Skip to main content

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

Abstract

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 MAXATP is only 26.4. For growth with glucose and inorganic salts a Y MAXATP value of 28.8 was found. Addition of amino acids was without effect on Y MAXATP but addition of nucleic acid bases increased the Y MAXATP 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 MAXATP 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 MAXATP 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.

This is a preview of subscription content, access via your institution.

References

  • 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.

    PubMed  Article  CAS  Google Scholar 

  • Ackrell, B. A. C. andJones, C. W. 1971b. The respiratory system ofAzotobacter vinelandii 2. Oxygen effects. — Eur. J. Biochem.20: 29–35.

    PubMed  Article  CAS  Google Scholar 

  • Barnes, E. M., Jr. 1972. Respiration-coupled glucose transport in membrane vesicles from Azotobacter vinelandii. — Arch. Biochem. Biophys.152: 795–799.

    PubMed  Article  CAS  Google Scholar 

  • Bauchop, T. andElsden, S. R. 1960. The growth of microorganisms in relation to their energy supply. — J. Gen. Microbiol.23: 457–469.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  Article  CAS  Google Scholar 

  • Bragg, P. D., Davies, P. L. andHou, C. 1972. Function of energy-dependent transhydrogenase inEscherichia coli. — Biochem. Biophys. Res. Comm.47: 1248–1255.

    PubMed  Article  CAS  Google Scholar 

  • Chung, A. E. 1970. Pyridine nucleotide transhydrogenase fromAzotobacter vinelandii. — J. Bacteriol.102: 438–447.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Dalton, H. and Postgate, J. R. 1969. Growth and physiology ofAzotobacter chroococcum in continuous culture. — J. Gen. Microbiol.56: 307–319.

    CAS  Google Scholar 

  • Decker, K., Jungermann, K. andThauer, R. K. 1970. Energy production in anaerobic organisms. — Angew. Chem. Int. Ed.9: 138–158.

    Article  CAS  Google Scholar 

  • Forrest, W. W. andWalker, D. J. 1971. The generation and utilization of energy during growth. — Advan. Microb. Physiol.5: 213–274.

    CAS  Google Scholar 

  • Fraenkel, D. G. 1968. Selection ofEscherichia coli mutants lacking glucose-6-phosphate dehydrogenase or gluconate-6-phosphate dehydrogenase. — J. Bacteriol.95: 1267–1271.

    PubMed  CAS  Google Scholar 

  • Goldfine, H. 1972. Comparative aspects of bacterial lipids. — Advan. Microb. Physiol.8: 1–58.

    CAS  Google Scholar 

  • 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 

  • 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.

    CAS  Google Scholar 

  • Harold, F. M. 1972. Conservation and transformation of energy by bacterial membranes. — Bacteriol. Rev.36: 172–230.

    PubMed  CAS  Google Scholar 

  • Hernandez, E. andJohnson, M. J. 1967. Energy supply and cell yield in aerobically grown microorganisms. — J. Bacteriol.94: 996–1001.

    PubMed  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • Jones, C. W., Brice, J. M., Wright, V. andAckrell, B. A. C. 1973. Respiratory protection of nitrogenase inAzotobacter vinelandii. — FEBS Letters29: 77–81.

    PubMed  Article  CAS  Google Scholar 

  • Kaback, H. R. 1970. Transport. — Annu. Rev. Biochem.39: 561–598.

    PubMed  Article  CAS  Google Scholar 

  • Kaback, H. R. 1972. Transport across isolated bacterial cytoplasmic membranes. — Biochim. Biophys. Acta265: 367–416.

    PubMed  CAS  Google Scholar 

  • Kapralek, F. 1972. The physiological role of tetrathionate respiration in growingCitrobacter. — J. Gen. Microbiol.71: 133–139.

    PubMed  CAS  Google Scholar 

  • Keister, D. L. andHemmes, R. B. 1966. Pyridine nucleotide transhydrogenase fromChromatium. — J. Biol. Chem.241: 2820–2825.

    PubMed  CAS  Google Scholar 

  • Lengyel, P. andSöll, D. 1969. Mechanism of protein biosynthesis. — Bacteriol. Rev.33: 264–301.

    PubMed  CAS  Google Scholar 

  • Lucas-Lenard, J. andLipmann, F. 1971. Protein biosynthesis. — Annu. Rev. Biochem.40: 409–448.

    PubMed  Article  CAS  Google Scholar 

  • McGill, D. J. andDawes, E. A. 1971. Glucose and fructose metabolism inZymomonas anaerobia. — Biochem. J.125: 1059–1068.

    PubMed  CAS  Google Scholar 

  • 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 

  • Mahler, H. R. andCordes, E. H. 1966. Biological chemistry, p. 872. — Harper and Row, New York.

    Google Scholar 

  • Mandelstamm, J. andMcQuillen, K. 1968. Biochemistry of bacterial growth, p. 540. — Blackwell Scientific Publications, Oxford and Edinburgh.

    Google Scholar 

  • 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 

  • Morowitz, H. J. 1968. Energy flow in biology: biological organization as a problem in thermal physics. — Academic Press, New York.

    Google Scholar 

  • Nagai, S., Nishizawa, Y. andAiba, S. 1969. Energetics of growth ofAzotobacter vinelandii in a glucose-limited chemostat culture. — J. Gen. Microbiol.59: 163–169.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  Article  CAS  Google Scholar 

  • Payne, W. J. 1970. Energy yields and growth of heterotrophs. Annu. Rev. Microbiol.24: 17–52.

    PubMed  Article  CAS  Google Scholar 

  • Pirt, S. J. 1965. The maintenance energy of bacteria in growing cultures. — Proc. Roy. Soc. London163B: 224–231.

    Google Scholar 

  • Reaveley, D. A. andBurge, R. E. 1972. Walls and membranes in bacteria. — Advan. Microb. Physiol.7: 1–81.

    CAS  Article  Google Scholar 

  • 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.

    PubMed  Article  CAS  Google Scholar 

  • 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.

    PubMed  Article  CAS  Google Scholar 

  • 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 

  • Stouthamer, A. H. andBettenhaussen, C. W. 1972. Influence of hydrogen acceptors on growth and energy production ofProteus mirabilis. — Antonie van Leeuwenhoek38: 81–90.

    PubMed  Article  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • van Uden, N. 1969. Kinetics of nutrient-limited growth. — Annu. Rev. Microbiol.23: 473–486.

    PubMed  Article  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • White, D. C. andSinclair, P. R. 1971. Branched electron-transport systems in bacteria. — Advan. Microb. Physiol.5: 173–211.

    CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Stouthamer, A.H. A theoretical study on the amount of ATP required for synthesis of microbial cell material. Antonie van Leeuwenhoek 39, 545–565 (1973). https://doi.org/10.1007/BF02578899

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02578899

Keywords

  • Inorganic Salt
  • Cell Material
  • Biomass Formation
  • Nucleic Acid Basis
  • Maintenance Coefficient