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

Anaerobiosis and acid-base status in marine invertebrates: a theoretical analysis of proton generation by anaerobic metabolism

  • 121 Accesses

  • 51 Citations


In animals, various organic acids are accumulated during hypoxia or anoxia as products of anaerobic energy metabolism. The diversity of such acids is largest in marine invertebrates where succinate, propionate, acetate, lactate, alanine, octopine, strombine, and alanopine, are produced mainly from glycogen and aspartate. The effect of these substances on the acid-base status was assessed by a theoretical analysis of the respective metabolic pathways. This resulted in a general rule which was applied to evaluate the proton balance of the reactions in energy metabolism: net changes in the number of carboxyl groups or changes in the degree of dissociation of other groups (e.g. phosphate or ammonia) determine the net amount of H+ ions released or bound by the substrates and the metabolic end products.

For marine invertebrates the results of the analysis can be summarized as follows: In glycogenolysis one mol of protons per mol of end products is released during cytosolic glycolysis, independent of the type of metabolic end product (lactate, octopine, alanopine, strombine, or alanine). The same applies for mitochondrial production of propionate and acetate, whereas formation of succinate results in dissociation of two mol H+ per mol. Fermentation of aspartate, however, diminishes the amount of protons which is produced in the succinate-propionate pathway. Net metabolisation of Mg ATP2− yields extra protons, whereas the cleavage of phosphagens (e.g. creatine phosphate, arginine phosphate) consumes protons.

Additionally the break-down of energy-rich phosphates to inorganic phosphate has to be taken into account because of the shift of the intracellular buffer curve caused by changes of the respective effective pK values.

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


  1. Aragon J, Lowenstein JM (1980) The purin-nucleotide cycle. Eur J Biochem 110:371–377

  2. Atkinson DE (1968) The energy charge of the adenylate pool as a regulatory parameter. Interaction with feedback modifiers. Biochemistry 7:4030–4034

  3. Atkinson DE, Walton GM (1967) Adenosine triphosphate conservation in metabolic regulation. J Biol Chem 242:3239–3241

  4. Barrow KD, Jamieson DD, Norton RS (1980)31P nuclearmagnetic-resonance studies of energy metabolism in tissue from the marine invertebrateTapes watlingi. Eur J Biochem 103:289–297

  5. Beis J, Newsholme EA (1975) The contents of adenine nucleotides, phosphagens and some glycolytic intermediates in resting muscles from vertebrates and invertebrates. Biochem J 152:23–32

  6. Boyer PD, Chance B, Ernster L, Mitchell P, Racker E, Slater EC (1977) Oxidative phosphorylation and photophosphorylation. Annu Rev Biochem 46:955–1026

  7. Burt CT, Glonek T, Barany M (1976) Analysis of phosphate metabolites, the intracellular pH, and the state of adenosine triphosphate in intact muscle by phosphorus nuclear magnetic resonance. J Biol Chem 251:2584–2591

  8. Burton RF (1980) Adenosine triphosphate as determinant of magnesium levels in cytoplasm. Comp Biochem Physiol 65A:1–4

  9. Cameron JN (1981) Acid-base responses to changes in CO2 in two pacific crabs: the coconut crab,Birgus latro and a mangrove crab,Cardiosoma carnifex. J Exp Zool 218:65–73

  10. Cohen SM, Burt CT (1977)31P nuclear magnetic relaxation studies of phosphocreatine in intact muscle: Determination of intracellular free magnesium. Proc Natl Acad Sci USA 74:4271–4275

  11. Cooper TG, Tchen TT, Wood HG, Benedict CR (1968) The carboxylation of phosphoenolpyruvate and pyruvate. I. The active species of ‘CO2’ utilization by phosphoenolpyruvate carboxykinase, carboxytransphosphorylase and pyruvate carboxylase. J Biol Chem 243:3857–3863

  12. Curtin NA, Woledge RC (1978) Energy changes and muscular contraction. Physiol Rev 58:690–761

  13. Dawson MJ, Gadian DG, Wilkie DR (1977) Contraction and recovery of living muscles studied by31P nuclear magnetic resonance. J Physiol (Lond) 267:703–735

  14. Dawson MJ, Gadian DG, Wilkie DR (1978) Muscular fatigue investigated by phosphorus nuclear magnetic resonance. Nature 274:861–866

  15. Dawson MJ, Gadian DG, Wilkie DR (1980) Mechanical relaxation rate and metabolism studied in fatiguing muscle by phosphorus nuclear magnetic resonance. J Physiol (Lond) 299:465–484

  16. Ebberink RHM, de Zwaan A (1980) Control of glycolysis in the posterior adductor muscle of the sea musselMytilus edulis. J Comp Physiol 137:165–171

  17. Ellington WR (1983a) The extent of intracellular acidification during anoxia in the catch muscles of two bivalve molluscs. J Exp Zool 227:313–327

  18. Ellington WR (1983b) Phosphorus nuclear magnetic resonance studies of energy metabolism in molluscan tissues: Effect of anoxia and ischemia on the intracellular pH and high energy phosphates in the ventricle of the whelk,Busycon contrarium. J Comp Physiol 153:159–166

  19. Gevers W (1977) Generation of protons by metabolic processes in heart cells. J Mol Cell Cardiol 9:867–874

  20. Gevers W (1979) Reply to Wilkie, D.R.: Generation of protons by metabolic processes other than glycolysis in muscle cells: a critical view. J Mol Cell Cardiol 11:328–330

  21. Grieshaber MK (1982) Metabolic regulation of energy metabolism. In: Addink ADF, Spronk N (eds) Exogenous and endogenous influences on metabolic and neural control. Pergamon Press, Oxford New York, pp 225–242

  22. Heisler N (1975) Intracellular pH of isolated rat diaphragm muscle with metabolic and respiratory changes of extracellular pH. Respir Physiol 23:243–255

  23. Heisler N (1980) Regulation of the acid-base status in fishes. In: Ali MA (ed) Environmental physiology of fishes. Plenum Press, New York, pp 123–162

  24. Heisler N, Piiper J (1971) The buffer value of rat diaphragm muscle tissue determined by\(P_{CO_2 } \) equilibration of homogenates. Respir Physiol 12:169–178

  25. Hochachka PW (1980) Living without oxygen: Closed and open systems in hypoxia tolerance. Harvard Univ Press, Cambridge, Mass

  26. Hochachka PW, Fields JHA, Mommsen TP (1983) Metabolic and enzyme regulation during rest-to-work transition: a mammal versus mollusc comparison. In: Hochachka PW (ed) Metabolic biochemistry and molecular biomechanics, (The Mollusca vol 1). Academic Press, New York London, pp 55–89

  27. Hochachka PW, Mommsen TP (1983) Protons and anaerobiosis. Science 219:1391–1398

  28. Hoult DJ, Busby SJW, Gadian DG, Radda GK, Richards RE, Seeley PJ (1974) Observation of tissue metabolites using31P nuclear magnetic resonance. Nature 252:285–287

  29. Krebs HA, Woods HF, Alberti KGMM (1975) Hyperlactataemia and lactic acidosis. Essays Med Biochem 1:81–103

  30. Lipmann F, Meyerhof O (1930) Über die Reaktionsänderung des tätigen Muskels. Biochem Z 227:84–109

  31. 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 257–274

  32. Meyerhof O, Lohmann K (1926) Über die Vorgänge bei der Muskelermüdung. Biochem Z 168:128–165

  33. Meyerhof O, Lohmann K (1928) Über die natürlichen Guanidinophosphorsäuren (Phosphagene) in der quergestreiften Muskulatur. II. Die physikalisch-chemischen Eigenschaften der Guanidinophosphorsäuren. Biochem Z 196:49–72

  34. Needham DM (1971) Machina carnis. The biochemistry of muscular contraction in its historical development. Cambridge University Press, Cambridge

  35. Netter H (1959) Theoretische Biochemie. Physikalisch-chemische Grundlagen der Lebensvorgänge. Springer, Berlin Heidelberg New York

  36. Newsholme EA, Beis J, Leech AR, Zammit VA (1978) The role of creatine kinase and arginine kinase in muscle. Biochem J 172:533–537

  37. Phillips RC, Eisenberg P, George P, Rutmann RJ (1965) Thermodynamic data for the secondary phosphate ionizations of adenosine, guanosine, inosine, cytidine and uridine nucleotides and triphosphate. J Biol Chem 240:4393–4397

  38. Phillips RC, George P, Rutman RJ (1966) Thermodynamic studies of the formation and ionization of the magnesium (II) complexes of ADP and ATP over the pH range 5 to 9. J Am Chem Soc 88:2631–2640

  39. Pörtner HO (1982) Biochemische und physiologische Anpassungen an das Leben im marinen Sediment: Untersuchungen am SpritzwurmSipunculus nudus L. Dissertation, Universität Düsseldorf

  40. Pörtner HO, Grieshaber MK, Heisler N (1984a) Anaerobiosis and acid-base status in marine invertebrates: Effect of environmental hypoxia on extracellular and intracellular pH inSipunculus nudus L. J Comp Physiol B 155:13–20

  41. Pörtner HO, Kreutzer U, Siegmund B, Heisler N, Grieshaber MK (1984b) Metabolic adaptation of the intertidal wormSipunculus nudus L. to functional and environmental hypoxia. Mar Biol 79:237–247

  42. Roos A, Boron WF (1978) Intracellular pH transients in rat diaphragm muscle measured with DMO. Am J Physiol 235:C49-C54

  43. Sahlin K, Edström L, Sjöholm H, Hultman E (1981) Effects of lactic acid accumulation and ATP decrease on muscle tension and relaxation. Am J Physiol 240:C121-C126

  44. Schöttler U (1980) Der Energiestoffwechsel bei biotopbedingter Anaerobiose: Untersuchungen an Anneliden. Verh Dtsch Zool Ges 1980:228–240

  45. Schöttler U, Wienhausen G (1981) The importance of the phosphoenolpyruvate carboxykinase in the anaerobic metabolism of two marine polychaetes. In vivo investigations onNereis virens andArenicola marina. Comp Biochem Physiol 68B:41–48

  46. Schroff G, Schöttler U (1977) Anaerobic reduction of fumarate in the body wall musculature ofArenicola marina (Polychaeta). J Comp Physiol 116:325–336

  47. Schroff G, Zebe E (1980) The anaerobic formation of propionic acid in the mitochondria of the lugwormArenicola marina. J Comp Physiol 138:35–41

  48. Schulz TKF, Kluytmans JH (1983) Pathway of propionate synthesis in the sea musselMytilus edulis L. Comp Biochem Physiol 75B:365–372

  49. Smith RM, Martell AE (1975) Critical stability constants, vol 2: Amines. Plenum Press, New York London

  50. Sober HA (ed) (1973) Handbook of biochemistry. Selected data for molecular biology. CRC Press, Cleveland Ohio

  51. Veloso D, Guynn RW, Oskarsson M, Veech RL (1973) The concentrations of free and bound magnesium in rat tissues. Relative constancy of free Mg2+ concentrations. J Biol Chem 248:4811–4819

  52. Wienhausen G (1981) Anaerobic formation of acetate in the lugwormArenicola marina. Naturwissenschaften 68:206

  53. Wilkie DR (1979) Generation of protons by metabolic processes other than glycolysis in muscle cells: a critical view. J Mol Cell Cardiol 11:325–330

  54. Wilson DR, Nishiki K, Erecinska M (1981) Energy metabolism in muscle and its regulation during individual contraction-relaxation cycles. Trends Biochem Sci 6:16–19

  55. Zammit VA (1978) Possible relationship between energy metabolism of muscle and oxygen binding characteristics of haemocyanin of cephalopods. J Mar Biol Ass UK 58:421–424

  56. Zandee DJ, Holwerda DA, de Zwaan A (1980) Energy metabolism in bivalves and cephalopods. In: Gilles R (ed) Animals and environmental fitness, vol 1. Pergamon Press, Oxford New York, pp 185–206

  57. Zebe E, Grieshaber MK, Schöttler U (1980) Biotopbedingte und funktionsbedingte Anaerobiose. Der Energiestoffwechsel wirbelloser Tiere bei Sauerstoffmangel. Biologie in unserer Zeit 10:175–182

  58. Zilva JF (1978) The origin of the acidosis in hyperlactataemia. Ann Clin Biochem 15:40–43

  59. 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

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

  61. Zwaan A de, de Bont AMT, Hemelraad J (1983) The role of phosphoenolpyruvate carboxykinase in the anaerobic metabolism of the sea musselMytilus edulis L. J Comp Physiol 153:267–274

Download references

Author information

Correspondence to H. O. Pörtner.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Pörtner, H.O., Heisler, N. & Grieshaber, M.K. Anaerobiosis and acid-base status in marine invertebrates: a theoretical analysis of proton generation by anaerobic metabolism. J Comp Physiol B 155, 1–12 (1984). https://doi.org/10.1007/BF00688785

Download citation


  • Marine Invertebrate
  • Creatine Phosphate
  • Octopine
  • Intracellular Buffer
  • Proton Generation