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Table of Contents
Vol. 13, No. 1-3, 2007
Issue release date: August 2007
Section title: Review
Free Access
J Mol Microbiol Biotechnol 2007;13:1–11
(DOI:10.1159/000103591)

The Energy Spilling Reactions of Bacteria and Other Organisms

Russell J.B.
US Plant, Soil and Nutrition Laboratory, Agricultural Research Service, USDA, Ithaca, N.Y., USA
email Corresponding Author

Abstract

For many years it was assumed that living organisms always utilized ATP in a highly efficient manner, but simple growth studies with bacteria indicated that the efficiency of biomass production was often at least 3-fold lower than the amount that would be predicted from standard biosynthetic pathways. The utilization of energy for maintenance could only explain a small portion of this discrepancy particularly when the growth rate was high. These ideas and thermodynamic arguments indicated that cells might have another avenue of energy utilization. This phenomenon has also been called ‘uncoupling’, ‘spillage’ and ‘overflow metabolism’, but ‘energy spilling’ is probably the most descriptive term. It appears that many bacteria spill energy, and the few that do not can be killed (large and often rapid decrease in viability), if the growth medium is nitrogen-limited and the energy source is in ‘excess’. The lactic acid bacterium, Streptococcus bovis, is an ideal bacterium for the study of energy spilling. Because it only uses substrate level phosphorylation to generate ATP, ATP generation can be calculated with a high degree of certainty. It does not store glucose as glycogen, and its cell membrane can be easily accessed. Comparative analysis of heat production, membrane voltage, ATP production and Ohm’s law indicated that the energy spilling reaction of S. bovis is mediated by a futile cycle of protons through the cell membrane. Less is known about Escherichia coli, but in this bacterium energy spilling could be mediated by a futile cycle of potassium or ammonium ions. Energy spilling is not restricted to prokaryotes and appears to occur in yeasts and in higher organisms. In man, energy spilling may be related to cancer, ageing, ischemia and cardiac failure.

© 2007 S. Karger AG, Basel


  

Key Words

  • Energy spilling
  • Uncoupling
  • Growth yield
  • Futile cycles

References

  1. Bauchop T, Elsden SR: The growth of microorganisms in relation to their energy supply.J Gen Microbiol 1960;23:457–469.
  2. Berman MC: Slippage and uncoupling in P-type cation pumps: implications for energy transduction mechanisms and regulation of metabolism. Biochim Biophys Acta2001;1503:329–340.
  3. Blaut M, Muller V, Gottschalk G: Energetics of Methanogens; in Krulwich T (ed): Bacterial Energetics. New York, Academic Press, 1990, pp 505–537.
  4. Bond DR, Russell JB: A role for fructose 1,6-diphosphate in the ATPase-mediated energy-spilling reaction of Streptococcus bovis. Appl Environ Microbiol 1996;62:2095–2099.
  5. Bond DR, Russell JB: Relationship between intracellular phosphate, proton motive force, and the rate of non-growth energy dissipation (energy spilling) in Streptococcus bovis JB1. Appl Environ Microbiol 1998;64:976–981.
  6. Bond DR, Russell JB: Proton motive force regulates the membrane conductance of Streptococcus bovis in a non-ohmic fashion. Microbiology 2000;146:687–694.
  7. Brand MD, Chien L-F, Ainscow EK, Rolfe DFS, Porter RK: The causes and functions of mitochondrial proton leak. Biochim Biophys Acta 1994;1187:132–139.
  8. Brock TD, Madigan JL: Biology of Microorganisms, ed 6, p 112. Englewood Cliffs, Prentice Hall, 1991.
  9. Buurman ET, Teixeira De Mattos MJ, Neijssel OM: Futile cycling of ammonium ions via the high affinity potassium uptake system (Kdp) of Escherichia coli. Arch Microbiol 1991;155:391–395.
  10. Buurman ET, Pennock J, Tempest DW, Teixeira De Mattos MJ, Neijssel OM: Replacement of potassium ions by ammonium ions in different micro-organisms grown in potassium-limited chemostat culture.Arch Microbiol 1989;152:58–63.
  11. Cook GM, Ye JJ, Russell JB, Saier MH: Properties of two sugar phosphate phosphatases from Streptococcus bovis and their involvement in inducer explusion. J Bacteriol 1995;177:7007–7009.
  12. Cooper RA, Anderson A: The formation and catabolism of methylglyoxal during glycolysis in Escherichia coli. FEBS Lett 1970;11:273–276.
  13. Cooper S: The origins and meaning of the Schaechter-Maaloe-Kjeldgaard experiments. J Gen Microbiol1993;139:1117–1124.
  14. Cot M, Loret MO, Francois J, Benbadis L: Physiological behaviour of Saccharomyces cerevisiae in aerated fed-batch fermentation for high level production of bioethanol. Biotechnol Bioeng 2001;75:345–354.
  15. Dimroth P: Sodium ion transport decarboxylases and otheraspects of sodium cycling in bacteria. Microbiol Rev 1987;51:320–340.
  16. Dlaskova A, Spacek T, Skobisova E, Santorova J, Jezek P: Certain aspects of uncoupling due to mitochondrial uncoupling proteins in vitro and in vivo. Biochim Biophys Acta 2006;1757:467–473.
  17. Feniouk BA, Mulkidjanian AY, Junge W: Proton slip in the ATP synthase of Rhodobacter capsulatus: induction, proton conduction, and nucleotide dependence. Biochim Biophys Acta 2005;1706:1184–1194.
  18. Ferguson GPT, Totemeyer S, MacLean MJ, Booth IR: Methylglyoxal production in bacteria: Suicide or survival? Arch Microbiol 1998;170:209–218.
  19. Fillingame RH, Dmitriev OY: Structural model of the transmembrane Fo rotary sector of H+-transporting ATP synthase derived by solution NMR and intersubunit cross-linking in situ. Biochim Biophys Acta 2002;1565:232–245.
  20. Flythe MD, Russell JB: The ability of acidic pH, growth inhibitors and glucose to increase the protonmotive force and energy spilling of amino acid fermenting Clostridium sporogenes MD1 cultures. Arch Microbiol 2005;183:236–242.
  21. Flythe MD, Russell JB: Fermentation acids inhibit amino acid deamination by Clostridium sporogenes MD1 via a mechanism involving a decline in intracellular glutamate rather than protonmotive force. Microbiology 2006;152:2619–2624.
  22. Flythe MD, Russell JB: The effect of acidic pH on the ability of Clostridium sporogenes MD1 to take up and retain intracellular potassium. FEMS Lett 2006;267:46–50.
  23. Garber K: News. J Natl Cancer Inst 2004;96:1805–1806.
  24. Gottschalk G: Bacterial Metabolism, ed 2. New York, Springer, 1986.
  25. Harold FM: The Vital Force: A Study of Bioenergetics. San Francisco, Freeman, 1986.
  26. Harold FM, Van Brunt J: Circulation of H+ and K+ across the plasma membrane is not obligatory for bacterial growth. Science 1977;197:372–373.
  27. Herbert D, Elsworth R, Telling RC: The continuous culture of bacteria: a theoretical and experimental study. J Gen Microbiol 1956;14:601–622.
  28. Hinkle PC, Kumar MA, Resetar A, Harris DL: Mechanistic stoichiometry of mitochondrial oxidative phosphorylation. Biochem 1991;30:3576–3582.
  29. Hungate R.E.: The rumen and its microbes, p. 282. 1966. Academic Press, New York, N.Y.
  30. Jay JM: Modern Food Microbiology, ed 4. New York, Van Nostrand Reinhold, 1989.
  31. Kleiber M: Davis, Memorial Book Department of Animal Science, University of California, 1976. http://animalscience.ucdavis.edu/memorial/kleiber.htm
  32. Klotz IM: Energy Changes in Biochemical Reactions. New York, Academic Press, 1967.
  33. Lehninger AL: Biochemistry, New York, Worth Publishers, 1975, p 12.
  34. Lehninger AL, Nelson DL, Cox MM: Principles of Biochemistry. New York, Worth Publishers, 1993, p 6.
  35. Lipmann F: Metabolic generation and utilization of phosphate bond energy. Adv Enzymol 1941;1:99–162.
  36. Liu JS, Marison IW, Von Stockar U: Microbial growth by a net heat up-take: a calorimetric and thermodynamic study on acetotrophic methanogenesis by Methanosarcina barkeri. Biotechnol Bioeng 2001;275:170–180.

    External Resources

  37. Lodge-Ivey SL, May T, Petersen MK, Strickland JR: Determination of methylglyoxal in ruminal fluid by high-performance liquid chromatography using fluorometric detection. J Agric Food Chem 2004;52:6875–6878.
  38. Maglione G, Russell JB: The adverse effect of nitrogen limitation and excess-cellobiose on Fibrobacter succinogenes. Appl Microbiol Biotechnol 1997;48:720–725.
  39. Maglione G, Russell JB, Wilson DB: Kinetics of cellulose digestion by Fibrobacter succinogenes S85. Appl Environ Microbiol 1997;63:665–669.
  40. Maloney PC: Microbes and membrane biology. FEMS Microbiol Rev 1990;87:91–102.
  41. Marr AG, Nilson EH, J CD: The maintenance requirement of Escherichia coli. Ann NY Acad Sci 1962;102:536–548.

    External Resources

  42. Mitchell P: Coupling of phosphorylation to electron and hydrogen transfer by a chemi-osmotic type of mechanism. Nature 1961;191:144–148.
  43. Monod J: The growth of bacterial cultures. Ann Rev Microbiol 1949;3:371–394.
  44. Morowitz HJ: Foundations of Bioenergetics. New York, Academic Press, 1978, p 344.
  45. Mulder MM, Teixeira MJ, Postma PW, Van Dam K: Energetic consequences of multiple K+ uptake systems in Escherichia coli. Biochim Biophys Acta 1986;851:223–228.
  46. Neijssel OM, Tempest DW: Bioenergetic aspects of aerobic growth of Klebsiella aerogenes NCTC 418 in carbon-limited and carbon-sufficient culture. Arch Microbiol 1976;107:215–221.
  47. Nichols DG: Bioenergetics: An Introduction to Chemiosmotic Theory. New York, Academic Press, 1982.
  48. Novick A, Szilard L: Experiments with the chemostat on spontaneous mutations of bacteria.PNAS 1950;36:708–719.
  49. Otto R: Uncoupling of growth and acid production in Streptococcus cremoris. Arch Microbiol 1984;140:225–230.
  50. Pirt S.J.: The maintenance energy of bacteria in growing cultures. Proc R Soc Lond B Biol Sci 1965;163:224–231.
  51. Racker E: Mechanisms of energy transformations. Annu Rev Biochem 1977;46:1006–1014.
  52. Racker E: A view of misconduct in science. Nature 1989;339:91–93.
  53. Racker E, Spector M: Warburg effect revisited: merger of biochemistry and molecular biology. Science 1981;213:303–307.
  54. Reizer J, Hoischen C, Titgemeyer F, Rivolta C, Rabus R, Stulke J, Karamata D, Saier MH Jr, Hillen W: A novel protein kinase that controls carbon catabolite repression in bacteria. Mol Microbiol 1998;27:1157–1169.
  55. Repke KRH: Reinstatement of the ATP high energy paradigm. Mol Cell Biochem 2004;160–161:95–99.
  56. Russell JB: Heat production by ruminal bacteria in continuous culture and its relationship to maintenance energy. J Bacteriol 1986;168:694–701.
  57. Russell JB: Low affinity, high capacity system of glucose transport in the ruminal bacterium Streptococus bovis: evidence for a mechanism of facilitated diffusion. Appl Environ Microbiol 1990;56:3304–3307.
  58. Russell JB: Resistance of Streptococcus bovis to acetic acid at low pH: relationship between intracellular pH and anion accumulation. Appl Environ Microbiol 1991a;57:255–259.
  59. Russell JB: A re-assessment of bacterial growth efficiency: the heat production and membrane potential of Streptococcus bovis in batch and continuous culture. Arch Microbiol 1991b;155:559–565.
  60. Russell JB: The effect of pH on the heat production and membrane resistance of Streptococcus bovis. Arch Microbiol 1992a;158:54–58.
  61. Russell JB: Glucose toxicity and inability of Bacteroides ruminicola to regulate glucose transport and utilization. Appl Environ Microbiol 1992b;58:2040–2045.
  62. Russell JB: The glucose toxicity of Prevotella ruminicola: methylglyoxal accumulation and its effect of membrane physiology. Appl Environ Microbiol 1993a;59:2844–2850.
  63. Russell JB: Effect of amino acids on the heat production and growth efficiency of Streptococcus bovis: balance of anabolic and catabolic rates. Appl Environ Microbiol 1993b;59:1747–1751.
  64. Russell JB, Dombrowski DB: Effect of pH on the efficiency of growth by pure cultures of rumen bacteria in continuous culture. Appl Environ Microbiol 1980;39:604–610.
  65. Russell JB, Strobel HJ: ATPase-dependent energy spilling by the ruminal bacterium, Streptococcus bovis. Arch Microbiol 1990;153:378–383.
  66. Russell JB, Cook GM: Energetics of bacterial growth: balance of anabolic and catabolic reactions. Microbiol Rev 1995;59:48–62.
  67. Russell JB, Diez-Gonzalez F: The effects of fermentation acids on bacterial growth. Adv Microbial Physiol 1998;39, 205–234.
  68. Russell JB, Bond DR, Cook GM: The fructose diphosphate/phosphate regulation of carbohydrate metabolism in low G + C Gram-positive anaerobes. Res Microbiol 1996;147:528–535.
  69. Schönheit P, Moll J, Thauer RK: Growth parameters (Ks, μmax, Ys) of Methanobacterium thermoautotrophicum. Arch Microbiol 1980;127:59–65.

    External Resources

  70. Skulachev VP: The latest news from the sodium world. Biochim Biophys Acta 1994;1187:216–221.
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  75. Streekstra H, Buurman ET, Hoitink CWG, Teixeira De Mattos MJ, Neijssel OM, Tempest DW: Fermentation shifts and metabolic reactivity during anaerobic carbon-limited growth of Klebsiella aerogenes NCTC 418 on fructose, gluconate, mannitol and pyruvate. Arch Microbiol 1987;148:137–143.
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  79. Thomas S, Russell JB: The effect of cellobiose, glucose and cellulose on the survival of Fibrobacter succinogenes A3C cultures grown under ammonia limitation. Curr Microbiol 2003;48:219–223.

    External Resources

  80. Thompson J: In vivo regulation of glycolysis and characterization of sugar: phosphotransferase systems in Streptococcus lactis. J Bacteriol 1978;136:465–476.
  81. Van Kessel JS, Russell JB: The effect of amino nitrogen on the energetics of ruminal bacteria and its impact on energy spilling. J Dairy Sci 1996;79:1237–1243.
  82. Von Stockar U, Liu JS: Does microbial life always feed on negative entropy? Thermodynamic analysis of microbial growth. Biochim Biophys Acta 1999;1412:191–211.
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Author Contacts

J.B. Russell
US Plant, Soil and Nutrition Laboratory
Tower Road
Ithaca, NY 14853 (USA)
Tel. +1 607 255 4508, Fax +1 607 255 3904, E-Mail jbr8@cornell.edu

  

Article Information

Number of Print Pages : 11
Number of Figures : 2, Number of Tables : 1, Number of References : 87

  

Publication Details

Journal of Molecular Microbiology and Biotechnology

Vol. 13, No. 1-3, Year 2007 (Cover Date: August 2007)

Journal Editor: Saier Jr., M.H. (La Jolla, Calif.)
ISSN: 1464–1801 (print), 1660–2412 (Online)

For additional information: http://www.karger.com/MMB


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References

  1. Bauchop T, Elsden SR: The growth of microorganisms in relation to their energy supply.J Gen Microbiol 1960;23:457–469.
  2. Berman MC: Slippage and uncoupling in P-type cation pumps: implications for energy transduction mechanisms and regulation of metabolism. Biochim Biophys Acta2001;1503:329–340.
  3. Blaut M, Muller V, Gottschalk G: Energetics of Methanogens; in Krulwich T (ed): Bacterial Energetics. New York, Academic Press, 1990, pp 505–537.
  4. Bond DR, Russell JB: A role for fructose 1,6-diphosphate in the ATPase-mediated energy-spilling reaction of Streptococcus bovis. Appl Environ Microbiol 1996;62:2095–2099.
  5. Bond DR, Russell JB: Relationship between intracellular phosphate, proton motive force, and the rate of non-growth energy dissipation (energy spilling) in Streptococcus bovis JB1. Appl Environ Microbiol 1998;64:976–981.
  6. Bond DR, Russell JB: Proton motive force regulates the membrane conductance of Streptococcus bovis in a non-ohmic fashion. Microbiology 2000;146:687–694.
  7. Brand MD, Chien L-F, Ainscow EK, Rolfe DFS, Porter RK: The causes and functions of mitochondrial proton leak. Biochim Biophys Acta 1994;1187:132–139.
  8. Brock TD, Madigan JL: Biology of Microorganisms, ed 6, p 112. Englewood Cliffs, Prentice Hall, 1991.
  9. Buurman ET, Teixeira De Mattos MJ, Neijssel OM: Futile cycling of ammonium ions via the high affinity potassium uptake system (Kdp) of Escherichia coli. Arch Microbiol 1991;155:391–395.
  10. Buurman ET, Pennock J, Tempest DW, Teixeira De Mattos MJ, Neijssel OM: Replacement of potassium ions by ammonium ions in different micro-organisms grown in potassium-limited chemostat culture.Arch Microbiol 1989;152:58–63.
  11. Cook GM, Ye JJ, Russell JB, Saier MH: Properties of two sugar phosphate phosphatases from Streptococcus bovis and their involvement in inducer explusion. J Bacteriol 1995;177:7007–7009.
  12. Cooper RA, Anderson A: The formation and catabolism of methylglyoxal during glycolysis in Escherichia coli. FEBS Lett 1970;11:273–276.
  13. Cooper S: The origins and meaning of the Schaechter-Maaloe-Kjeldgaard experiments. J Gen Microbiol1993;139:1117–1124.
  14. Cot M, Loret MO, Francois J, Benbadis L: Physiological behaviour of Saccharomyces cerevisiae in aerated fed-batch fermentation for high level production of bioethanol. Biotechnol Bioeng 2001;75:345–354.
  15. Dimroth P: Sodium ion transport decarboxylases and otheraspects of sodium cycling in bacteria. Microbiol Rev 1987;51:320–340.
  16. Dlaskova A, Spacek T, Skobisova E, Santorova J, Jezek P: Certain aspects of uncoupling due to mitochondrial uncoupling proteins in vitro and in vivo. Biochim Biophys Acta 2006;1757:467–473.
  17. Feniouk BA, Mulkidjanian AY, Junge W: Proton slip in the ATP synthase of Rhodobacter capsulatus: induction, proton conduction, and nucleotide dependence. Biochim Biophys Acta 2005;1706:1184–1194.
  18. Ferguson GPT, Totemeyer S, MacLean MJ, Booth IR: Methylglyoxal production in bacteria: Suicide or survival? Arch Microbiol 1998;170:209–218.
  19. Fillingame RH, Dmitriev OY: Structural model of the transmembrane Fo rotary sector of H+-transporting ATP synthase derived by solution NMR and intersubunit cross-linking in situ. Biochim Biophys Acta 2002;1565:232–245.
  20. Flythe MD, Russell JB: The ability of acidic pH, growth inhibitors and glucose to increase the protonmotive force and energy spilling of amino acid fermenting Clostridium sporogenes MD1 cultures. Arch Microbiol 2005;183:236–242.
  21. Flythe MD, Russell JB: Fermentation acids inhibit amino acid deamination by Clostridium sporogenes MD1 via a mechanism involving a decline in intracellular glutamate rather than protonmotive force. Microbiology 2006;152:2619–2624.
  22. Flythe MD, Russell JB: The effect of acidic pH on the ability of Clostridium sporogenes MD1 to take up and retain intracellular potassium. FEMS Lett 2006;267:46–50.
  23. Garber K: News. J Natl Cancer Inst 2004;96:1805–1806.
  24. Gottschalk G: Bacterial Metabolism, ed 2. New York, Springer, 1986.
  25. Harold FM: The Vital Force: A Study of Bioenergetics. San Francisco, Freeman, 1986.
  26. Harold FM, Van Brunt J: Circulation of H+ and K+ across the plasma membrane is not obligatory for bacterial growth. Science 1977;197:372–373.
  27. Herbert D, Elsworth R, Telling RC: The continuous culture of bacteria: a theoretical and experimental study. J Gen Microbiol 1956;14:601–622.
  28. Hinkle PC, Kumar MA, Resetar A, Harris DL: Mechanistic stoichiometry of mitochondrial oxidative phosphorylation. Biochem 1991;30:3576–3582.
  29. Hungate R.E.: The rumen and its microbes, p. 282. 1966. Academic Press, New York, N.Y.
  30. Jay JM: Modern Food Microbiology, ed 4. New York, Van Nostrand Reinhold, 1989.
  31. Kleiber M: Davis, Memorial Book Department of Animal Science, University of California, 1976. http://animalscience.ucdavis.edu/memorial/kleiber.htm
  32. Klotz IM: Energy Changes in Biochemical Reactions. New York, Academic Press, 1967.
  33. Lehninger AL: Biochemistry, New York, Worth Publishers, 1975, p 12.
  34. Lehninger AL, Nelson DL, Cox MM: Principles of Biochemistry. New York, Worth Publishers, 1993, p 6.
  35. Lipmann F: Metabolic generation and utilization of phosphate bond energy. Adv Enzymol 1941;1:99–162.
  36. Liu JS, Marison IW, Von Stockar U: Microbial growth by a net heat up-take: a calorimetric and thermodynamic study on acetotrophic methanogenesis by Methanosarcina barkeri. Biotechnol Bioeng 2001;275:170–180.

    External Resources

  37. Lodge-Ivey SL, May T, Petersen MK, Strickland JR: Determination of methylglyoxal in ruminal fluid by high-performance liquid chromatography using fluorometric detection. J Agric Food Chem 2004;52:6875–6878.
  38. Maglione G, Russell JB: The adverse effect of nitrogen limitation and excess-cellobiose on Fibrobacter succinogenes. Appl Microbiol Biotechnol 1997;48:720–725.
  39. Maglione G, Russell JB, Wilson DB: Kinetics of cellulose digestion by Fibrobacter succinogenes S85. Appl Environ Microbiol 1997;63:665–669.
  40. Maloney PC: Microbes and membrane biology. FEMS Microbiol Rev 1990;87:91–102.
  41. Marr AG, Nilson EH, J CD: The maintenance requirement of Escherichia coli. Ann NY Acad Sci 1962;102:536–548.

    External Resources

  42. Mitchell P: Coupling of phosphorylation to electron and hydrogen transfer by a chemi-osmotic type of mechanism. Nature 1961;191:144–148.
  43. Monod J: The growth of bacterial cultures. Ann Rev Microbiol 1949;3:371–394.
  44. Morowitz HJ: Foundations of Bioenergetics. New York, Academic Press, 1978, p 344.
  45. Mulder MM, Teixeira MJ, Postma PW, Van Dam K: Energetic consequences of multiple K+ uptake systems in Escherichia coli. Biochim Biophys Acta 1986;851:223–228.
  46. Neijssel OM, Tempest DW: Bioenergetic aspects of aerobic growth of Klebsiella aerogenes NCTC 418 in carbon-limited and carbon-sufficient culture. Arch Microbiol 1976;107:215–221.
  47. Nichols DG: Bioenergetics: An Introduction to Chemiosmotic Theory. New York, Academic Press, 1982.
  48. Novick A, Szilard L: Experiments with the chemostat on spontaneous mutations of bacteria.PNAS 1950;36:708–719.
  49. Otto R: Uncoupling of growth and acid production in Streptococcus cremoris. Arch Microbiol 1984;140:225–230.
  50. Pirt S.J.: The maintenance energy of bacteria in growing cultures. Proc R Soc Lond B Biol Sci 1965;163:224–231.
  51. Racker E: Mechanisms of energy transformations. Annu Rev Biochem 1977;46:1006–1014.
  52. Racker E: A view of misconduct in science. Nature 1989;339:91–93.
  53. Racker E, Spector M: Warburg effect revisited: merger of biochemistry and molecular biology. Science 1981;213:303–307.
  54. Reizer J, Hoischen C, Titgemeyer F, Rivolta C, Rabus R, Stulke J, Karamata D, Saier MH Jr, Hillen W: A novel protein kinase that controls carbon catabolite repression in bacteria. Mol Microbiol 1998;27:1157–1169.
  55. Repke KRH: Reinstatement of the ATP high energy paradigm. Mol Cell Biochem 2004;160–161:95–99.
  56. Russell JB: Heat production by ruminal bacteria in continuous culture and its relationship to maintenance energy. J Bacteriol 1986;168:694–701.
  57. Russell JB: Low affinity, high capacity system of glucose transport in the ruminal bacterium Streptococus bovis: evidence for a mechanism of facilitated diffusion. Appl Environ Microbiol 1990;56:3304–3307.
  58. Russell JB: Resistance of Streptococcus bovis to acetic acid at low pH: relationship between intracellular pH and anion accumulation. Appl Environ Microbiol 1991a;57:255–259.
  59. Russell JB: A re-assessment of bacterial growth efficiency: the heat production and membrane potential of Streptococcus bovis in batch and continuous culture. Arch Microbiol 1991b;155:559–565.
  60. Russell JB: The effect of pH on the heat production and membrane resistance of Streptococcus bovis. Arch Microbiol 1992a;158:54–58.
  61. Russell JB: Glucose toxicity and inability of Bacteroides ruminicola to regulate glucose transport and utilization. Appl Environ Microbiol 1992b;58:2040–2045.
  62. Russell JB: The glucose toxicity of Prevotella ruminicola: methylglyoxal accumulation and its effect of membrane physiology. Appl Environ Microbiol 1993a;59:2844–2850.
  63. Russell JB: Effect of amino acids on the heat production and growth efficiency of Streptococcus bovis: balance of anabolic and catabolic rates. Appl Environ Microbiol 1993b;59:1747–1751.
  64. Russell JB, Dombrowski DB: Effect of pH on the efficiency of growth by pure cultures of rumen bacteria in continuous culture. Appl Environ Microbiol 1980;39:604–610.
  65. Russell JB, Strobel HJ: ATPase-dependent energy spilling by the ruminal bacterium, Streptococcus bovis. Arch Microbiol 1990;153:378–383.
  66. Russell JB, Cook GM: Energetics of bacterial growth: balance of anabolic and catabolic reactions. Microbiol Rev 1995;59:48–62.
  67. Russell JB, Diez-Gonzalez F: The effects of fermentation acids on bacterial growth. Adv Microbial Physiol 1998;39, 205–234.
  68. Russell JB, Bond DR, Cook GM: The fructose diphosphate/phosphate regulation of carbohydrate metabolism in low G + C Gram-positive anaerobes. Res Microbiol 1996;147:528–535.
  69. Schönheit P, Moll J, Thauer RK: Growth parameters (Ks, μmax, Ys) of Methanobacterium thermoautotrophicum. Arch Microbiol 1980;127:59–65.

    External Resources

  70. Skulachev VP: The latest news from the sodium world. Biochim Biophys Acta 1994;1187:216–221.
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