Antonie van Leeuwenhoek

, Volume 39, Issue 1, pp 545–565 | Cite as

A theoretical study on the amount of ATP required for synthesis of microbial cell material

  • A. H. Stouthamer


The amount of ATP required for the formation of microbial cells growing under various conditions was calculated. It was assumed that the chemical composition of the cell was the same under all these conditions. The analysis of the chemical composition of microbial cells of Morowitz (1968) was taken as a base. It was assumed that 4 moles of ATP are required for the incorporation of one mole of amino acid into protein. The amount of ATP required on account of the instability and frequent regeneration of messenger RNA was calculated from data in the literature pertaining to the relative rates of synthesis of the various classes of RNA molecules in the cell. An estimate is given of the amount of ATP required for transport processes. For this purpose it was assumed that 0.5 mole of ATP is necessary for the uptake of 1 g-ion of potassium or ammonium, and 1 mole of ATP for the uptake of 1 mole of phosphate, amino acid, acetate, malate etc. The results of the calculations show that from preformed monomers (glucose, amino acids and nucleic acid bases) 31.9 g cells can be formed per g-mole of ATP when acetyl-CoA is formed from glucose. When acetyl-CoA cannot be formed from glucose and must be formed from acetate, Y ATP MAX is only 26.4. For growth with glucose and inorganic salts a Y ATP MAX value of 28.8 was found. Addition of amino acids was without effect on Y ATP MAX but addition of nucleic acid bases increased the Y ATP MAX value to that for cells growing with preformed monomers. Under these conditions 15–20% of the total ATP required for cell formation is used for transport processes. Much lower Y ATP MAX values are found for growth with malate, lactate or acetate and inorganic salts. During growth on these substrates a greater part of the ATP required for cell formation is used for transport processes. The calculated figures are very close to the experimental values found.

The interrelations between Y ATP MAX and YATP, the specific growth rate (μ), the maintenance coefficient (me) and the P/O rate are given. From a review of the literature evidence is presented that these parameters may vary under different growth conditions. It is concluded that in previous studies on the relation between ATP production and formation of cell material these effects have unjustly been neglected.


Inorganic Salt Cell Material Biomass Formation Nucleic Acid Basis Maintenance Coefficient 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Ackrell, B. A. C. andJones, C. W. 1971a. The respiratory system ofAzotobacter vinelandii. 1. Properties of phosphorylating respiratory membranes. — Eur. J. Biochem.20: 22–28.PubMedCrossRefGoogle Scholar
  2. Ackrell, B. A. C. andJones, C. W. 1971b. The respiratory system ofAzotobacter vinelandii 2. Oxygen effects. — Eur. J. Biochem.20: 29–35.PubMedCrossRefGoogle Scholar
  3. Barnes, E. M., Jr. 1972. Respiration-coupled glucose transport in membrane vesicles from Azotobacter vinelandii. — Arch. Biochem. Biophys.152: 795–799.PubMedCrossRefGoogle Scholar
  4. Bauchop, T. andElsden, S. R. 1960. The growth of microorganisms in relation to their energy supply. — J. Gen. Microbiol.23: 457–469.PubMedGoogle Scholar
  5. Benemann, J. R., Yoch, D. C., Valentine, R. C. andArnon, D. I. 1971. The electron transport system in nitrogen fixation byAzotobacter. III. Requirements for NADPH-supported nitrogenase activity. — Biochim. Biophys. Acta226: 205–212.PubMedCrossRefGoogle Scholar
  6. Bragg, P. D., Davies, P. L. andHou, C. 1972. Function of energy-dependent transhydrogenase inEscherichia coli. — Biochem. Biophys. Res. Comm.47: 1248–1255.PubMedCrossRefGoogle Scholar
  7. Chung, A. E. 1970. Pyridine nucleotide transhydrogenase fromAzotobacter vinelandii. — J. Bacteriol.102: 438–447.PubMedGoogle Scholar
  8. Colowick, S. P., Kaplan, N. O., Neufield, E. F. andCiotti, M. M. 1952. Pyridine nucleotide transhydrogenase. I. Indirect evidence for the reaction and purification of the enzyme. — J. Biol. Chem.195: 95–106.PubMedGoogle Scholar
  9. Dalton, H. and Postgate, J. R. 1969. Growth and physiology ofAzotobacter chroococcum in continuous culture. — J. Gen. Microbiol.56: 307–319.Google Scholar
  10. Decker, K., Jungermann, K. andThauer, R. K. 1970. Energy production in anaerobic organisms. — Angew. Chem. Int. Ed.9: 138–158.CrossRefGoogle Scholar
  11. Forrest, W. W. andWalker, D. J. 1971. The generation and utilization of energy during growth. — Advan. Microb. Physiol.5: 213–274.Google Scholar
  12. Fraenkel, D. G. 1968. Selection ofEscherichia coli mutants lacking glucose-6-phosphate dehydrogenase or gluconate-6-phosphate dehydrogenase. — J. Bacteriol.95: 1267–1271.PubMedGoogle Scholar
  13. Goldfine, H. 1972. Comparative aspects of bacterial lipids. — Advan. Microb. Physiol.8: 1–58.Google Scholar
  14. Gunsalus, I. C. andShuster, C. W. 1961. Energy-yielding metabolism in bacteria, p. 1–58.In I. C. Gunsalus and R. Y. Stanier, (eds.), The Bacteria, Vol. 2. — Academic Press, New York and Londen.Google Scholar
  15. Hadjipetrou, L. P., Gerrits, J. P., Teulings, F. A. G. andStouthamer, A. H. 1964. Relation between energy production and growth ofAerobacter aerogenes. — J. Gen. Microbiol.36: 139–150.Google Scholar
  16. Harold, F. M. 1972. Conservation and transformation of energy by bacterial membranes. — Bacteriol. Rev.36: 172–230.PubMedGoogle Scholar
  17. Hernandez, E. andJohnson, M. J. 1967. Energy supply and cell yield in aerobically grown microorganisms. — J. Bacteriol.94: 996–1001.PubMedGoogle Scholar
  18. Hill, S., Drozd, J. W. andPostgate, J. R. 1972. Environmental effects on the growth of nitrogen-fixing bacteria. — J. Appl. Chem. Biotechnol.22: 541–558.Google Scholar
  19. Jones, C. W., Brice, J. M., Wright, V. andAckrell, B. A. C. 1973. Respiratory protection of nitrogenase inAzotobacter vinelandii. — FEBS Letters29: 77–81.PubMedCrossRefGoogle Scholar
  20. Kaback, H. R. 1970. Transport. — Annu. Rev. Biochem.39: 561–598.PubMedCrossRefGoogle Scholar
  21. Kaback, H. R. 1972. Transport across isolated bacterial cytoplasmic membranes. — Biochim. Biophys. Acta265: 367–416.PubMedGoogle Scholar
  22. Kapralek, F. 1972. The physiological role of tetrathionate respiration in growingCitrobacter. — J. Gen. Microbiol.71: 133–139.PubMedGoogle Scholar
  23. Keister, D. L. andHemmes, R. B. 1966. Pyridine nucleotide transhydrogenase fromChromatium. — J. Biol. Chem.241: 2820–2825.PubMedGoogle Scholar
  24. Lengyel, P. andSöll, D. 1969. Mechanism of protein biosynthesis. — Bacteriol. Rev.33: 264–301.PubMedGoogle Scholar
  25. Lucas-Lenard, J. andLipmann, F. 1971. Protein biosynthesis. — Annu. Rev. Biochem.40: 409–448.PubMedCrossRefGoogle Scholar
  26. McGill, D. J. andDawes, E. A. 1971. Glucose and fructose metabolism inZymomonas anaerobia. — Biochem. J.125: 1059–1068.PubMedGoogle Scholar
  27. McKechnie, I. andDawes, E. A. 1969. An evaluation of the pathways of metabolism of glucose, gluconate and 2-oxogluconate byPseudomonas aeruginosa by measurement of molar growth yields. — J. Gen. Microbiol.55: 341–349.Google Scholar
  28. Mahler, H. R. andCordes, E. H. 1966. Biological chemistry, p. 872. — Harper and Row, New York.Google Scholar
  29. Mandelstamm, J. andMcQuillen, K. 1968. Biochemistry of bacterial growth, p. 540. — Blackwell Scientific Publications, Oxford and Edinburgh.Google Scholar
  30. Mitchell, P. 1970. Membrane of cells and organelles: Morphology, transport and metabolism, p. 121–166.In Organization and control in procaryotic and eucaryotic cells, Symp. Soc. Gen. Microbiol., 20th. — Cambridge University Press, London.Google Scholar
  31. Morowitz, H. J. 1968. Energy flow in biology: biological organization as a problem in thermal physics. — Academic Press, New York.Google Scholar
  32. Nagai, S., Nishizawa, Y. andAiba, S. 1969. Energetics of growth ofAzotobacter vinelandii in a glucose-limited chemostat culture. — J. Gen. Microbiol.59: 163–169.PubMedGoogle Scholar
  33. Norris, T. E. andKoch, A. L. 1972. Effect of growth rate on the relative rates of synthesis of messenger, ribosomal and transfer RNA inEscherichia coli. — J. Mol. Biol.64: 633–649.PubMedCrossRefGoogle Scholar
  34. Payne, W. J. 1970. Energy yields and growth of heterotrophs. Annu. Rev. Microbiol.24: 17–52.PubMedCrossRefGoogle Scholar
  35. Pirt, S. J. 1965. The maintenance energy of bacteria in growing cultures. — Proc. Roy. Soc. London163B: 224–231.Google Scholar
  36. Reaveley, D. A. andBurge, R. E. 1972. Walls and membranes in bacteria. — Advan. Microb. Physiol.7: 1–81.CrossRefGoogle Scholar
  37. Schairer, H. U. andHaddock, B. A. 1972. β-Galactoside accumulation in a Mg2+-, Ca2+-activated ATPase deficient mutant ofE. coli. — Biochem. Biophys. Res. Comm.48: 544–551.PubMedCrossRefGoogle Scholar
  38. Simoni, R. D. andShallenberger, M. K. 1972. Coupling of energy to active transport of amino acids inEscherichia coli. — Proc. Nat. Acad. Sci.69: 2663–2667.PubMedCrossRefGoogle Scholar
  39. Stouthamer, A. H. 1969. Determination and significance of molar growth yields, p. 629–663.In J. R. Norris and D. W. Ribbons, (eds.), Methods in microbiology, Vol. 1. — Academic Press, New York and London.Google Scholar
  40. Stouthamer, A. H. andBettenhaussen, C. W. 1972. Influence of hydrogen acceptors on growth and energy production ofProteus mirabilis. — Antonie van Leeuwenhoek38: 81–90.PubMedCrossRefGoogle Scholar
  41. Stouthamer, A. H. andBettenhaussen, C. 1973. Utilization of energy for growth and maintenance in continuous and batch cultures of microorganisms. A reevaluation of the method for the determination of ATP production by measuring molar growth yields. — Biochim. Biophys. Acta301: 53–70.PubMedGoogle Scholar
  42. Tempest, D. W., Dicks, J. W. andHunter, J. R. 1966. The interrelationship between potassium, magnesium and phosphorus in potassium-limited chemostat cultures ofAerobacter aerogenes. — J. Gen. Microbiol.45: 135–146.Google Scholar
  43. van Uden, N. 1969. Kinetics of nutrient-limited growth. — Annu. Rev. Microbiol.23: 473–486.PubMedCrossRefGoogle Scholar
  44. de Vries, W., Kapteijn, W. M. C., van der Beek, E. G. andStouthamer, A. H. 1970. Molar growth yields and fermentation balances ofLactobacillus casei L3 in batch cultures and in continuous cultures. — J. Gen. Microbiol.63: 333–345.PubMedGoogle Scholar
  45. White, D. C. andSinclair, P. R. 1971. Branched electron-transport systems in bacteria. — Advan. Microb. Physiol.5: 173–211.Google Scholar

Copyright information

© H. Veenman & Zonen B.V. 1973

Authors and Affiliations

  • A. H. Stouthamer
    • 1
  1. 1.Biological LaboratoryFree UniversityAmsterdamthe Netherlands

Personalised recommendations