Skip to main content
SpringerLink
Log in

Physiology of pyruvate metabolism in Lactococcus lactis

  • Metabolism
  • Published:
Antonie van Leeuwenhoek Aims and scope Submit manuscript

Abstract

Lactococcus lactis, a homofermentative lactic acid bacterium, has been studied extensively over several decades to obtain sometimes conflicting concepts relating to the growth behaviour. In this review some of the data will be examined with respect to pyruvate metabolism. It will be demonstrated that the metabolic transformation of pyruvate can be predicted if the growth-limiting constraints are adequately established. In general lactate remains the major product under conditions in which sugar metabolism via a homolactic fermentation can satisfy the energy requirements necessary to assimilate anabolic substrates from the medium. In contrast, alternative pathways are involved when this energy supply becomes limiting or when the normal pathways can no longer maintain balanced carbon flux. Pyruvate occupies an important position within the metabolic network of L. lactis and the control of pyruvate distribution within the various pathways is subject to co-ordinated regulation by both gene expression mechanisms and allosteric modulation of enzyme activity.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Abbe K, Takahashi S & Yamada T (1982) Involvement of oxygensensitive pyruvate formate-lyase in mixed acid fermentation by Streptococcus mutans under strictly anaerobic conditions. J. Bacteriol. 152: 175–182

    Google Scholar 

  • Archibald FS & Fridovich I (1981a) Manganese and defenses against oxygen toxicity in Lactobacillus plantarum. J. Bacteriol. 145: 442–451

    Google Scholar 

  • (1981b) Manganese, superoxide dismutase, and oxygen tolerance in some lactic acid bacteria. J. Bacteriol. 146: 928–936

    Google Scholar 

  • Benson KH, Godon JJ, Renault P, Griffin HG & Gasson MJ (1996) Effect of ilvBN-encoded a-acetolactate synthase expression on diacetyl production in Lactococcus lactis. Appl. Microbiology Biotechnol. 45: 107–111

    Google Scholar 

  • Benthin S, Nielsen J & Villadsen J (1993) Two uptake systems for fructose in Lactococcus lactis subsp cremoris FD1 produce glycolytic and gluconeogenic fructose phosphates and induce oscillations in growth and lactic acid formation. Appl. Env. Microbiol. 59: 3206–3211

    Google Scholar 

  • Bisset DL & Anderson RL (1974) Lactose and D-galactose metabolism in group N Streptococci: presence of enzymes for both the D-galactose 1-phosphate and D-tagatose 6-phosphate pathways hydrolysing enzymes in Streptococcus lactis and Streptococcus cremoris and also in some species of Streptococci. J. Bacteriol. 117: 318–320

    Google Scholar 

  • Cancilla MR, Davidson BE, Hillicr AJ, Nguyen NY & Thompson J (1995) The Lactococcus lactis triosephosphate isomerase gene, tpi, is monocistronic. Microbiology 141: 229–238

    Google Scholar 

  • Cocaign-Bousquet M, Garrigues C, Novak L, Lindley ND & Loubiere P (1995) Rational development of a simple synthetic medium for the sustained growth of Lactococcus lactis. J. Appl. Bacteriol. 79: 108–116

    Google Scholar 

  • Cogan TM (1981) Constitutive nature of the enzymes of citrate metabolism in Streptococcus lactis subsp diacetylactis. J. Dairy Res. 48: 489–495

    Google Scholar 

  • Cogan JF, Walsh D & Condon S (1989) Impact of aeration on the metabolic end-products formed from glucose and galactose by Streptococcus lactis. J. Appl. Bacteriol. 66: 77–84

    Google Scholar 

  • Collins LB & Thomas TD (1974) Pyruvate kinase of Streptococcus lactis. J. Bacteriol. 120: 52–58

    Google Scholar 

  • Condon S (1987) Responses of lactic acid bacteria to oxygen. FEMS Microbiol. Rev. 46: 269–280

    Google Scholar 

  • Cook GM & Russell JB (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 

  • Crow VL (1990) Properties of 2,3-butanediol dehydrogenases from Lactococcus lactis subsp lactis in relation to citrate fermentation. Appl. Environ. Microbiol. 56: 1656–1665

    Google Scholar 

  • Crow VL & Wittenberger CL (1979) Separation and properties of NAD+ and NADP+-dependent glyceraldehyde-3-phosphate dehydrogenases from Streptococcus mutans. J. Biol. Chem. 254: 1134–1142

    Google Scholar 

  • Crow VL & Thomas TD (1982) D-tagatose 1,6-diphosphate aldolase from lactic Streptococci: purification, properties, and use in measuring intracellular tagatose 1,6-diphosphate. J. Bacteriol. 151: 600–608

    Google Scholar 

  • (1984) Properties of a Streptococcus lactis strain that ferments lactose slowly. J. Bacteriol. 157: 28–34

    Google Scholar 

  • Crow VL, Davey GP, Pearce LE & Thomas TD (1983) Plasmid linkage of the D-tagatose-6 phosphate pathway in Streptococcus lactis: Effect on lactose and galactose metabolism. J. Bacteriol. 153: 76–83

    Google Scholar 

  • Demko GM, Blanton SJB & Benoit RE (1972) Heterofermentative carbohydrate metabolism of lactose-impaired mutants of Streptococcus lactis. J. Bacteriol. 112: 1335–1345

    Google Scholar 

  • Drinan DF, Tobin S & Cogan TM (1976) Citric acid metabolism in hetero- and homofermentative lactic acid bacteria. Appl. Environ. Microbiol. 31: 481–486

    Google Scholar 

  • Eggeling I, Cordes C, Eggeling L & Sahm H (1987) Regulation of acetohydroxy-acid synthase in Corynebacterium glutamicum during fermentation of a-ketobutyrate to L-isoleucine. Appl. Microbiol. Biotechnol. 25: 346–351

    Google Scholar 

  • Farrow JAE (1980) Lactose hydrolysing enzymes in Streptococcus lactis and Streptococcus cremoris and also in some other species of Streptococci. J. Appl. Bacteriol. 49: 493–503

    Google Scholar 

  • Godon JJ (1992) Regulation génétique de la synthèse des acides aminés branchés chez Lactococcus lactis. Thèse, Université Paris XI

  • Godon JJ, Chopin MC & Ehrlich SD (1992) Branched-chain amino acid biosynthesis genes in Lactococcus lactis subsp lactis. J. Bacteriol. 174: 6580–6589

    Google Scholar 

  • Grufferty RC & Condon S (1983) Effect of fermentation sugar on hydrogen peroxide accumulation by Streptococcus lactis C10. J. Dairy Res. 50: 481–489

    Google Scholar 

  • Hanson L & Haggstrom HM (1984) Effects of growth conditions on the activities of superoxide dismutase and NADH-oxidase/NADH-peroxidase in Streptococcus lactis. Curr. Microbiol. 10: 345–352

    Google Scholar 

  • Higuchi M, Shimada M, Yamamoto Y, Hayashi T, Koga T & Kamio Y (1993) Identification of two distinct NADH oxidases corresponding to H2O2-forming oxidase induced in Streptococcus mutans. J Gen. Microbiol. 139: 2343–2351

    Google Scholar 

  • Hugenholtz J & Starrenburg MJC (1992) Diacetyl production by different strains of Lactococcus lactis subsp lactis var diacetylactis and Leuconostoc spp. Appl. Microbiol. Biotechnol. 38: 17–22

    Google Scholar 

  • Hugenholtz J, Starrenburg MJC & Weerkamp AH (1994) Diacetyl production by Lactococcus lactis: optimilisation and metabolic engineering. In: ECB6 Proceedings of the 6th European Congress on Biotechnology (Eds.), L Alberghina, L Frontali & P Sensi. Elsevier Science B.V., Amsterdam, Netherlands

    Google Scholar 

  • Ishizaki A, Ueda T, Tanaka K & Stanbury PF (1992) L-Lactate production from xylose employing Lactococcus lactis IO-1. Biotech. Lett. 14: 599–604

    Google Scholar 

  • Jordan KN & Cogan TM (1988) Production of acetolactate by Streptococcus diacetylactis and Leuconostoc ssp. J. Dairy Res. 55: 227–238

    Google Scholar 

  • Kandler O (1983) Carbohydrate metabolism in lactic acid bacteria. Antonie van Leeuwenhoek 49: 209–224

    Google Scholar 

  • Kaneko T, Watanabe Y & Suzuki H (1989) Enhancement of diacetyl production by a diacetyl-resistant mutant of citrate-positive Lactococcus lactis subsp. lactis 3022 and by aerobic conditions of growth. J. Dairy Sci. 73: 291–298

    Google Scholar 

  • Kaneko T, Takahashi M & Suzuki H (1990) Acetoin fermentation by citrate-positive Lactococcus lactis subsp. lactis 3022 grown aerobically in the presence of hemin or Cu2+. Appl. Environ. Microbiol. 56: 2644–2649

    Google Scholar 

  • Kaneko T, Watanabe Y & Suzuki H (1991) Differences between Lactobacillus casei 2206 and citrate-positive Lactococcus lactis subsp. lactis 3022 in the characteristics of diacetyl production. Appl. Env. Microbiol. 57: 3040–3042

    Google Scholar 

  • Kell DB & Westerhoff HV (1986) Metabolic control theory: its role in microbiology and biotechnology. FEMS Microbiol. Rev. 39: 305–320

    Google Scholar 

  • Knappe J & Sawers G (1990) A radical-chemical route to acetyl-CoA: the anaerobically induced pyruvate formate-lyase system of Escherichia coli. FEMS Microbiol. Rev. 75: 383–398

    Google Scholar 

  • Konings WN, Poolman B & Driessen AJM (1989) Bioenergetics and solute transport in Lactococci. CRC Crit. Rev. Microbiol. 16: 419–475

    Google Scholar 

  • LeBlanc DJ, Crow VL, Lee LN & Garon CF (1979) Influence of the lactose plasmid on the metabolism of galactose by Streptococcus lactis. J. Bacteriol. 137: 878–884

    Google Scholar 

  • Llanos RM, Hillier A & Davidson BE (1992) Cloning, nucleotide sequence, expression and chromosomal location of ldh, the gene encoding L-Lactate dehydrogenase, from Lactococcus lactis. J. Bacteriol. 174: 6956–6964

    Google Scholar 

  • Llanos RM, Harris CJ, Hillier AJ & Davidson BE (1993) Identification of a novel operon in Lactococcus lactis encoding three enzymes for lactic acid synthesis: phosphofructokinase, pyruvate kinase, and lactate dehydrogenase. J. Bacteriol. 175: 2541–2551

    Google Scholar 

  • Lohmeier-Vogel EM, Hahn-Hagerdahl B, & Vogel HJ (1986) Phosphorus-31 NMR studies of maltose and glucose metabolism in Streptococcus lactis. Appl. Microbiol. Biotechnol. 25: 43–51

    Google Scholar 

  • Loubiere P, Novak L, Cocaign-Bousquet M & Lindley ND (1996) Besoins nutritionnels des bacteries lactiques: interactions entre flux de carbone et d'azote. Lait 76, (in press)

  • Marugg JD, Goelling D, Stahl U, Ledeboer AM, Toonen MY, Verhue WM & Verrips CT (1994) Identification and caracterization of the a-acetolactate synthase gene from Lactococcus lactis subsp lactis biovar diacetylactis. Appl. Env. Microbiol. 60: 1390–1394

    Google Scholar 

  • McKay LL, Baldwin KA & Zottola EA (1972) Loss of lactose metabolism in lactic Streptococci. Appl. Microbiol. 23: 1090–1096

    Google Scholar 

  • Monnet C, Phalip V, Schmitt P & Divies C (1994) Comparison of a-acetolactate decarboxylase in Lactococcus spp and Leuconostoc spp. Biotech. Lett. 16: 257–262

    Google Scholar 

  • Phalip V, Monnet C, Schmitt P, Renault P, Godon JJ & Divies C (1994) Purification and properties of the a-acetolactate decaboxylase from Lactococcus lactis subsp lactis NCDO 2118. FEBS Lett. 351: 95–99

    Google Scholar 

  • Platteeuw C, Hugenholtz J, Starrenburg M, van Alen-Boerrigter I & de Vos WM (1995) Metabolic engineering of Lactococcus lactis: influence of the overproduction of a-acetolactate synthase in strains deficient in lactate dehydrogenase as a function of culture conditions. Appl. Environ. Microbiol. 61: 3967–3971

    Google Scholar 

  • Poolman B (1993) Energy transduction in lactic acid bacteria. FEMS Microbiol. Rev. 12: 125–148

    Google Scholar 

  • Poolman B, Bosman B, Kiers J & Konings WN (1987a) Control of glycolysis by glyceraldehyde-3-phosphate dehydrogenase in Streptococcus cremoris and Streptococcus lactis. J. Bacteriol. 169: 5887–5890

    Google Scholar 

  • Poolman B, Driessen AJM & Konings WN (1987b) Regulation of solute transport in streptococci by external and internal pH values. Microbiol. Rev. 51: 498–508

    Google Scholar 

  • Qian N, Stanley GA, Hahn-Hagerdal B & Radstrom P (1994) Purification and characterisation of two phosphoglucomutases from Lactococcus lactis subsp lactis and their regulation in maltose and glucose utilizing cells. J. Bacteriol. 176: 5304–5311

    Google Scholar 

  • Ramos A, Jordan KN, Cogan TM & Santos H (1994) 13C nuclear magnetic resonance studies of citrate and glucose cometabolism by Lactococcus lactis. Appl. Environ. Microbiol. 60: 1739–1748

    Google Scholar 

  • Romano AH, Brino G, Peterkofsky A & Reizer J (1987) Regulation of b-galactoside transport and accumulation in heterofermentative lactic acid bacteria. J. Bacteriol. 169: 5589–5596

    Google Scholar 

  • Saier MH, Chaivaix S, Cook GM, Deutscher J, Reizer J & Ye GJJ (1996) Catabolite repression and inducer control in Gram-positive bacteria. Microbiology 142: 217–230

    Google Scholar 

  • Sedewotz B, Schleifer KH & Gotz F (1984a) Purification and biochemical characterization of pyruvate oxidase from Lactobacillus plantarum. J. Bacteriol. 160: 273–278

    Google Scholar 

  • Sedewitz B, Schleifer KH & Gotz F (1984b) Physiological role of pyruvate oxidase in aerobic metabolism of Lactobacillus plantarum. J. Bacteriol. 160: 462–465

    Google Scholar 

  • Sesma F, Gardiol D, De Ruiz Holgado AP & De Mendoza D (1990) Cloning of the citrate permease gene of Lactococcus lactis subsp. lactis biovar diacetylactis and expression in Escherichia coli. Appl. Environ. Microbiol. 56: 2099–2103

    Google Scholar 

  • Shaw K & Berg CM (1980) Substrate channeling: a-ketobutyrate inhibition of acetohydroxy acid synthase in Salmonella typhimurium. J. Bacteriol. 143: 1509–1512

    Google Scholar 

  • Sjoberg A. & Hahn-Hagerdal B (1989) b-glucose-1-phosphate, a possible mediator for polysaccharide formation in maltose-assimilating Lactococcus lactis. Appl. Env. Microbiol. 55: 1549–1554

    Google Scholar 

  • Smart JB & Thomas TD (1987) Effect of oxygen on lactose metabolism in Lactic Streptococci. Appl. Env. Microbiol. 53: 533–541

    Google Scholar 

  • Smith MR, Hugenholtz J, Mikoczi P, Ree E, Bunch AW & Bont JAM (1992) The stability of the lactose and citrate plasmids in Lactococcus lactis biovar. diacetylactis. FEMS Microbiol. Lett. 96: 7–12

    Google Scholar 

  • Snoep JL, Teixeira de Mattos MJ, Postma PW & Neijssel OM (1990) Involvement of pyruvate dehydrogenase in product formation in pyruvate-limited anaerobic chemostat cultures of Enterococcus faecalis NCTC 775. Arch. Microbiol. 154: 50–55

    Google Scholar 

  • (1991) Effect of the energy source on the NADH/NAD ratio and on pyruvate catabolism in anaerobic chemostat cultures of Enterococcus faecalis NCTC 775. FEMS Microbiol. Lett. 81: 63–66

    Google Scholar 

  • Snoep JL, Teixeira de Mattos MJ, Starrenburg MJC & Hugenholtz J (1992a) Isolation, characterization, and physiological role of the pyruvate dehydrogenase complex and a-acetolactate synthase of Lactococcus lactis subsp. lactis bv diacetylactis. J. Bacteriol. 174: 4838–4841

    Google Scholar 

  • Snoep JL, De Graef MR, Westphal AH, De Kok A, Teixeira de Mattos MJ & Neijssel OM (1992b) Pyruvate catabolism during transient state conditions in chemostat cultures of Enterococcus faecalis NCTC 775: importance of internal pyruvate concentrations and NADH/NAD+ ratios. J Gen. Microbiol. 138: 2015–2020

    Google Scholar 

  • (1993a) Differences in sensitivity to NADH of purified pyruvate dehydrogenase complexes of Enterococcus faecalis, Lactococcus lactis, Azotobacter vinelandii and Escherichia coli: implications for their activity in vivo. FEMS Microbiol. Lett. 114: 279–284

    Google Scholar 

  • Snoep JL, Van Bommel M, Lubbers F, Teixeira de Mattos MJ & Neijssel OM (1993b) The role of lipoic acid in product formation by Enterococcus faecalis NCTC 775 and reconstitution in vivo and in vitro of the pyruvate dehydrogenase complex. J Gen. Microbiol. 139: 1325–1329

    Google Scholar 

  • Starrenburg MJC & Hugenholtz J (1991) Citrate fermentation by Lactococcus and Leuconostoc spp. Appl. Env. Microbiol. 57: 3535–3540

    Google Scholar 

  • Swomdell SR, Griffin HG & Gasson J (1994) Cloning, sequencing and comparison of three lactococcal L-lactate dehydrogenase genes. Microbiol. 140: 1301–1305

    Google Scholar 

  • Takahashi S, Abbe K & Yamada T (1982) Purification of pyruvate formate-lyase from Streptococcus mutans and its regulatory properties. J. Bacteriol. 149: 1034–1040

    Google Scholar 

  • Thomas TD (1976a) Activator specificity of pyruvate kinase from lactic Streptococci J. Bacteriol. 125: 1240–1242

    Google Scholar 

  • (1976b) Regulation of lactose fermentation in group N Streptococci. Appl. Env. Microbiol. 32: 474–478

    Google Scholar 

  • Thomas TD, Ellwood DC & Longyear MC (1979) Change from homo-to heterolactic fermentation by Streptococcus lactis resulting from glucose limitation in anaerobic chemostat cultures. J. Bacteriol. 138: 109–117

    Google Scholar 

  • Thomas TD, Turner KW & Crow VL (1980) Galactose fermentation by Streptococcus lactis and Streptococcus cremoris: pathways, products, and regulation. J. Bacteriol. 144: 672–682

    Google Scholar 

  • Thompson J (1978) In vivo regulation of glycolysis and characterisation of sugar: phosphotransferase systems in Streptococcus lactis. J. Bacteriol. 136: 465–476

    Google Scholar 

  • (1979) Lactose metabolism in Streptococcus lactis: phosphorylation of galactose and glucose moieties in vivo. J. Bacteriol. 140: 774–785

    Google Scholar 

  • (1980) Galactose transport systems in Streptococcus lactis. J. Bacteriol. 144: 683–691

    Google Scholar 

  • Thompson J & Torchia DA (1984) Use of 31P nuclear magnetic resonance spectroscopy and 14C fluorography in studies of glycolysis and regulation of pyruvate kinase in Streptococcus lactis. J. Bacteriol. 158: 791–800

    Google Scholar 

  • Thompson J, Chassy BM & Egan W (1985) Lactose metabolism in Streptococcus lactis: studies with a mutant lacking glucokinase and mannose-phosphotransferase activities. J. Bacteriol. 162: 217–223

    Google Scholar 

  • Thompson J & Gentry-Weeks CR (1994) Mtabolisme des sucres par les bactries Lactiques. In: Bactries lactiques, Vol 1. (Eds.), De Roissart H et Luquet, FM Lorica, Uriage. pp 239–290

    Google Scholar 

  • Verhue WM & Tjan FSB (1991) Study of the citrate metabolism of Lactococcus lactis subsp lactis biovar diacetylactis by means of 13C nuclear magnetic resonance. Appl. Environ. Microbiol. 57: 3371–3377

    Google Scholar 

  • Veyrat A, Monedero V & Perez-Martinez G (1994) Glucose transport by the phosphoenolpyruvate: mannose phosphotransferase system in Lactobacillus casei ATCC 393 and its role in carbon catabolite repression. Microbiology 140: 1141–1149

    Google Scholar 

  • Westby A, Nuraida L, Owens JD & Gibbs PA (1993) Inability of Lactobacillus plantarum and other lactic acid bacteria to grow on D-ribose as sole source of fermentable carbohydrate. J. Appl. Bacteriol. 75: 168–175

    Google Scholar 

  • Yamada T (1987) Regulation of glycolysis in Streptococci. In: Sugar Transport and Metabolism in Gram-Positive Bacteria. (eds.), J. Reizer and A. Peterkofsky. Ellis Howood Series in Biochemistry and Biotechnology. pp 69–93

  • Ye JJ, Reizer J & Saier MH (1994) Regulation of deoxyglucose phosphate accumulation in Lactococcus lactis vesicles by metabolite activated, ATP-dependent phosphorylation of serine-46 in HPr of the phosphotransferase system. Microbiology 140: 3421–3429

    Google Scholar 

  • Zitzelberger W, Gotz F & Schleifer KH (1984) Distribution of superoxide dismutases, oxidases, and NADH peroxidases in various Streptococci. FEMS Microbiol. Lett. 21: 243–246

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Centre de Bioingnierie Gilbert Durand, UMR CNRS & Lab Ass INRA, Institut National des Sciences Appliques, Complexe Scientifique de Rangueil, 31077, Toulouse cedex, France

    Muriel Cocaign-Bousquet, Christel Garrigues, Pascal Loubiere & Nicolas D. Lindley

Authors
  1. Muriel Cocaign-Bousquet
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Christel Garrigues
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Pascal Loubiere
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Nicolas D. Lindley
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cocaign-Bousquet, M., Garrigues, C., Loubiere, P. et al. Physiology of pyruvate metabolism in Lactococcus lactis . Antonie van Leeuwenhoek 70, 253–267 (1996). https://doi.org/10.1007/BF00395936

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00395936

Key words

Search

Navigation