Archives of Microbiology

, Volume 120, Issue 3, pp 275–281 | Cite as

Growth and energy production in Bacteroides amylophilus

  • Howard F. Jenkinson
  • Malcolm Woodbine
Article

Abstract

The molar growth yield (Ym) of Bacteroides amylophilus strain WP91 on maltose was 68±2 g/mol when determined from batch cultures at the peaks of maximal growth. Continued incubation led to considerable cell lysis. When calculated from batch cultures in exponential phase (specific growth rate, μ=0.57 h-1) Ym was 101 g/mol. The maximum value of Ym in maltose-limited chemostat cultures at the maximum dilution rate (D) attainable (D=μ=0.39 h-1) was about 79 g/mol. Ammonia-Fmited chemostat cultures metabolized maltose with a much reduced efficiency and this was associated with a difference in morphology and chemical composition of the cells. The theoretical maximum molar growth yields (Y m max ) were 55 and 114 g/mol for ammonia- and maltose-limited growth respectively. However, if account was taken of extracellular nitrogen-containing material in ammonia-limited cultures, Y m max became 60. The maintenance coefficient (ms), estimated from the lines relating the specific rate of maltose consumption (qm) and D (where ms=qm at D=0), was 7.4±0.6×10-4 mol maltose/g x h for both nutrient limitations. A difference in maintenance energy demand, independent of growth-rate, could not account, therefore, for the observed differences in Ym between ammonia- and maltose-limited growth.

Key words

Bacteroides amylophilus Rumen bacteria Growth yield Nutrient limitation Energetics Maintenance energy 

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References

  1. Bauchop, T., Elsden, S. R.: The growth of micro-organisms in relation to their energy supply. J. Gen. Microbiol. 23, 457–469 (1960)Google Scholar
  2. Blackburn, T. H.: Protease production by Bacteroides amylophilus, a rumen bacterium. Ph. D. Thesis, University of Aberdeen (1965)Google Scholar
  3. Blackburn, T. H.: Protease production by Bacteroides amylophilus strain H-18. J. Gen. Microbiol. 53, 27–36 (1968)Google Scholar
  4. Blackburn, T. H., Hobson, P. N.: Further studies on the isolation of proteolytic bacteria from the sheep rumen. J. Gen. Microbiol. 29, 69–81 (1962)Google Scholar
  5. Bryant, M. P.: Nutritional requirements of the predominant rumen cellulolytic bacteria. Fed. Proc. 32, 1809–1813 (1973)Google Scholar
  6. Caldwell, D. R., Keeney, M., Barton, J. S., Kelley, J. F.: Sodium and other inorganic growth requirements of Bacteroides amylophilus. J. Bacteriol. 114, 782–789 (1973)Google Scholar
  7. Conway, E. J.: Microdiffusion analysis and volumetric error, 5th ed. London: CrosbyLockwood & Son Ltd. 1962Google Scholar
  8. Dawes, E. A., Senior, P. J.: The role and regulation of energy reserve polymers in micro-organisms. Adv. Microb. Physiol. 10, 135–266 (1973)Google Scholar
  9. DeLuca, H. F.: Manometric analyses. In: Manometric and biochemical techniques, 5th ed. (W. W. Umbreit, R. H. Burris, J. F. Stauffer, eds.). pp. 247. Minnesota: Burgess Publishing Company 1972Google Scholar
  10. Dubois, M., Gilles, K. A., Hamilton, J. K., Rebers, P. A., Smith, F.: Colorimetric method for determination of sugars and related substances. Analyt. Chem. 28, 350–356 (1956)Google Scholar
  11. Forrest, W. W., Walker, D. J.: The generation and utilization of energy during growth. Adv. Microb. Physiol. 5, 213–274 (1971)Google Scholar
  12. Henderson, C., Hobson, P. N., Summers, R.: The production of amylase, protease and lipolytic enzymes by two species of anaerobic rumen bacteria. In: Continuous cultivation of micro-organisms (J. Malek, ed.), pp. 189–204. Prague: Academia 1969Google Scholar
  13. Herbert, D.: The chemical composition of micro-organisms as a function of their environment. In: Microbial reaction to environment. Symp. Soc. gen. Microbiol. 11, 391–416 (1961)Google Scholar
  14. Herbert, D.: Stoicheiometric aspects of microbial growth. In: Continuous culture 6: applications and new fields (A. C. R. Dean, D. C. Ellwood, C. G. T. Evans, J. Melling, eds.), pp. 1–30. Chichester: Ellis Horwood Ltd. 1976Google Scholar
  15. Herbert, D., Phipps, P. J., Strange, R. E.: Chemical analysis of microbial cells. In: Methods in microbiology, Vol. 5B (J. R. Norris, D. W. Ribbons, eds.), pp. 209–344. London: Academic Press 1971Google Scholar
  16. Hobson, P. N.: Continuous culture of rumen bacteria: apparatus. J. Gen. Microbiol. 38, 161–166 (1965)Google Scholar
  17. Hobson, P. N., Summers, R.: The continuous culture of anaerobic bacteria. J. gen. Microbiol. 47, 53–65 (1967)Google Scholar
  18. Hobson, P. N., Summers, R.: ATP pool and growth yield in Selenomonas ruminantium. J. Gen. Microbiol. 70, 351–360 (1972)Google Scholar
  19. Hobson, P. N., McDougall, E. J., Summers, R.: The nitrogen sources of Bacteroides amylophilus. J. Gen. Microbiol. 50, i (1968)Google Scholar
  20. Holdeman, L. V., Moore, W. E. C.: Anaerobic laboratory manual. Blacksburg: Virginia Polytechnic Institute and State University 1972Google Scholar
  21. Hullah, W. A., Blackburn, T. H.: Uptake and incorporation of amino acids and peptides by Bacteroides amylophilus. App. Microbiol. 21, 187–191 (1971)Google Scholar
  22. Hungate, R. E.: The rumen and its microbes. London: Academic Press 1966Google Scholar
  23. Hungate, R. E.: A roll tube method for the cultivation of strict anaerobes. In: Methods in microbiology, Vol. 3B (J. B. Norris, D. W. Ribbons, eds.), pp. 117–132. London: Academic Press Inc. 1969Google Scholar
  24. Jenkinson, H. F.: Aspects of rumen bacterial growth. Ph. D. Thesis, University of Nottingham (1978)Google Scholar
  25. Latham, M. J., Sharpe, E. M.: The isolation of anaerobic organisms from the bovine rumen. In: Isolation of anaerobes (D. A. Shapton, R. G. Board, eds.), pp. 132–147. London: Academic Press Inc. 1971Google Scholar
  26. Lazdunski, A., Belaich, J. P.: Uncoupling in bacterial growth: ATP pool variation in Zymomonas mobilis cells in relation to different uncoupling conditions of growth. J. Gen. Microbiol. 70, 187–197 (1972)Google Scholar
  27. Lowry, O. H., Rosebrough, N. J., Farr, A. L., Randall, R. J.: Protein measurement with the Folin-phenol reagent. J. Biol. Chem. 193, 265–275 (1951)Google Scholar
  28. McGill, D. J., Dawes, E. A.: Glucose and fructose metabolism in Zymomonas anaerobia. Biochem. J. 125, 1059–1068 (1971)Google Scholar
  29. Macy, J. M., Snellen, J. E., Hungate, R. E.: Use of syringe methods for anaerobiosis. Amer. J. clin. Nutr. 25, 1318–1323 (1972)Google Scholar
  30. Monod, J.: Recherches sur la croissance des cultures bactériennes. Paris: Herman and Cie 1942Google Scholar
  31. Moustafa, H. H., Collins, E. B.: Molar growth yields of certain lactic acid bacteria as influenced by autolysis. J. Bacteriol 96, 117–125 (1968)Google Scholar
  32. Neijssel, O. M., Tempest, D. W.: Bioenergetic aspects of aerobic growth of Klebsiella aerogenes NCTC 418 in carbon-limited and carbon-sufficient chemostat culture. Arch. Microbiol. 107, 215–221 (1976)Google Scholar
  33. Parker, C. A.: A method for the determination of total nitrogen in microgram amounts. Aust. J. exp. Biol. med. Sci. 39, 515–520 (1961)Google Scholar
  34. Payne, W. J.: Energy yields and growth of heterotrophs. Ann. Rev. Microbiol. 24, 17–52 (1970)Google Scholar
  35. Pirt, S. J.: The maintenance energy of bacteria in growing cultures. Proc. R. Soc. London, Ser. B 163, 224–231 (1965)Google Scholar
  36. Postgate, J. R.: The viability of very slow-growing populations: A model for the natural ecosystem. Bull. Ecol. Res. Comm. (Stockholm) 17, 287–292 (1973)Google Scholar
  37. Powell, E. O.: The growth rate of micro-organisms as a function of substrate concentration. In: Microbial physiology and continuous culture (E. O. Powell, C. G. T. Evans, R. E. Strange, D. W. Tempest, eds.), pp. 34–56. London: H.M.S.O. 1967Google Scholar
  38. Rodgers, K.: Estimation of succinic acid in biological materials. Biochem. J. 80, 240–244 (1961)Google Scholar
  39. Stouthamer, A. H.: Energetic aspects of the growth of micro-organisms. In: Microbial energetics. Symp. Soc. Gen. Microbiol. 27, 285–315 (1977)Google Scholar
  40. Stouthamer, A. H., Bettenhaussen, C.: Utilization of energy for growth and maintenance in continuous and batch cultures of micro-organisms. Biochim. biophys. Acta 301, 53–70 (1973)Google Scholar
  41. Umbreit, W. W., Burris, R. H., Stauffer, J. F.: Manometric and biochemical techniques, 5th. Minneapolis: Burgess Publishing Company 1972Google Scholar
  42. Veldkamp, H.: Continuous culture in microbial physiology and ecology. Shildon: Meadowfield Press Ltd. 1976Google Scholar
  43. de Vries, W., Kapteijn, W. M. C., van der Beek, E. G., Stouthamer, A. H.: Molar growth yields and fermentation balances of Lactobacillus casei L3 in batch cultures and in continous cultures. J. Gen. Microbiol. 63, 333–345 (1970)Google Scholar

Copyright information

© Springer-Verlag 1979

Authors and Affiliations

  • Howard F. Jenkinson
    • 1
  • Malcolm Woodbine
    • 1
  1. 1.Department of Applied Biochemistry and NutritionUniversity of Nottingham, School of AgricultureSutton BoningtonUK

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