Skip to main content
PMC home page
Applied and Environmental Microbiology logoLink to Applied and Environmental Microbiology
. 1996 Jul;62(7):2577–2585. doi: 10.1128/aem.62.7.2577-2585.1996

Citrate and Sugar Cofermentation in Leuconostoc oenos, a (sup13)C Nuclear Magnetic Resonance Study

A Ramos, H Santos
PMCID: PMC1388901  PMID: 16535363

Abstract

(sup13)C nuclear magnetic resonance spectroscopy was used to investigate citrate-glucose cometabolism in nongrowing cell suspensions of the wine lactic acid bacterium Leuconostoc oenos. The use of isotopically enriched substrates allowed us to identify and quantify in the end products the carbon atoms derived from each of the substrates supplied; furthermore, it was possible to differentiate between products derived from the metabolism of endogenous carbon reserves and those derived from external substrates. Citrate-sugar cometabolism was also monitored in dilute cell suspensions for comparison with the nuclear magnetic resonance results. A clear metabolic shift of the end products from glucose metabolism was observed when citrate was provided along with glucose: ethanol was replaced by acetate, and 2,3-butanediol was produced. Reciprocally, the production of lactate and 2,3-butanediol from citrate was increased in the presence of glucose. When citrate was cometabolized with glucose, a 10-fold reduction in the intracellular concentration of glucose-6-phosphate was observed, a result in line with the observed citrate-induced stimulation of glucose consumption. The presence of citrate provided additional pathways for NADP(sup+) regeneration and allowed the diversion of sugar carbon to reactions in which ATP was synthesized. The increased growth rates and maximal biomass yields of L. oenos growing on citrate-glucose mixtures resulted from increased ATP synthesis both by substrate-level phosphorylation and by a chemiosmotic mechanism.

Full Text

The Full Text of this article is available as a PDF (354.1 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Birkhed D., Tanzer J. M. Glycogen synthesis pathway in Streptococcus mutans strain NCTC 10449S and its glycogen synthesis-defective mutant 805. Arch Oral Biol. 1979;24(1):67–73. doi: 10.1016/0003-9969(79)90177-8. [DOI] [PubMed] [Google Scholar]
  2. Cogan T. M., O'dowd M., Mellerick D. Effects of pH and Sugar on Acetoin Production from Citrate by Leuconostoc lactis. Appl Environ Microbiol. 1981 Jan;41(1):1–8. doi: 10.1128/aem.41.1.1-8.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Dicks L. M., Dellaglio F., Collins M. D. Proposal to reclassify Leuconostoc oenos as Oenococcus oeni [corrig.] gen. nov., comb. nov.. Int J Syst Bacteriol. 1995 Apr;45(2):395–397. doi: 10.1099/00207713-45-2-395. [DOI] [PubMed] [Google Scholar]
  4. Fornachon J. C. Influence of different yeasts on the growth of lactic acid bacteria in wine. J Sci Food Agric. 1968 Jul;19(7):374–378. doi: 10.1002/jsfa.2740190705. [DOI] [PubMed] [Google Scholar]
  5. Hamilton I. R. Synthesis and degradiation of intracellular polyglucose in Streptococcus salivarius. Can J Microbiol. 1968 Jan;14(1):65–77. doi: 10.1139/m68-011. [DOI] [PubMed] [Google Scholar]
  6. Kanodia S., Roberts M. F. Methanophosphagen: Unique cyclic pyrophosphate isolated from Methanobacterium thermoautotrophicum. Proc Natl Acad Sci U S A. 1983 Sep;80(17):5217–5221. doi: 10.1073/pnas.80.17.5217. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. ROGOSA M., FRANKLIN J. G., PERRY K. D. Correlation of the vitamin requirements with cultural and biochemical characters of Lactobacillus spp. J Gen Microbiol. 1961 Jul;25:473–482. doi: 10.1099/00221287-25-3-473. [DOI] [PubMed] [Google Scholar]
  8. Ramos A., Jordan K. N., Cogan T. M., Santos H. C Nuclear Magnetic Resonance Studies of Citrate and Glucose Cometabolism by Lactococcus lactis. Appl Environ Microbiol. 1994 Jun;60(6):1739–1748. doi: 10.1128/aem.60.6.1739-1748.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Ramos A., Lolkema J. S., Konings W. N., Santos H. Enzyme Basis for pH Regulation of Citrate and Pyruvate Metabolism by Leuconostoc oenos. Appl Environ Microbiol. 1995 Apr;61(4):1303–1310. doi: 10.1128/aem.61.4.1303-1310.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Ramos A., Poolman B., Santos H., Lolkema J. S., Konings W. N. Uniport of anionic citrate and proton consumption in citrate metabolism generates a proton motive force in Leuconostoc oenos. J Bacteriol. 1994 Aug;176(16):4899–4905. doi: 10.1128/jb.176.16.4899-4905.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Salou P., Loubiere P., Pareilleux A. Growth and energetics of Leuconostoc oenos during cometabolism of glucose with citrate or fructose. Appl Environ Microbiol. 1994 May;60(5):1459–1466. doi: 10.1128/aem.60.5.1459-1466.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Starrenburg M. J., Hugenholtz J. Citrate Fermentation by Lactococcus and Leuconostoc spp. Appl Environ Microbiol. 1991 Dec;57(12):3535–3540. doi: 10.1128/aem.57.12.3535-3540.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Veiga da Cunha M., Foster M. A. Sugar-glycerol cofermentations in lactobacilli: the fate of lactate. J Bacteriol. 1992 Feb;174(3):1013–1019. doi: 10.1128/jb.174.3.1013-1019.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Veiga-Da-Cunha M., Firme P., Romão M. V., Santos H. Application of C Nuclear Magnetic Resonance To Elucidate the Unexpected Biosynthesis of Erythritol by Leuconostoc oenos. Appl Environ Microbiol. 1992 Jul;58(7):2271–2279. doi: 10.1128/aem.58.7.2271-2279.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Veiga-da-Cunha M., Santos H., Van Schaftingen E. Pathway and regulation of erythritol formation in Leuconostoc oenos. J Bacteriol. 1993 Jul;175(13):3941–3948. doi: 10.1128/jb.175.13.3941-3948.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Applied and Environmental Microbiology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES