M. (1976). A rapid and sensitive method for quantitation of microgram quantities of protein utilizing the principle of dye binding.Anal. Biochem. 72248.

  10. Cameselle, J. C., Sanchez, J. L., and Carrion, A. (1980). The regulation of glycolysis in the hepatopancreas of the sea musselMytilus edulis L.Comp. Biochem. Physiol. 65B95.

  11. Chemical Rubber Company (1974).Handbook of Biochemistry Chemical Rubber Company, Cleveland, Ohio.

  12. Corbin, K. W. (1977). Phosphoglucose isomerase polymorphism and natural selection in the sand crab,Emerita talpoida.Evolution 31331.

  13. Cornish-Bowden, A., and Endrenyi, L. (1981). Fitting of enzyme kinetic data without prior knowledge of weights.Biochem. J. 1931005.

  14. Currie, D. J. (1982). Estimating Michaelis-Menten parameters: Bias, variance, and experimental design.Biometrics 38907.

  15. Duggleby, R. G. (1979). Experimental designs for estimating the kinetic parameters for enzyme-catalyzed reactions.J. Theor. Biol. 81671.

  16. Dyson, J. E. D., and Noltmann, E. A. (1968). The effect of pH and temperature on the kinetic parameters of phosphoglucose isomerase: Participation of histidine and lysine in a proposed dual function mechanism.J. Biol. Chem. 2431401.

  17. Eanes, W. F. (1984). Viability interactions,in vivo activity and G6PD polymorphism inDrosophila melanogaster.Genetics 10695.

  18. Ebberink, R. H. M., and deZwaan, A. (1980). Control of glycolysis in the posterior adductor muscle of the sea musselMytilus edulis.J. Comp. Physiol. B 137165.

  19. Endrenyi, L., and Chan, F.-Y. (1981). Optimal design of experiments for the estimation of precise hyperbolic kinetic and binding parameters.J. Theor. Biol. 90241.

  20. Gabbott, P. A. (1976). Energy metabolism. In Bayne, B. L. (ed.),Marine Mussels: Their Ecology and Physiology Cambridge University Press, Cambridge, U.K., pp. 293–356.

  21. Gonzales, J., and Yevich. (1976). Responses of an estuarine population of the blue musselMytilus edulis to heated water from a steam generating plant.Mar. Biol. 34177.

  22. Hall, J. G. (1983). Ph.D. dissertation, State University of New York at Stony Brook, Stony Brook.

  23. Hall, J. G. (1985). The adaptation of enzymes to temperature: Catalytic characterization of glucosephosphate isomerase homologues isolated fromMytilus edulis andIsognomon alatus, bivalve molluscs inhabiting different thermal environments.Mol. Biol. Evol. 2251.

  24. Hall, J. G., and Koehn, R. K. (1983). The evolution of enzyme catalytic efficiency and adaptive inference from steady-state kinetic data.Evol. Biol. 1653.

  25. Hoffmann, R. J. (1981a). Evolutionary genetics ofMetridium senile. I. Kinetic differences in phosphoglucose isomerase allozymes.Biochem. Genet. 19129.

  26. Hoffmann, R. J. (1981b). Evolutionary genetics ofMetridium senile. II. Geographic patterns of allozyme variation.Biochem. Genet. 19 145.

  27. Hoffmann, R. J. (1983). Temperature modulation of the kinetics of phosphoglucose isomerase genetic variants from the sea anemoneMetridium senile.J. Exp. Zool. 227361.

  28. Hutchins, L. W. (1947). The bases for temperature zonation in geographical distribution.Ecol. Monogr. 17325.

  29. Incze, L. S., Lutz, R. A., and Watling, L. (1980). Relationships between effects of environmental temperature and seston on growth and mortality ofMytilus edulis in a temperature northern estuary.Mar. Biol. 57147.

  30. Koehn, R. K., and Williams, G. C. (1978). Genetic differentiation without isolation in the American eel,Anguilla rostrata. II. Temporal stability of geographic patterns.Evolution 32624.

  31. Koehn, R. K., Milkman, R., and Mitton, J. B. (1976). Population genetics of marine pelecypods. IV. Selection, migration and genetic differences in the blue mussel,Mytilus edulis.Evolution 302.

  32. Koehn, R. K., Zera, A. J., and Hall, J. G. (1983). Enzyme polymorphism and natural selection. In Nei, M., and Koehn, R. K. (eds.),Evolution of Genes and Proteins Sinauer Associates, Sunderland, Mass., pp. 115–236.

  33. Koehn, R. K., Hall, J. G., Innes, D. J., and Zera, A. J. (1984). Genetic differentiation ofMytilus edulis in eastern North America.Mar. Biol. 79117.

  34. Levinton, J. S., and Suchanek, T. H. (1978). Geographic variation, niche breadth and genetic differentiation at different scales in the musselsMytilus californianus andM. edulis.Mar. Biol. 49363.

  35. Lewontin, R. C. (1974).The Genetic Basis of Evolutionary Change Columbia University Press, New York.

  36. Londesborough, J. (1980). The causes of sharply bent or discontinuous Arrhenius plots for enzyme-catalyzed reactions.Eur. J. Biochem. 105211.

  37. Nei, M. (1975).Molecular Population Genetics and Evolution American Elsevier, New York.

  38. Nei, M., and Koehn, R. K. (eds.) (1983).Evolution of Genes and Proteins Sinauer Associates, Sunderland, Mass.

  39. Nevo, E. (1978). Genetic variation in natural populations: Patterns and theory.Theor. Pop. Biol. 13121.

  40. Newsholme, E. A., and Start, C. (1973).Regulation in Metabolism John Wiley and Sons, New York.

  41. Noltmann, E. A. (1972). Aldose-ketose isomerases. In Boyer, P. D. (ed.),The Enzymes, Vol. VI. Academic Press, New York, pp. 271–354.

  42. Northrup, D. B. (1983). Fitting enzyme-kinetic data to V/K.Anal. Biochem. 132457.

  43. Page, M. I. (1980). Transition states, standard states, and enzymic catalysis.Int. J. Biochem. 11331.

  44. Palumbi, S. R., Sidell, B. D., Van Beneden, R., Smith, G. D., and Powers, D. A. (1980). Glucosephosphate isomerase (GPI) of the teleostFundulus heteroclitus (Linnaeus): Isozymes, allozymes, and their physiological roles.J. Comp. Physiol. B 138 49.

  45. Place, A. R., and Powers, D. A. (1978). Genetic bases for protein polymorphism inFundulus heteroclitus (L.). I. Lactate dehydrogenase (Ldh-B), malate dehydrogenase (Mdh-A), glucosephosphate isomerase (Gpi-B), and phosphoglucomutase (Pgm-A).Biochem. Genet. 16577.

  46. Place, A. R., and Powers, D. A. (1979). Genetic variation and relative catalytic efficiences: Lactate dehydrogenase-B allozymes ofFundulus heteroclitus.Proc. Natl. Acad. Sci. USA 762354.

  47. Powers, D. A., and Place, A. R. (1978). Biochemical genetics ofFundulus heteroclitus (L.). I. Temporal and spatial variation in gene frequencies of Ldh-B, Mdh-A, Gpi-B, and Pgm-A.Biochem. Genet. 16593.

  48. Reed, K. R. H., and Cumming, K. B. (1967). Thermal tolerance of the bivalve molluscsModiolus modiolus (L.),Mytilus edulis L., andBrachidontes demissus Dillwyn.Comp. Biochem. Physiol. 22149.

  49. Reeves, R. B. (1972). An imidazole alphastat hypothesis for vertebrate acid base regulation: Tissue carbon dioxide content and body temperature in bullfrogs.Resp. Physiol. 14219.

  50. Selander, R. K. (1976). Genic variation in natural populations. In Ayala, F. J. (ed.),Molecular Evolution Sinauer Associates, Sunderland, Mass., pp. 21–45.

  51. Selwyn, M. J. (1965). A simple test for inactivation of an enzyme during assay.Biochim. Biophys. Acta 105193.

  52. Somero, G. N. (1978). Temperature adaptation of enzymes: Biological optimization through structure-function compromises.Annu. Rev. Ecol. Syst. 91.

  53. Somero, G. N. (1981). pH-temperature interactions on proteins: Principles of optimal pH and buffer system design.Mar. Biol. Lett. 2163.

  54. Tilley, W. E., Gracy, R. W., and Welch, S. G. (1974). A point mutation increasing the stability of human phosphoglucose isomerase.J. Biol. Chem. 2494571.

  55. Waley, S. G. (1981). An easy method for the determination of initial rates.Biochem. J. 1931009.

  56. Weber, K., Pringle, J. R., and Osborn, M. (1972). Measurement of molecular weights by electrophoresis on SDS-acrylamide gel. In Hirs, C. H., and Timasheff, S. N. (eds.),Methods in Enzymology, Vol. XXVI Academic Press, New York, pp. 3–27.

  57. Wells, H. W., and Gray, I. E. (1960). The seasonal occurrence ofMytilus edulis on the Carolina coast as a result of transport around Cape Hatteras.Biol. Bull. Mar. Biol. Lab. Woods Hole 119550.

  58. Widdows, J. (1976). Physiological adaptation ofMytilus edulis to cyclic temperatures.J. Comp. Physiol. 105115.

  59. Widdows, J. (1978). Combined effects of body size, food concentration and season on the physiology ofMytilus edulis.J. Mar. Biol. Assoc. U.K. 58109.

  60. Williams, G. C., Koehn, R. K., and Mitton, J. B. (1973). Differentiation without isolation in the American eel,Anguilla rostrata.Evolution 27192.

  61. Wilson, A. C., Carlson, S. S., and White, T. J. (1977). Biochemical evolution.Annul Rev. Biochem. 46573.

  62. Zera, A. J., Koehn, R. K., and Hall, J. G. (1985). Allozymes and biochemical adaptation. In Kerkut, G. A., and Gilbert, L. I. (eds.),Comprehensive Insect Physiology, Biochemistry, and Pharmacology, Vol. 10 Pergamon Press, New York, pp. 633–674.

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This research was supported by NSF Grant DEB 7908802 and USPHS Grant GM 21133 to R. K. Koehn. This is contribution 536 from the Program in Ecology and Evolution of the State University of New York, Stony Brook.

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Hall, J.G. Temperature-related kinetic differentiation of glucosephosphate isomerase alleloenzymes isolated from the blue mussel,Mytilus edulis . Biochem Genet 23, 705–728 (1985).

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Key words

  • glucosephosphate isomerase (EC
  • Mytilus edulis
  • alleloenzymes
  • enzyme kinetics
  • temperature