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A mathematical model of the link between growth and L-malic acid consumption for five strains of Oenococcus oeni

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Abstract

In winemaking, after the alcoholic fermentation of red wines and some white wines, L-malic acid must be converted into L-lactic acid to reduce the acidity. This malolactic fermentation (MLF) is usually carried out by the lactic acid bacteria Oenococcus oeni. Depending on the level of process control, selected O. oeni is inoculated or the natural microbiota of the cellar is used. This study considers the link between growth and MLF for five strains of O. oeni species. The kinetics of growth and L-malic acid consumption were followed in modified MRS medium (20 °C, pH 3.5, and 10 % ethanol) in anaerobic conditions. A large variability was found among the strains for both their growth and their consumption of L-malic acid. There was no direct link between biomass productivities and consumption of L-malic acid among strains but there was a link of proportionality between the specific growth of a strain and its specific consumption of L-malic acid. Experiments with and without malic acid clearly demonstrated that malic acid consumption improved the growth of strains. This link was quantified by a mathematical model comparing the intrinsic malic acid consumption capacity of the strains.

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References

  • Alberto MR, Farias ME, Manca de Nadra MC (2001) Effect of gallic acid and catechin on Lactobacillus hilgardii 5w growth and metabolism of organic compounds. J Agric Food Chem 49:4359–4363

    Article  CAS  Google Scholar 

  • Armada L, Fernández E, Falqué E (2010) Influence of several enzymatic treatments on aromatic composition of white wines. Food Sci Technol 43:1517–1525

    CAS  Google Scholar 

  • Arnink K, Henick-Kling T (2005) Influence of Saccharomyces cerevisiae and Oenococcus oeni strains on successful malolactic conversion in wine. AM J Enol Vitic 56:228–237

    CAS  Google Scholar 

  • Asmundson RV, Kelly WJ (1990) Proceedings of the seventh Australian wine industry technical conference. In: Williams PJ, Davidson D, Lee TH (eds), 14–16 August 1989, S.A Winetitles, Adelaide, p 251–252

  • Augagneur Y, Ritt JFM, Linares D, Remize F, Tourdot-Maréchal R, Garmyn D, Guzzo J (2007) Dual effect of organic acids as a function of external pH in Oenococcus oeni. Arch Microbiol 188:147–157

    Article  CAS  Google Scholar 

  • Borneman AR, Bartowsky EJ, McCarthy J, Chambers PJ (2010) Genotypic diversity in Oenococcus oeni by high-density microarray comparative genome hybridization and whole genome sequencing. Appl Microbiol Biotechnol 86:681–691

    Article  CAS  Google Scholar 

  • Bravo-Ferrada BM, Delfederico L, Hollmann A, Valdés La Hens D, Curilén Y, Caballero A, Semorile L (2011) Oenococcus oeni from patagonian red wines: isolation, characterization and technological properties. Int J Microbiol Res 3(1):48–55

    Article  CAS  Google Scholar 

  • Carreté R, Vidal MT, Bordons A, Constanti M (2002) Inhibitory effect of sulphur dioxide and other stress compounds in wine on the ATPase activity of Oenococcus oeni. FEMS Microbiol Lett 211:155–159

    Article  Google Scholar 

  • González-Arenzana L, Santamaría P, López R, Tenorio C, López-Alfaro I (2012) Ecology of indigenous lactic acid bacteria along different winemaking processes of tempranillo red wine from la Rioja (spain). Sci. world J. doi:10.1100/2012/796327

    Google Scholar 

  • Guerrini S, Bastianinia A, Blaiottab G, Granchia L, Moschettib G, Coppolab S, Romano P, Vincenzini M (2002a) Phenotypic and genotypic characterization of Oenococcus oeni strains isolated from Italian wines. Int J Food Microbiol 83:1–14

    Article  Google Scholar 

  • Guerrini S, Bastianini A, Granchi L, Vincenzini M (2002b) Effect of oleic acid on Oenococcus oeni strains and malolactic fermentation in wine. Curr Microbiol 44:5–9

    Article  CAS  Google Scholar 

  • Guilloux-Benatier M, Le Fur Y, Feuillat M (1998) Influence of fatty acids on the growth of wine microorganisms Saccharomyces cerevisiae and Oenococcus oeni. J Ind Microbiol Biotech 20:144–149

    Article  CAS  Google Scholar 

  • Guzzo J, Jobin MP, Delmas F, Fortier LC, Garmyn D, Tourdot-Maréchal R, Lee B, Diviès C (2000) Regulation of stress response in Oenococcus oeni as a function of environmental changes and growth phase. Int J Food Microbiol 55:27–31

    Article  CAS  Google Scholar 

  • Guzzo J, Coucheney F, Pierre F, Fortier LC, Delmas F, Diviès C, Tourdot-Maréchal R (2002) Acidophilic behaviour of the malolactic bacterium Oenococcus oeni. Int J Food Sci Technol 22:107–111

    CAS  Google Scholar 

  • Henick-Kling T (1990) pH and regulation of malolactic activity in Leuconostoc oenos. In: Actualités Œnologiques 89. in Comptes rendus du 4e Symposium International d’Œnologie (Bordeaux, 1989), Actualités Œnologiques 89, Institut d’Œnologie Université de Bordeaux II. Dunod, Paris, p 320–325

  • Henick-Kling T, Park YH (1994) Consideration for the use of yeast and bacterial starter cultures: SO2 and timing of inoculation. AM J Enol Vitic 45:464–469

    Google Scholar 

  • Ingram LO, Butke T (1984) Effects of alcohols on microorganisms. Adv Microb Physiol 25:254–290

    Google Scholar 

  • King SW, Beelman RB (1986) Metabolic interactions between Saccharomyces cerevisiae and Leuconostoc œnos in a model grape juice/wine system. AM J Enol Vitic 37:53–60

    CAS  Google Scholar 

  • Knoll C, Divol B, Du Toit M (2008) Genetic screening of lactic acid bacteria of œnological origin for bacteriocin-encoding genes. Food Microbiol 25:983–991

    Article  CAS  Google Scholar 

  • Kroll RG, Booth IR (1983) The relationships between intracellular pH, the pH gradient and potassium transport in Escherichia coli. Biochem J 216:709–716

    CAS  Google Scholar 

  • Kunkee RE (1967) Malolactic fermentation. Adv Appl Microbiol 9:235–279

    Article  CAS  Google Scholar 

  • Kunkee RE (1974) Malolactic fermentation and winemaking. Adv Chem Ser 137:151–170

    Article  CAS  Google Scholar 

  • Lechiancole T, Blaiotta G, Messina D, Fusco V, Villani F, Salzano G (2006) Evaluation of intra-specific diversities in Oenococcus oeni through analysis of genomic and expressed DNA. Syst Appl Microbiol 29:375–381

    Article  CAS  Google Scholar 

  • Lerm E, Engelbrecht L, Du Toit M (2010) Malolactic fermentation: the ABC’s of MLF. Afr J Enol Vitic 31:186–212

    CAS  Google Scholar 

  • Maicas S, Pardo I, Ferrer S (2000) The effects of freezing and freeze-drying of Oenococcus oeni upon induction of malolactic fermentation in red wine. Int J Food Sci Technol 35:75–79P

    Article  CAS  Google Scholar 

  • Nehme N, Mathieu F, Taillandier P (2008) Quantitative study of interactions between Saccharomyces cerevisiae and Oenococcus oeni strains. J Ind Microbiol Biotechnol 35:685–693

    Article  CAS  Google Scholar 

  • Nehme N, Mathieu F, Taillandier P (2010) Impact of the co-culture of Saccharomyces cerevisiae–Oenococcus oeni on malolactic fermentation and partial characterization of a yeast-derived inhibitory peptidic fraction. Food Microbiol 27:150–157

    Article  CAS  Google Scholar 

  • Olguin NT (2010) Molecular study of the mechanisms of Oenococcus oeni involved in its adaptation to wine conditions and in the development of malolactic fermentation. PhD Thesis, Universitat Rovira I Virgili, Tarragona, Spain

  • Osborne JP, Dube Mornea A, Mira de Ordu R (2006) Degradation of free and sulphur dioxide-bound acetaldehyde by malolactic lactic acid bacteria in white wine. J Appl Microbiol 02947:1365–2672

    Google Scholar 

  • Poolman B, Molenaar D, Smid EJ, Ubbink T, Abbe T, Renault PP, Konings WN (1991) Malolactic fermentation: electrogenic malate uptake and malate/lactate antiport generate metabolic energy. J Bacteriol 173:6030–6037

    CAS  Google Scholar 

  • Rankine BC (1977) Developments in malolactic fermentation of Australian red table wines. AM J Enol Vitic 28:27–33

    CAS  Google Scholar 

  • Reguant C, Bordons A, Arola L, Rozes N (2000) Influence of phenolic compounds on the physiology of Oenococcus oeni from wine. J Appl Microbiol 88:1065–1071

    Article  CAS  Google Scholar 

  • Remize F, Gaudin A, Kong Y, Guzzo J, Alexandre H, Krieger S, Guilloux-Benatier M (2006) Oenococcus oeni preference for peptides: qualitative and quantitative analysis of nitrogen assimilation. Arch Microbiol 185:459–469

    Article  CAS  Google Scholar 

  • Rivas B, Marcobal Á, Munoz R (2004) Allelic diversity and population structure in Oenococcus oeni as determined from sequence analysis of housekeeping genes. Appl Environ Microbiol 70:7210–7219

    Article  Google Scholar 

  • Romano P, Suzzi G (1993) Sulphur dioxide and wine microorganisms. In: Fleet GH (ed) Wine microbiology and biotechnology. Harwood Academic Publishers, Chur, Switzerland, pp 373–393

    Google Scholar 

  • Rosa F, Sa-Correia I (1992) Ethanol tolerance and activity of plasma membrane ATPase in kluyveromyces marxianus and Saccharomyces cerevisiae. Enzym Microbial Technol 14:23–27

    Article  CAS  Google Scholar 

  • Ruiz P, Izquierdo PM, Seseña S, Palop ML (2009) Analysis of lactic acid bacteria populations during spontaneous malolactic fermentation of Tempranillo wines at five wineries during two consecutive vintages. Food Control 21(1):70–75

    Article  Google Scholar 

  • Saguir FM, Manca de Nadra MC (1997) Growth and metabolism of Leuconostoc œnos in synthetic media. Microbiol Aliment Nutr 15:131–138

    CAS  Google Scholar 

  • Saguir FM, Compos IEL, Manca de Nadra MC (2009) Identification of dominant lactic acid bacteria isolated from grape juices. Assessment of its biochemical activities relevant to flavor development in wine. Int J Wine Res 1:175–185

    CAS  Google Scholar 

  • Salema M, Poolman B, Lolkema JS, Loureiro Dias MC, Konings WN (1994) Uniport of monoanionic L-malate in membrane vesicles from Leuconostoc oenos. Eur J Biochem 225:289–295

    Article  CAS  Google Scholar 

  • Swinnen IAM, Bernaerts K, Dens EJJ, Geeraerd AH, Van Impe JF (2004) Predictive modelling of the microbial lag phase: a review. Int J Food Microbiol 94:137–159

    Article  CAS  Google Scholar 

  • Taillandier P, Tataridis P, Strehaiano P (2002) Quantitative study of antagonism between Saccharomyces cerevisiae and Oenococcus oeni. In: Lallemand technical meetings symposium, Biarritz vol 10, p 21–26

  • Ugliano M, Genovese A, Moio L (2003) Hydrolysis of wine aroma precursors during malolactic fermentation with four commercial starter cultures of Oenococcus oeni. J Agric Food Chem 51:5073–5078

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The study was conducted within the framework of the ANR programme DIVOENI biodiversity no. ANR-07 BDIV 011-01. We thank all partners for providing strains of the Oenococcus Collection.

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Authors and Affiliations

  1. Laboratoire de Génie Chimique, Université de Toulouse, INPT, UPS, 4, Allée Emile Monso, BP 83234, 31432, Toulouse Cedex 4, France

    N. Fahimi, C. Brandam & P. Taillandier

  2. Laboratoire de Génie Chimique, CNRS, 31030, Toulouse, France

    N. Fahimi, C. Brandam & P. Taillandier

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  1. N. Fahimi
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  2. C. Brandam
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  3. P. Taillandier
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Correspondence to N. Fahimi.

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Fahimi, N., Brandam, C. & Taillandier, P. A mathematical model of the link between growth and L-malic acid consumption for five strains of Oenococcus oeni . World J Microbiol Biotechnol 30, 3163–3172 (2014). https://doi.org/10.1007/s11274-014-1743-8

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  • DOI: https://doi.org/10.1007/s11274-014-1743-8

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