Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

The role of phosphoenolpyruvate carboxykinase in the anaerobic metabolism of the sea musselMytilus edulis L.

  • 54 Accesses

  • 27 Citations


The importance of PEP-carboxykinase and the utilization of aspartate in the anaerobic formation of succinate in the sea mussel was investigated in in vivo experiments by applying the metabolic inhibitors 3-mercaptopicolinate and aminooxyacetate, inhibitors of PEP-carboxykinase and transaminases, respectively. The posterior adductor muscle was analyzed separately from the remainder of the soft body (Rest). The following results were obtained:

  1. 1.

    In winter, succinate formation in the adductor muscle could be blocked by aminooxyacetate, whereas 3-mercaptopicolinate displayed no effect. This was studied for the 6 h following the onset of aerial exposure and for the period 12–18 h. In contrast, both inhibitors reduced the formation of succinate in the Rest. Therefore in adductor muscle all carbon for succinate formation must have been derived from aspartate, whereas for the Rest both aspartate and carbohydrate utilization (via PEP-carboxykinase) must have been involved. In summer, however, for adductor muscle a reduction of succinate formation and an increased aspartate utilization was observed after application of 3-mercaptopicolinate. The involvement of PEP-carboxykinase in the anaerobic formation of succinate in the adductor muscle appears therefore to be depending on the season.

  2. 2.

    In the adductor muscle extra strombine and octopine were formed when aspartate utilization was blocked by aminooxyacetate. In the Rest opines were no important end products.

  3. 3.

    Forced shell valve closure resulted, when compared to normal aerial exposure, in an increased utilization of aspartate and an increased accumulation of alanine and succinate. Only in the groups subjected to forced valve closure strombine, and to a lesser extent octopine, appeared to accumulate in substantial quantities. When anaerobiosis progresses, the rate at which the concentration changes of aspartate, alanine and succinate occur declines, but not that of strombine formation.

  4. 4.

    For the adductor muscle the decrease in aspartate exceeded the increase in succinate. The opposite was true for the Rest. In the adductor muscle only part of the utilized aspartate is used for succinate formation, whilst the other part in converted via transaminations and a decarboxylation into alanine according to the overall reaction aspartate →CO2+alanine. It is suggested that the latter conversion may be involved in anaerobic hydrogen transport across the mitochondrial inner membrane.

This is a preview of subscription content, log in to check access.





ethylenediamine tetraacetic acid


glutamate-oxaloacetate transaminase


glutamate-pyruvate transaminase


malate dehydrogenase




  1. Addink ADF, Veenhof PR (1975) Regulation of mitochondrial matrix enzymes inMytilus edulis L. Proc 9th Eur Mar Biol Symp, pp 109–119

  2. Bergmeyer HU, Bernt E (1974a) Glutamate-pyruvate transaminase. In: Bergmeyer HU (ed) Methods of enzymatic analysis. Academic Press, New York London, pp 752–758

  3. Bergmeyer HU, Bernt E (1974b) Glutamate-oxaloacetate transaminase. In: Bergmeyer HU (ed) Methods of enzymatic analysis. Academic Press, New York London, pp 727–733

  4. Collicutt JM (1975) Anaerobic metabolism in oyster heart. M Sc thesis. University of British Columbia,

  5. Collicutt JM, Hochachka PW (1977) The anaerobic oyster heart: compling of glucose and aspartate fermentation. J Comp Physiol 115:147–157

  6. Ebberink RHM, Zwaan A de (1980) Control of glycolysis in the posterior adductor muscle of the sea musselMytilus edulis. J Comp Physiol 137:165–172

  7. Ebberink RHM, Zurburg W, Zandee DI (1979) The energy demand of the posterior adductor muscle ofMytilus edulis in catch during exposure to air. Mar Biol Lett 1:21–23

  8. Fields JHA (1976) A dehydrogenase requiring alanine and pyruvate as substrates from the oyster adductor muscle. Fed Proc 37:1687

  9. Holwerda DA, Zwaan A de (1980) On the role of fumarate reductase in anaerobic carbohydrate catabolism ofMytilus edulis L. Comp Biochem Physiol [B] 67:447–453

  10. Hochachka PW, Mustafa T (1972) Invertebrate facultative anaerobiosis. Science 178:1056–1060

  11. Hochachka PW, Mustafa T (1973) Enzymes in facultative anaerobiosis of molluscs. I. Malic enzymes of oyster adductor muscle. Comp Biochem Physiol [B] 45:625–637

  12. Kaziro Y (1969) Crystalline propionyl-CoA carboxylase from pig heart. In: Lowenstein JM (ed) Methods of enzymology, vol 13. Academic Press, New York London, pp 182–190

  13. Livingstone DR (1982) Energy production in the muscle tissues of different kinds of molluscs. In: Addink ADF, Spronk N (eds) Exogenous and endogenous influences on metabolic and neural control. Pergamon Press, Oxford New York, pp 257–273

  14. Lehninger AL (1976) Biochemistry, Worth, New York, p 535

  15. Pamatmat MM (1980) Facultative anaerobiosis of benthos. In: Tenore KR, Coull BC (eds) Marine benthic dynamics. The Belle W. Baruch Library in Marine Science, no 11 University of Carolina Press, pp 69–90

  16. Schöttler U (1979) On the anaerobic metabolism of three species ofNereis (Annelids). Mar Biol Prog Ser 1:249–254

  17. Schöttler U, Wienhausen G (1981) The importance of the phosphoenolpyruvate carboxykinase in the anaerobic metabolism of two marine polychaetes. Comp Biochem Physiol [B] 68:41–48

  18. Utter MF, Kurahashi K (1954) Mechanism of action of oxaloacetic carboxylase. J Biol Chem 207:821–841

  19. Zandee DI, Kluytmans JH, Zurburg W, Pieters H (1980) Seasonal variations in biochemical composition ofMytilus edulis with reference to energy metabolism and gametogenesis. Neth J Sea Res 14:1–29

  20. Zebe E, Salge U, Wiemann C, Wilps H (1981) The energy metabolism of the leechHirudo medicinalis in anoxia and muscular work. J Exp Zool 218:157–163

  21. Zurburg W, Ebberink RHM (1981) The anaerobic energy demand ofMytilus edulis. Organ specific differences in ATP-supplying processes and metabolic routes. Mol Physiol 1:153–164

  22. Zurburg W, Bont AMT de, Zwaan A de (1982) Recovery from exposure to air and the occurrence of strombine in different organs of the sea musselMytilus edulis. Mol Physiol 2:135–147

  23. Zwaan A de, Wijsman TCM (1976) Anaerobic metabolism in bivalvia (Mollusca). Comp Biochem Physiol [B] 54:313–324

  24. Zwaan A de, Zurburg W (1981) The formation of strombine in the adductor muscle of the sea musselMytilus edulis L. Mar Biol Lett. 2:179–192

  25. Zwaan A de, Holwerda DA, Veenhof PR (1981) Anaerobic malate metabolism in mitochondria of the sea musselMytilus edulis L. Mar Biol Lett 2:131–140

  26. Zwaan A de, Bont AMT de, Verhoeven A (1982) Anaerobic energy metabolism in isolated adductor muscle of the sea musselMytilus edulis L. J Comp Physiol 149:137–143

  27. Zwaan A de, Bont AMT de, Zurburg W, Bayne BL, Livingstone DR (1983) On the role of strombine formation in the energy metabolism of adductor muscle of a sessile bivalve. J Comp Physiol 149:557–563

Download references

Author information

Rights and permissions

Reprints and Permissions

About this article

Cite this article

de Zwaan, A., de Bont, A.M.T. & Hemelraard, J. The role of phosphoenolpyruvate carboxykinase in the anaerobic metabolism of the sea musselMytilus edulis L.. J Comp Physiol B 153, 267–274 (1983). https://doi.org/10.1007/BF00689630

Download citation


  • Adductor Muscle
  • Succinate
  • Aerial Exposure
  • Valve Closure
  • Phosphoenolpyruvate Carboxykinase