Natural-abundance isotope ratio mass spectrometry as a means of evaluating carbon redistribution during glucose-citrate cofermentation by Lactococcus lactis

European Journal of Biochemistry

Volumn 271, Issue 22, 2004, Pages 4392-4400

  Mahmoud, Mohamed ^a   Gentil, Emmanuel ^a   Robins, Richard J ^a  

^a UNIVERSITÉ DE NANTES   (France)

Author keywords

Carbon balance; Isotope ratio mass spectrometry; Lactic acid bacteria; Metabolic regulation; Pyruvate

Indexed keywords

2,3 BUTANEDIONE; ACETIC ACID; ACETOIN; CARBON; CARBON 13; CITRIC ACID; FORMIC ACID; GLUCOSE; LACTIC ACID; PYRUVIC ACID;

ARTICLE; BACTERIAL METABOLISM; CARBON BALANCE; CARBON METABOLISM; FERMENTATION; GLUCOSE METABOLISM; ISOTOPE RATIO MASS SPECTROMETRY; LACTOCOCCUS LACTIS; LACTOCOCCUS LACTIS DIACETYLACTIS; MASS SPECTROMETRY; METABOLIC REGULATION; NONHUMAN; OXIDATION REDUCTION STATE; PRIORITY JOURNAL; PROTEIN METABOLISM; PROTON NUCLEAR MAGNETIC RESONANCE;

CARBON; CARBON ISOTOPES; CITRATES; FERMENTATION; GLUCOSE; LACTOCOCCUS LACTIS; MASS SPECTROMETRY; PYRUVIC ACID;

BACTERIA (MICROORGANISMS); LACTOCOCCUS LACTIS; LACTOCOCCUS LACTIS SUBSP. LACTIS BV. DIACETYLACTIS; POSIBACTERIA; STREPTOCOCCUS;

EID: 9644288057     PISSN: 00142956     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1432-1033.2004.04376.x     Document Type: Article

References (47)

1. Cocaign-Bousquet, M., Garrigues, C., Loubière, P. & Lindley, N. (1996) Physiology of pyruvate metabolism in Lactococcus lactis. Antonie Leeuwenhoek 70, 253-267.
2. Rondags, E., Halliday, E. & Marc, I. (1998) Diacetyl production mechanism by a strain of Lactococcus lactis spp. lactis bv. diacetylactis. Study of α-acetolactic acid extracellular accumulation under anaerobiosis. Appl. Biochem. Biotechnol. 69, 113-125.
3. Hugenholtz, J. (1993) Citrate metabolism in lactic acid bacteria. FEMS Microbiol. Rev. 12, 165-178.
4. van Beynum, J. & Pette, J. (1939) The decomposition of citric acid by Betacoccus cremoris. J. Dairy Res. 10, 250-266.
5. Hache, C., Cachon, R., Wache, Y., Belguendouz, T., Riondet, C., Deraedt, A. & Diviès, C. (1999) Influence of lactose-citrate cometabolism on the differences of growth and energetics in Lactococcus lactis, Leuconostoc mesenteroides ssp. cremoris. Appl. Microbiol. 22, 507-513.
6. Magni, C., de Mendoza, D., Konings, W. & Lolkema, J. (1999) Mechanism of citrate metabolism in Lactococcus lactis: resistance against lactate toxicity at low pH. J. Bacteriol. 181, 1451-1457.
7. Boumerdassi, H., Monnet, C., Desmazeaud, M. & Corrieu, G. (1997) Effect of citrate on production of diacetyl and acetoin by Lactococcus lactis ssp. lactis CNRZ. 483 cultivated in the presence of oxygen. J. Dairy Sci. 80, 634-639.
8. Petit, C., Vilchez, F. & Marczak, R. (1989) Influence of citrate on diacetyl and acetoin production by fully grown cells of Streptococcus lactis subsp. diaceylactis. Curr. Microbiol. 19, 319-323.
9. Cachon, R. & Diviès, C. (1993) A descriptive model for citrate utilization by Lactococcus lactis ssp. lactis bv. diacetylactis. Biotecnol. Lett. 15, 837-842.
10. Goupry, S., Croguennec, T., Gentil, E. & Robins, R.J. (2000) Metabolic flux in glucose/citrate co-fermentation by lactic acid bacteria as measured by isotopic ratio analysis. FEMS Microbiol. Lett. 182, 207-211.
11. Goupry, S., Gentil, E., Akoka, S. & Robins, R. (2003) Co-fermentation of glucose and citrate by Lactococcus lactis diacetylactis: quantification of the relative metabolic rates by isotopic ratio analysis at natural abundance. Appl. Microbiol. Biotechnol. 62, 489-497.
12. Snoep, J., Teixeira de Mattos, M., Starrenburg, M. & Hugenholtz, J. (1992) Isolation, characterization and physiological role of the pyruvate dehydrogenase complex and alpha-acetolactate synthase of Lactococcus lactis subsp. lactis bv diacetylactis. J. Bacteriol. 174, 4838-4841.
13. Curic, M., Stuer-Lauridsen, B., Renault, P. & Nilsson, D. (1999) A general method for selection of α-acetolactate decarboxylase-deficient Lactococcus lactis mutants to improve diacetyl formation. Appl. Environ. Microbiol. 65, 1202-1206.
14. Hugenholtz, J., Kleerebezem, M., Starrenburg, M., Delcour, J., de Vos, W. & Hols, P. (2000) Lactococcus lactis as a cell factory for high-level diacetyl production. Appl. Environ. Microbiol. 66, 4112-4114.
15. Hugenholtz, J. & Kleerebezem, M. (1999) Metabolic engineering of lactic acid bacteria: overview of the approaches and results of pathway rerouting involved in food fermentations. Curr. Opin. Biotechnol. 10, 492-497.
16. 13C nuclear magnetic resonance studies of citrate and glucose cometabolism by Lactococcus lactis. Appl. Environ. Microbiol. 60, 1739-1748.
17. 13C nuclear magnetic resonance. Appl. Environ. Microbiol. 57, 3371-3377.
18. Koebmann, B., Andersen, H., Solem, C. & Jensen, P. (2002) Experimental determination of control of glycolysis in Lactococcus lactis. Antonie Leeuwenhoek 82, 237-248.
19. 13C NMR. J. Biol. Chem. 277, 28088-28098.
20. Andersen, H., Pedersen, M., Hammer, K. & Jensen, P. (2001) Lactate dehydrogenase has no control on lactate production but has a strong negative control on formate production in Lactococcus lactis. Eur. J. Biochem. 268, 6379-6389.
21. Neves, A., Ramos, A., Shearman, C., Gasson, M. & Santos, H. (2002) Catabolism of mannitol in Lactococcus lactis MG1363 and a mutant defective in lactate dehydrogenase. Microbiology 148, 3467-3476.
22. Monnet, C., Aymes, F. & Corrieu, G. (2000) Diacetyl and α-acetolactate overproduction by Lactococcus lactis subsp. lactis biovar. diacetylactis mutants that are deficient in α-acetolatate decarboxylase and have low lactate dehydrogenase activity. Appl. Environ. Microbiol. 66, 5518-5520.
23. Swindell, S., Benson, K., Griffin, H., Renault, P., Ehrlich, S. & Gasson, M. (1996) Genetic manipulation of the pathway for diacetyl metabolism in Lactococcus lactis. Appl. Environ. Microbiol. 62, 2641-2643.
24. 13C-NMR. Eur. J. Biochem. 267, 3859-3868.
25. Hoefnagel, M., Starrenburg, M., Martens, D., Hugenholtz, J., Kleerebezem, M., Van Swam, I., Bongers, R., Westerhoff, H. & Snoep, J. (2002) Metabolic engineering of lactic acid bacteria, the combined approach: kinetic modelling, metabolic control and experimental analysis. Microbiology 148, 1003-1013.
26. Brand, W. (1996) High precision isotope ratio monitoring techniques in mass spectrometry. J. Mass Spectrom. 31, 225-235.
27. Terzaghi, B. & Sandine, W. (1975) Improved medium for lactic Streptococci and their bacteriophages. Appl. Microbiol. 29, 807-813.
28. Silvestre, V., Goupry, S., Trierweiler, M., Robins, R. & Akoka, S. (2001) Determination of substrate and product concentrations in lactic acid bacterial fermentation by proton NMR using the ERETIC method. Anal. Chem. 73, 1862-1868.
29. Goupry, S., Gentil, E., Rochut, N. & Robins, R. (2000) Evaluation of solid-phase microextraction for the isotopic analysis of volatile compounds produced during fermentation by lactic acid bacteria. J. Agric. Food Chem. 48, 2222-2227.
30. Nordkvist, M., Jensen, N. & Villadsen, J. (2003) Glucose metabolism in Lactococcus lactis MG1363 under different aeration conditions: requirement of acetate to sustain growth under microaerobic conditions. Appl. Environ. Microbiol. 69, 3462-3468.
31. Crow, V. (1990) Properties of 2,3-butanediol dehydrogenases from Lactococcus lactis subsp. lactis in relation to citrate fermentation. Appl. Microbiol. Biotechnol. 56, 1656-1665.
32. Rattray, F., Walfridsson, M. & Nilsson, D. (2000) Purification and characterization of a diacetyl reductase from Leuconostoc pseudomesenteroides. Int. Dairy J. 10, 781-789.
33. Hugenholtz, J. & Starrenburg, M. (1992) Diacetyl production by different strains of Lactococcus lactis subsp. lactis var. diacetylactis and Leuconostoc spp. Appl. Microbiol. Biotechnol. 38, 17-22.
34. Monnet, C., Schmitt, P. & Diviès, C. (1994) Diacetyl production in milk by an α-acetolactate acid accumulating strain of Lactococcus lactis ssp. lactis biovar. diacetylactis. J. Dairy Sci. 77, 2916-2924.
35. Rondags, E., Stein, G., Germain, P. & Marc, I. (1996) Kinetic study of the chemical reactivity of α-acetolactate as a function of pH in water, and in fresh and fermented culture media used for Lactococcus lactis spp. lactis bv. diacetylactis cultivation. Biotechnol. Lett. 18, 747-752.
36. Boumerdassi, H., Desmazeaud, M., Monnet, C., Boquein, C. & Corrieu, G. (1996) Improvement of diacetyl production by Lactococcus lactis ssp. lactis CNRZ. 483 through oxygen control. J. Dairy Sci. 79, 775-781.
37. de Man, J. (1959) The formation of diacetyl and acetoin from α-acetolactic acid. Recueil des Traveaux Chimiques des Pays-Bas de Belgique 78, 480-486.
38. Park, S.-H., Xing, R. & Whitman, W. (1995) Nonenzymatic acetolactate oxidation to diacetyl by flavine, nicotinamide and quinone coenzymes. Biochim. Biophys. Acta 1245, 366-370.
39. Cachon, R., Daniel, S. & Diviès, C. (1995) Proton-dependent kinetics of citrate uptake in growing cells of Lactococcus lactis subsp. lactis bv. diacetylactis. FEMS Microbiol. Lett. 131, 319-323.
40. 2H-RMN en abondance naturelle. Thèse de Doctorat, Université de Nantes, France.
41. O'Leary, M. (1992) Physical and chemical basis of carbon isotope fractionation in plants. Plant Cell Environ. 15, 1099-1104.
42. Melzer, E. & Schmidt, H.-L. (1987) Carbon isotope effects on the pyruvate dehydrogenase reaction and their importance for relative carbon-13 depletion in lipids. J. Biol. Chem. 262, 8159-8164.
43. 2. Biochem. J. 252, 913-915.
44. Rinaldi, G., Meinschein, W. & Hayes, J. (1974) Intramolecular carbon isotopic distribution in biologically produced acetoin. Biomed. Mass Spectr. 1, 415-417.
45. Cachon, R. & Diviės, C. (1993) Kinetics of lactate fermentation and citrate bioconversion by Lactococcus lactis ssp. lactis in batch culture. J. Appl. Bacteriol. 75, 387-392.
46. Solem, C., Koebmann, B. & Jensen, P. (2003) Glyceraldehyde-3- phosphate dehydrogenase has no control over glycolytic flux in Lactococcus lactis MG1363. J. Bacteriol. 185, 1564-1571.
47. Lin, J., Schmitt, P. & Diviès, C. (1991) Characterisation of a citrate-negative mutant of Leuconostoc mesenteroides subsp. mesenteroides: metabolic and plasmidic properties. Appl. Microbiol. Biotechnol. 34, 628-631.