1887

Abstract

The physiological behaviour of subsp. MG 1363 was characterized in continuous culture under various acidic conditions (pH 4·7–6·6). Biomass yield was diminished in cultures with low pH and the energy dedicated to maintenance increased due to organic acid inhibition and cytoplasmic acidification. Under such acidic conditions, the specific rate of glucose consumption by the bacterium increased, thereby enhancing energy supply. This acceleration of glycolysis was regulated by both an increase in the concentrations of glycolytic enzymes (hierarchical regulation) and the specific modulation of enzyme activities (metabolic regulation). However, when the inhibitory effect of intracellular pH on enzyme activity was taken into account in the model of regulation, metabolite regulation was shown to be the dominant factor controlling pathway flux. The changes in glycolytic enzyme concentrations were not correlated directly to modifications in transcript concentrations. Analyses of the relative contribution of the phenomena controlling enzyme synthesis indicated that translational regulation had a major influence compared to transcriptional regulation. An increase in the translation efficiency was accompanied by an important decrease of total cellular RNA concentrations, confirming that the translation apparatus of was optimized under acid stress conditions.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.26146-0
2003-07-01
2024-03-29
Loading full text...

Full text loading...

/deliver/fulltext/micro/149/7/mic1491935.html?itemId=/content/journal/micro/10.1099/mic.0.26146-0&mimeType=html&fmt=ahah

References

  1. Asanuman N., Hino T. 2000; Effect of pH and energy supply on activity and amount of pyruvate formate-lyase in Streptococcus bovis . Appl Environ Microbiol 66:3773–3777
    [Google Scholar]
  2. Christensen J. E., Dudley E. G., Pederson J. H., Steele J. L. 1999; Peptidases and amino acid catabolism in lactic acid bacteria. Antonie van Leeuwenhoek 76:217–246
    [Google Scholar]
  3. Cocaign-Bousquet M., Garrigues C., Novak L., Lindley N. D., Loubière P. 1995; Rational development of a simple synthetic medium for the sustained growth of Lactococcus lactis . J Appl Bacteriol 79:108–116
    [Google Scholar]
  4. Cook G. M., Russell J. B. 1994; The effect of extracellular pH and lactic acid on pH homeostasis in Lactococcus lactis and Streptococcus bovis . Curr Microbiol 28:165–168
    [Google Scholar]
  5. Even S., Lindley N. D., Cocaign-Bousquet M. 2001; Molecular physiology of sugar catabolism in Lactococcus lactis IL 1403. J Bacteriol 183:3817–3824
    [Google Scholar]
  6. Even S., Lindley N. D., Loubière P., Cocaign-Bousquet M. 2002; Dynamic response of catabolic pathways to auto-acidification in Lactococcus lactis : transcript profiling in relation to metabolic and energetic constraints. Mol Microbiol 45:1143–1152
    [Google Scholar]
  7. Fontaine L., Even S., Soucaille P., Lindley N. D., Cocaign-Bousquet M. 2001; Transcript quantification based on chemical labelling of RNA associated to fluorescent detection. Anal Biochem 298:246–252
    [Google Scholar]
  8. Garrigues C., Loubière P., Lindley N. D., Cocaign-Bousquet M. 1997; Control of the shift from homolactic acid to mixed-acid fermentation in Lactococcus lactis : predominant role of the NADH/NAD+ ratio. J Bacteriol 179:5282–5287
    [Google Scholar]
  9. Gasson M. J. 1983; Plasmid complements of Streptococcus lactis NCDO 712 and other lactic streptococci after protoplast induced curing. J Bacteriol 154:1–9
    [Google Scholar]
  10. Hartke A., Bouché S., Giard J.-C., Benachour A., Boutibonnes P., Auffray Y. 1996; The lactic acid stress response of Lactococcus lactis subsp. lactis . Curr Microbiol 33:194–199
    [Google Scholar]
  11. Hutkins R. W., Nannen N. L. 1993; pH homeostasis in lactic acid bacteria. J Dairy Sci 76:2354–2365
    [Google Scholar]
  12. Kashket E. R. 1987; Bioenergetics of lactic acid bacteria: cytoplasmic pH and osmotolerance. FEMS Microbiol Rev 46:233–244
    [Google Scholar]
  13. Kim W. S., Ren J., Dunn N. W. 1999; Differentiation of Lactococcus lactis subspecies lactis and subspecies cremoris strains by their adaptative response to stresses. FEMS Microbiol Lett 171:57–65
    [Google Scholar]
  14. Kobayashi H., Suzuki T., Unemoto T. 1986; Streptococcal cytoplasmic pH is regulated by changes in amount and activity of a proton-translocating ATPase. J Biol Chem 261:627–630
    [Google Scholar]
  15. Le Bloas P., Guilbert N., Loubière P., Lindley N. D. 1993; Growth inhibition and pyruvate overflow during glucose metabolism of Eubacterium limosum are related to a limited capacity to reassimilate CO2 by the acyl-CoA pathway. J Gen Microbiol 139:1861–1869
    [Google Scholar]
  16. Loubière P., Salou P., Leroy M. J., Lindley N. D., Pareilleux A. 1992; Electrogenic malate uptake and improved growth energetics of the malolactic bacterium Leuconostoc oenos grown on glucose-malate mixtures. J Bacteriol 174:5302–5308
    [Google Scholar]
  17. Loubière P., Cocaign-Bousquet M., Matos J., Goma G., Lindley N. D. 1997; Influence of end-products inhibition and nutrient limitations on the growth of Lactococcus lactis subsp. lactis . J Appl Microbiol 82:95–100
    [Google Scholar]
  18. Melchiorsen C. R., Jensen N. B., Christensen B., Vaever Jokumsen K., Villadsen J. 2001; Dynamics of pyruvate metabolism in Lactococcus lactis . Biotechnol Bioeng 74:271–279
    [Google Scholar]
  19. Mercade M., Lindley N. D., Loubière P. 2000; Metabolism of Lactococcus lactis subsp. cremoris MG 1363 in acid stress conditions. Int J Food Microbiol 55:161–165
    [Google Scholar]
  20. Nannen N. L., Hutkins R. W. 1991a; Intracellular pH effects in lactic acid bacteria. J Dairy Sci 74:741–746
    [Google Scholar]
  21. Nannen N. L., Hutkins R. W. 1991b; Proton-translocating adenosine triphosphatase activity in lactic acid bacteria. J Dairy Sci 74:747–751
    [Google Scholar]
  22. Neidhardt F. C., Ingraham J. L., Schaechter M. 1990; Composition and organization of the bacterial cell. In Physiology of the Bacterial Cell. A Molecular Approach pp  1–29 Sunderland, MA: Sinauer;
    [Google Scholar]
  23. Nierlich D. P. 1978; Regulation of bacterial growth, RNA and protein synthesis. Annu Rev Microbiol 32:393–432
    [Google Scholar]
  24. Nomura M., Nakajima I., Fujita Y., Kobayashi M., Kimoto H., Suzuki I., Aso H. 1999; Lactococcus lactis contains only one glutamate decarboxylase gene. Microbiology 145:1375–1380
    [Google Scholar]
  25. Novak L., Cocaign-Bousquet M., Lindley N. D., Loubière P. 1997; Metabolism and energetics of Lactococcus lactis during growth in complex or synthetic media. Appl Environ Microbiol 65:2665–2670
    [Google Scholar]
  26. O'Sullivan E., Condon S. 1997; Intracellular pH is a major factor in the induction of tolerance to acid and other stresses in Lactococcus lactis . Appl Environ Microbiol 63:4210–4215
    [Google Scholar]
  27. O'Sullivan E., Condon S. 1999; Relationship between acid tolerance, cytoplasmic pH, and ATP and H+-ATPase levels in chemostat cultures of Lactococcus lactis . Appl Environ Microbiol 65:2287–2293
    [Google Scholar]
  28. Poolman B., Driessen A. J. M., Konings W. N. 1987a; Regulation of solute transport in streptococci by external and internal pH values. Microbiol Rev 51:498–508
    [Google Scholar]
  29. Poolman B., Driessen A. J. M., Konings W. N. 1987b; Regulation of arginine-ornithine exchange and the arginine deiminase pathway in Streptococcus lactis . J Bacteriol 169:5597–5604
    [Google Scholar]
  30. Rallu F., Gruss A., Maguin E. 1996; Lactococcus lactis and stress. Antonie van Leeuwenhoek 70:243–251
    [Google Scholar]
  31. Sanders J. W., Venema G., Kok J. 1999; Environmental stress responses in Lactococcus lactis . FEMS Microbiol Rev 23:483–501
    [Google Scholar]
  32. Siegumfeldt H., Rechinger K. B., Jakobsen M. 2000; Dynamic changes of intracellular pH in individual lactic acid bacterium cells in response to a rapid drop in extracellular pH. Appl Environ Microbiol 66:2330–2335
    [Google Scholar]
  33. Small P. L. C., Waterman S. R. 1998; Acid stress, anaerobiosis and gadCB : lessons from Lactococcus lactis and Escherichia coli . Trends Microbiol 6:214–216
    [Google Scholar]
  34. ter Kuile B. H., Westeroff H. V. 2001; Transcriptome meets metabolome: hierarchical and metabolic regulation of the glycolytic pathways. FEBS Lett 500:169–171
    [Google Scholar]
  35. Thomas T. D., Ellwood D. C., Longyear M. C. 1979; Change from homo- to heterolactic fermentation by Streptococcus lactis cremoris : pathways, products and regulation. J Bacteriol 144:672–682
    [Google Scholar]
  36. Uribelarrea J. L., Pacaud S., Goma G. 1985; New method for measuring the cell water content by thermogravimetry. Biotechnol Lett 7:75–80
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.26146-0
Loading
/content/journal/micro/10.1099/mic.0.26146-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error