Food and Bioprocess Technology

, Volume 4, Issue 6, pp 876–906 | Cite as

Lactobacillus: the Next Generation of Malolactic Fermentation Starter Cultures—an Overview

  • Maret du Toit
  • Lynn Engelbrecht
  • Elda Lerm
  • Sibylle Krieger-Weber
Review Paper

Abstract

Malolactic fermentation (MLF) is a secondary wine fermentation conducted by lactic acid bacteria (LAB). This fermentation is important in winemaking as it deacidifies the wine, it contributes to microbial stability and lastly it contributes to wine aroma through the production of metabolites. Oenococcus oeni is the main species used in commercially available starter culture currently, but research has indicated that different Lactobacillus species also partake in MLF and this has shifted the focus in the MLF field to evaluate the potential of lactobacilli as starter cultures for the future. There are 17 different species of Lactobacillus associated with winemaking either being associated with the grapes/beginning of alcoholic fermentation or the MLF and wine. Lactobacillus associated with wine is mainly facultative or obligatory heterofermentative and can withstand the harsh wine conditions such as high ethanol levels, low pH and temperatures and sulphur dioxide. Wine lactobacilli contain the malolactic enzyme encoding gene, but sequence homology shows that it clusters separate from O. oeni. Lactobacillus also possesses more enzyme encoding genes compared to O. oeni, important for the production of wine aroma compounds such as glycosidase, protease, esterase, phenolic acid decarboxylase and citrate lyase. Another characteristic associated with wine lactobacilli is the production of bacteriocins, especially plantaricins which would enable them to combat spoilage LAB. All these characteristics, together with their ability to conduct MLF just as efficiently as O. oeni, make them suitable for a new generation of MLF starter cultures.

Keywords

Lactobacillus Wine Malolactic fermentation Starter cultures Metabolism 

References

  1. Alberto, M. R., Arena, M. E., & Manca de Nadra, M. C. (2007). Putrescine production from agmatine by Lactobacillus hilgardii: Effect of phenolic compounds. Food Control, 18, 898–903.CrossRefGoogle Scholar
  2. Alexandre, H., Costello, P. J., Remize, F., Guzzo, J., & Guillox-Benatier, M. (2004). Saccharomyces cerevisiaeOenococcus oeni interactions in wine: Current knowledge and perspectives. International Journal of Food Microbiology, 93, 141–154.CrossRefGoogle Scholar
  3. Amerine, M. A., & Kunkee, R. E. (1968). Microbiology of winemaking. Annual Review of Microbiology, 22, 323–358.CrossRefGoogle Scholar
  4. Amerine, M. A., & Ough, C. S. (1980). Methods of analysis of musts and wines. New York: Wiley.Google Scholar
  5. Amoroso, M. J., Saguir, F. M., & Manca de Nadra, M. C. (1993). Variation of nutritional requirements of Leuconostoc oenos by organic acids. Journal International des Sciences de la Vigne et du Vin, 27, 135–144.Google Scholar
  6. Araque, I., Gil, J., Carreté, R., Bordons, A., & Reguant, C. (2009). Detection of arc genes related with the ethyl carbamate precursors in wine lactic acid bacteria. Journal of Agricultural and Food Chemistry, 57, 1841–1847.CrossRefGoogle Scholar
  7. Ardö, Y. (2006). Flavour formation by amino acid catabolism. Biotechnology Advanced, 24, 238–242.CrossRefGoogle Scholar
  8. Arena, M. E., & Manca de Nadra, M. C. (2001). Biogenic amine production by Lactobacillus. Journal of Applied Microbiology, 90, 158–162.CrossRefGoogle Scholar
  9. Arena, M. E., Saguir, F. M., & Manca de Nadra, M. C. (1999). Arginine, citrulline and ornithine metabolism by lactic acid bacteria from wine. International Journal of Food Microbiology, 52, 155–161.CrossRefGoogle Scholar
  10. Arena, M. E., Fiocco, D., Manca de Nadra, M. C., Pardo, I., & Spano, G. (2007). Characterization of a Lactobacillus plantarum strain able to produce tyramine and partial cloning of a putative tyrosine decarboxylase gene. Current Microbiology, 55, 205–210.CrossRefGoogle Scholar
  11. Back, W. (1978). Elevation of Pediococcus cerevisiae subsp. dextrinicus Coster and White to species status Pediococcus dextrinicus (Coster and White) comb. nov. International Journal of Systematic Bacteriology, 28, 523–527.CrossRefGoogle Scholar
  12. Bae, S., Fleet, G. H., & Heards, G. M. (2006). Lactic acid bacteria associated with wine grapes from several Australian vineyards. Journal of Applied Microbiology, 100, 712–727.CrossRefGoogle Scholar
  13. Bartowsky, E. J. (2009). Bacterial spoilage of wine and approaches to minimize it. Letters in Applied Microbiology, 48, 149–156.CrossRefGoogle Scholar
  14. Bartowsky, E. J., & Henschke, P. A. (2004). The ‘buttery’ attribute of wine—diacetyl—desirability, spoilage and beyond. International Journal of Food Microbiology, 96, 235–252.CrossRefGoogle Scholar
  15. Bauer, R., Nel, H. A., & Dicks, L. M. T. (2003). Pediocin PD-1 as a method to control growth of Oenococcus oeni in wine. American Journal of Enology and Viticulture, 54, 86–91.Google Scholar
  16. Bauer, R., Du Toit, M., & Kossmann, J. (2010). Influence of environmental parameters on production of the acrolein precursor 3-hydroxypropionaldehyde by Lactobacillus reuteri DSMZ 20016 and its accumulation by wine lactobacilli. International Journal of Food Microbiology, 137, 28–31.CrossRefGoogle Scholar
  17. Beneduce, L., Spano, G., Vernile, A., Tarantino, D., & Massa, S. (2004). Molecular characterization of lactic acid populations associated with wine spoilage. Journal of Basic Microbiology, 44, 10–16.CrossRefGoogle Scholar
  18. Borneman, A. R., Bartowsky, E. J., McCarthy, J., & Chambers, P. J. (2010). Genotypic diversity in Oenococcus oeni by high-density microarray comparative genome hybridization and whole genome sequencing. Applied Microbiology and Biotechnology, 86, 681–691.CrossRefGoogle Scholar
  19. Bossi, A., Rinalducci, S., Zolla, L., Antonioli, P., Righetti, P. G., & Zapparoli, G. (2007). Effect of tannic acid on Lactobacillus hilgardii analysed by a proteomic approach. Applied Microbiology, 102, 787–795.CrossRefGoogle Scholar
  20. Bou, M., & Krieger, S. (2004). Alcohol-tolerant malolactic strains for the maturation of wines with average or high pH (Pub. N: WO/2004/111179; PCT/FR2004/001421).Google Scholar
  21. Bou, M., & Powell, C. (2006). Strain selection techniques. In R. Morenzoni (Ed.), Malolactic fermentation in wine—understanding the science and the practice (pp. 6.1–6.8). Montréal: Lallemand.Google Scholar
  22. Boulton, R. B., Singleton, V. L., Bisson, L. F., & Kunkee, R. E. (1996). In R. B. Boulton (Ed.), Principles and practices of winemaking. New York: Chapman and Hall.Google Scholar
  23. Campos, F. M., Figueiredo, A. R., Hogg, T. A., & Couto, J. A. (2009a). Effect of phenolic acids on glucose and organic acid metabolism by lactic acid bacteria from wine. Food Microbiology, 26, 409–414.CrossRefGoogle Scholar
  24. Campos, F. M., Couto, J. A., Figueiredo, A. R., Tóth, I. V., Rangel, A. O. S. S., & Hogg, T. A. (2009b). Cell membrane damage induced by phenolic acids on wine lactic acid bacteria. International Journal of Food Microbiology, 135, 144–151.CrossRefGoogle Scholar
  25. Caridi, A., & Corte, V. (1997). Inhibition of malolactic fermentation by cryotolerant yeasts. Biotechnology Letters, 19, 723–726.CrossRefGoogle Scholar
  26. Carr, J. G., & Davies, P. A. (1970). Homofermentative lactobacilli of ciders including Lactobacillus mali sp. nov. The Journal of Applied Bacteriology, 33, 768–774.Google Scholar
  27. Carr, J. G., & Davies, P. A. (1972). The ecology and classification of strains of Lactobacillus collinoides nov. spec.: A bacterium commonly found in fermenting apple juice. The Journal of Applied Bacteriology, 35, 463–471.Google Scholar
  28. Carre, E. (1982). Recherches sur la croissance des bacteries lactiques en vinification. Désacidification biologique des vins. PhD thesis. Université de Bordeaux II, Bordeaux, France.Google Scholar
  29. Cavin, J. F., Andioc, V., Etievant, P. X., & Davies, C. (1993). Ability of wine lactic acid bacteria to metabolize phenol carboxylic acids. American Journal of Enology and Viticulture, 44, 76–80.Google Scholar
  30. Cavin, J. F., Barthelmebs, L., & Diviès, C. (1997). Molecular characterization of an inducible ρ-coumaric acid decarboxylase from Lactobacillus plantarum: Gene cloning, transcriptional analysis, overexpression in Escherichia coli, purification and characterization. Applied and Environmental Microbiology, 66, 3368–3375.Google Scholar
  31. Chang, I. S., Kim, B. H., & Shin, P. K. (1997). Use of sulfite and hydrogen peroxide to control bacterial contamination in ethanol fermentation. Applied and Environmental Microbiology, 63, 1–6.Google Scholar
  32. Charpentier, C., & Feuillat, M. (1993). Yeast autolysis. In G. H. Fleet (Ed.), Wine microbiology and biotechnology (pp. 225–242). Switzerland: Harwood Academic.Google Scholar
  33. Chatonnet, P., Dubourdieu, D., Boidron, J. N., & Pons, M. (1992). The origin of ethylphenols in wines. Journal of the Science of Food and Agriculture, 60, 165–178.CrossRefGoogle Scholar
  34. Chatonnet, P., Dubourdieu, D., & Boidron, J. N. (1995). The influence of Brettanomyces/Dekkera sp. yeast and lactic acid bacteria on the ethylphenol content of red wines. American Journal of Enology and Viticulture, 46, 463–468.Google Scholar
  35. Chisholm, M. G., & Samuels, J. M. (1992). Determination of the impact of the metabolites of sorbic acid on the odor of a spoiled red wine. Journal of Agricultural and Food Chemistry, 40, 630–633.CrossRefGoogle Scholar
  36. Claisse, O., & Lonvaud-Funel, A. (2000). Assimilation of glycerol by a strain of Lactobacillus collinoides isolated from cider. Food Microbiology, 17, 513–519.CrossRefGoogle Scholar
  37. Comitini, F., Ferretti, R., Clementi, F., Mannazzu, I., & Ciani, M. (2005). Interactions between Saccharomyces cerevisiae and malolactic bacteria: Preliminary characterization of a yeast proteinaceous compound(s) active against Oenococcus oeni. Journal of Applied Microbiology, 99, 105–111.CrossRefGoogle Scholar
  38. Constantini, A., Cersosimo, M., Del Prete, V., & Garcia-Moruno, E. (2006). Production of biogenic amines by lactic acid bacteria: Screening by PCR, thin layer chromatography, and HPLC of strains isolated from wine and must. Journal of Food Protection, 69, 391–396.Google Scholar
  39. Costello, P. J., & Henschke, P. A. (2002). Mousy off-flavour of wine: Precursors and biosynthesis of the causative N-heterocycles 2-ethyltetrahydropyradine, 2-acetyltetrahydropyridine, and 2-acetyl-1-pyrroline by Lactobacillus hilgardii DSM 20176. Journal of Agricultural and Food Chemistry, 50, 7079–7087.CrossRefGoogle Scholar
  40. Costello, P., Lee, T. H., & Henschke, P. A. (2001). Ability of lactic acid bacteria to produce N-heterocycles causing mousy off-flavour in wine. Australian Journal of Grape and Wine Research, 7, 160–167.CrossRefGoogle Scholar
  41. Coton, E., Rollan, G., Bertrand, A., & Lonvaud-Funel, A. (1998). Histamine producing lactic acid bacteria in wines: Early detection, frequency, and distribution. American Journal of Enology and Viticulture, 49, 199–204.Google Scholar
  42. Coton, E., Torlois, S., Bertrand, A., & Lonvaud-Funel, A. (1999). Biogenic amines and wine lactic acid bacteria. Bulletin of the International Organisation of Vine and Wine (OIV), 815–816, 22–35.Google Scholar
  43. Couto, J. A., & Hogg, T. A. (1994). Diversity of ethanol-tolerant lactobacilli isolated from Douro fortified wine: Clustering and identification by numerical analysis of electrophoretic protein profiles. The Journal of Applied Bacteriology, 76, 487–491.Google Scholar
  44. Couto, J. A., Campos, F. M., Figueiredo, A. R., & Hogg, T. A. (2006). Ability of lactic acid bacteria to produce volatile phenols. American Journal of Enology and Viticulture, 57, 166–171.Google Scholar
  45. Cox, D. J. (1991). Studies on the energetics and growth benefits of malolactic fermentation in lactic acid bacteria. PhD thesis. Cornell University, Ithaca, New York.Google Scholar
  46. Cox, D. J., & Henick-Kling, T. (1989). Chemiosmotic energy from malolactic fermentation. The Journal of Applied Bacteriology, 171, 5750–5752.Google Scholar
  47. Crowell, E. A., & Guymon, I. F. (1975). Wine constituents arising from sorbic acid addition and identification of 2-ethoxyhexa-3, 5-diene as a source of geranium-like off-odor. American Journal of Enology and Viticulture, 26, 97–102.Google Scholar
  48. Curiel, J. A., Muñoz, R., & Lópezde Felip, F. (2010). pH and dose-dependent effects of quercetin on the fermentation capacity of Lactobacillus plantarum. Food Science and Technology, 43, 926–933.Google Scholar
  49. Curk, M.-C., Hubert, J.-C., & Bringel, F. (1996). Lactobacillus paraplantarum sp. nov., a new species related to Lactobacillus plantarum. International Journal of Systematic Bacteriology, 46, 595–598.CrossRefGoogle Scholar
  50. Daeschel, M. A., Jung, D.-S., & Watson, B. T. (1991). Controlling wine malolactic fermentation with nisin and nisin-resistant strains of Leuconostoc oenos. Applied and Environmental Microbiology, 57, 601–603.Google Scholar
  51. Davis, C. R., Wibowo, D., Eschenbruch, R., Lee, T. H., & Fleet, G. H. (1985). Practical implications of malolactic fermentation: A review. American Journal of Enology and Viticulture, 36, 290–301.Google Scholar
  52. Davis, C. R., Wibowo, D. J., Lee, T. H., & Fleet, G. H. (1986a). Growth and metabolism of lactic acid bacteria during and after malolactic fermentation of wines at different pH. Applied and Environmental Microbiology, 5, 539–545.Google Scholar
  53. Davis, C. R., Wibowo, D. J., Lee, T. H., & Fleet, G. H. (1986b). Growth and metabolism of lactic acid bacteria during fermentation of some Australian wines. Food Technology in Australia, 38, 35–40.Google Scholar
  54. Davis, C. R., Wibowo, D., Fleet, G. H., & Lee, T. H. (1988). Properties of wine lactic acid bacteria: Their potential enological significance. American Journal of Enology and Viticulture, 39, 137–142.Google Scholar
  55. De las Rivas, B., Delas Rivas, B., Marcobal, Á., Carrascose, A. V., & Muñoz, R. (2006). PCR detection of foodborne bacteria producing the biogenic amines histamine, tyramine, putrescine, and cadaverine. Journal of Food Protection, 69, 2509–2514.Google Scholar
  56. De las Rivas, B., Rodríguez, H., Curiel, J. A., Landete, J. M., & Munoz, R. (2009). Molecular screening of wine lactic acid bacteria degrading hydroxycinnamic acids. Journal of Agricultural and Food Chemistry, 57, 490–494.CrossRefGoogle Scholar
  57. Delfini, C., & Morsiani, M. G. (1992). Resistance to sulfur dioxide of malolactic strains of Leuconostoc oenos and Lactobacillus sp. isolated from wines. Sciences des Aliments, 12, 493–511.Google Scholar
  58. Derré, I., Rapoport, G., & Msadek, T. (1999). CtsR, a novel regulator of stress and heat shock response, controls clp and molecular chaperone gene expression in Gram-positive bacteria. Molecular Microbiology, 31, 117–132.CrossRefGoogle Scholar
  59. Dias, L., Pereira-da-Silva, S., Tavares, M., Malfeito-Ferreira, M., & Loureiro, V. (2003). Factors affecting the production of 4-ethylphenol by the yeast Dekkera bruxellensis in enological conditions. Food Microbiology, 20, 377–384.CrossRefGoogle Scholar
  60. Dick, K. J., Molan, P. C., & Eschenbruch, R. (1992). The isolation from Saccharomyces cerevisiae of two antibacterial cationic proteins that inhibit malolactic bacteria. Vitis, 31, 105–116.Google Scholar
  61. Dicks, L. M. T., & Endo, A. (2009). Taxonomic status of lactic acid bacteria in wine and key characteristics to differentiate species. South African Journal of Enology and Viticulture, 30, 72–90.Google Scholar
  62. Dittrich, H. H. (1977). Mikrobiologie des Weines. Handbuch der Getränketechnologie. Stuttgart: Ulmer Verlag.Google Scholar
  63. Donnelly, D. M. (1977). Airborne microbial contamination in a winery bottling room. American Journal of Enology and Viticulture, 28, 176–181.Google Scholar
  64. Dott, W., Heinzel, M., & Trüper, H. G. (1976). Sulphite formation by wine yeast. Archives of Mikrobiologie, 107, 289–292.CrossRefGoogle Scholar
  65. Douglas, H. C., & Cruess, W. V. (1936). A Lactobacillus from California wine: Lactobacillus hilgardii. Food Research, 1, 113–119.Google Scholar
  66. Downing, L. (2003). Characterisation of biogenic amine-encoding genes in lactic acid bacteria isolated from South African wine. MSc Thesis. Institute for Wine Biotechnology, Stellenbosch University, Stellenbosch, South Africa.Google Scholar
  67. Drici-Cachon, A., Guzzo, J., Cavin, F., & Diviès, C. (1996). Acid tolerance in Leuconostoc oenos. Isolation and characterisation of an acid resistant mutant. Applied Microbiology and Biotechnology, 44, 785–789.Google Scholar
  68. Du Plessis, L. D. W., & Van Zyl, J. A. (1963). The microbiology of South African winemaking: Part IV. The taxonomy and the incidence of lactic acid bacteria from dry wines. South African Journal of Agricultural Science, 6, 261–273.Google Scholar
  69. Du Plessis, H. W., Dicks, L. M. T., Pretorius, I. S., Lambrechts, M. G., & Du Toit, M. (2004). Identification of lactic acid bacteria isolated from South African brandy base wines. International Journal of Food Microbiology, 91, 19–29.CrossRefGoogle Scholar
  70. Du Toit, C. (2002). The evaluation of bacteriocins and enzymes for biopreservation of wine. Master Thesis. Institute for Wine Biotechnology, Stellenbosch University, South Africa.Google Scholar
  71. Du Toit, M., & Pretorius, I. S. (2000). Microbial spoilage and preservation of wine: Using weapons from nature’s own arsenal—A review. South African Journal of Enology and Viticulture, 21, 74–96 (special issue).Google Scholar
  72. Dueñas, M., Irastorza, A., Fernadez, C., & Bilbao, A. (1995). Heterofermentative lactobacilli causing ropiness in Basque Country ciders. Journal of Food Protection, 59, 76–80.Google Scholar
  73. Edinger, W. D., & Splittstoesser, D. F. (1986a). Sorbate tolerance by lactic acid bacteria associated with grapes and wine. Journal of Food Science, 51, 1077–1078.CrossRefGoogle Scholar
  74. Edinger, W. D., & Splittstoesser, D. F. (1986b). Production by lactic acid bacteria of sorbic alcohol, the precursor of the geranium odor compound. American Journal of Enology and Viticulture, 37, 34–38.Google Scholar
  75. Edwards, C. G., & Beelman, R. B. (1987). Inhibition of malolactic bacterium, Leuconostoc oenos (PSU-1), by decanoic acid and subsequent removal of the inhibition by yeast ghosts. American Journal of Enology and Viticulture, 38, 239–242.Google Scholar
  76. Edwards, C. G., & Jensen, K. A. (1992). Occurrence and characterisation of lactic acid bacteria from Washington State Wines: Pediococcus spp. American Journal of Enology and Viticulture, 43, 233–238.Google Scholar
  77. Edwards, C. G., Haag, K. M., Collins, M. D., Hutson, R. A., & Huang, Y. C. (1998). Lactobacillus kunkeei sp. nov.: A spoilage organism associated with grape juice fermentations. Journal of Applied Microbiology, 84, 698–702.CrossRefGoogle Scholar
  78. Edwards, C. G., Collins, M. D., Lawson, P. A., & Rodriguez, A. V. (2000). Lactobacillus nagelii sp. nov., an organism isolated from a partially fermented wine. International Journal of Systematic and Evolutionary Microbiology, 50, 699–702.CrossRefGoogle Scholar
  79. Eliseeva, G. S., Nagornaia, S. S., Zherebilo, O. E., Podgorski, V. S., & Ignatova, E. A. (2001). Biological deacidification of wines using lactic-acid bacteria and yeasts [in Russian]. Prikladnaya Biokhimiya i Mikrobiologiy, 37, 487–493.Google Scholar
  80. Eschenbruch, R. (1974). Sulfite and sulfide formation during winemaking—A review. American Journal of Enology and Viticulture, 25, 157–161.Google Scholar
  81. Escot, S., Feuillat, M., Dulau, L., & Charpentier, C. (2001). Release of polysaccharides on colour stability and wine astringency. Australian Journal of Journal of Grape and Wine Research, 7, 153–159.CrossRefGoogle Scholar
  82. Esterbauer, H., Schaur, R. J., & Zollner, H. (1991). Chemistry and biochemistry of 4-hydroxynonenal, malondialdehyde and related aldehydes. Free Radical Biology & Medicine, 11, 81–128.CrossRefGoogle Scholar
  83. Farías, M. E., Rollán, G. C., & Manca de Nadra, M. C. (1996). Influence of nutritional factors on the protease production by Leuconostoc oenos from wine. The Journal of Applied Bacteriology, 81, 398–402.Google Scholar
  84. Ferchichi, M., Hemme, D., Nardi, M., & Pamboukdjan, N. (1985). Production of methanethiol from methionine by Brevibacterium linens CNRZ 918. Journal of General Microbiology, 131, 715–723.Google Scholar
  85. Fernandes, J. O., & Ferreira, M. A. (2000). Combined ion-pair extraction and gas chromatography-mass spectrometry for the simultaneous determination of diamines, polyamines and aromatic amines in Port wine and grape juice. Journal of Chromatography A, 886, 183–195.CrossRefGoogle Scholar
  86. Figueiredo, A. R., Campos, F., de Freitas, V., Hogg, T., & Couto, J. A. (2008). Effect of phenolic aldehydes and flavonoids on growth and inactivation of Oenococcus oeni and Lactobacillus hilgardii. Food Microbiology, 25, 105–112.CrossRefGoogle Scholar
  87. Fleet, G. H., Lafon-Lafourcade, S., & Ribereau-Gayon, P. (1984). Evolution of yeasts and lactic acid bacteria during fermentation and storage of Bordeaux wines. Applied and Environmental Microbiology, 48, 1034–1038.Google Scholar
  88. Fugelsang, K. C., & Edwards, C. G. (1997). In K. C. Fugelsang & C. G. Edwards (Eds.), Wine microbiology: Practical applications and procedures. New York: Springer.Google Scholar
  89. Fumi, M. D., Krieger-Weber, S., Déléris-Bou, M., Silva, A., & du Toit, M. (2010). A new generation of malolactic starter cultures for high pH wines. Proceedings International IVIF Congress 2010, WB3 Microorganisms—Malolactic-Fermentation.Google Scholar
  90. G-Alegría, E., López, I., Ruiz, J. I., Sáenz, J., Fernández, E., Zarazaga, M., et al. (2004). High tolerance of wild Lactobacillus plantarum and Oenococcus oeni strains to lyophilisation and stress environmental conditions of acid pH and ethanol. FEMS Microbiology Letters, 230, 53–61.CrossRefGoogle Scholar
  91. Gardini, F., Zaccarelli, A., Belletti, N., Faustini, F., Cavazza, A., Maruscelli, M., et al. (2005). Factors influencing biogenic amine production by a strain of Oenococcus oeni in a model system. Food Control, 16, 609–616.CrossRefGoogle Scholar
  92. Garvie, E. I. (1967a). The growth factor and amino acid requirements of species of the genus Leuconostoc, including Leuconostoc paramesenteroides (sp. nov.) and Leuconostoc oenos. Journal of General Microbiology, 48, 439–447.Google Scholar
  93. Garvie, E. I. (1967b). Leuconostoc oenos sp. nov. Journal of General Microbiology, 48, 431–438.Google Scholar
  94. Garvie, E. I. (1979). Proposal of neotype strains for Leuconostoc mesenteroides (Tsenkovskii) van Tieghem, Leuconostoc dextranicum (Beijernick) Hucker and Pederson and Leuconostoc cremoris (Knudsen and Sørensen) Garvie. International Journal of Systematic Bacteriology, 29, 149–152.CrossRefGoogle Scholar
  95. Garvie, E. I. (1983). Leuconostoc mesenteroides subsp. cremoris (Kudsen and Sørensen) comb. nov. and Leuconostoc mesenteroides subsp. dextranicum (Beijernick) comb. nov. International Journal of Systematic Bacteriology, 33, 118.CrossRefGoogle Scholar
  96. Gerbaux, V., Vincent, B., & Bertrand, A. (2002). Influence of maceration temperature and enzymes on the content of volatile phenols in Pinot noir wines. American Journal of Enology and Viticulture, 53, 131–137.Google Scholar
  97. Glória, M. B. A., Watson, B. T., Simon-Sarkadi, L., & Daeschel, M. A. (1998). A survey of biogenic amines in Oregon Pinot noir and Cabernet Sauvignon wines. American Journal of Enology and Viticulture, 49, 279–282.Google Scholar
  98. Grimaldi, A., Bartowsky, E., & Jiranek, V. (2005). Screening of Lactobacillus spp. and Pediococcus spp. for glycosidase activities that are important in oenology. Journal of Applied Microbiology, 99, 1061–1069.CrossRefGoogle Scholar
  99. Guerrini, S., Mangani, S., Granchi, L., & Vincenzini, M. (2002). Biogenic amine production by Oenococcus oeni. Current Microbiology, 44, 374–378.CrossRefGoogle Scholar
  100. Guerzoni, M. E., Sinigaglia, M., Gardini, F., Ferruzzi, M., & Torriani, S. (1995). Effects of pH, temperature, ethanol, and malate concentration on Lactobacillus plantarum and Leuconostoc oenos: Modelling of the malolactic activity. American Journal of Enology and Viticulture, 3, 368–374.Google Scholar
  101. Guzzo, J., & Desroche, N. (2009). Physical and chemical stress factors in lactic acid bacteria. In H. König, F. Fröhlich, & G. Unden (Eds.), Biology of microorganisms on grapes, in must and in wine (pp. 293–306). Berlin: Springer-Verlag.CrossRefGoogle Scholar
  102. Henick-Kling, T. (1986). Growth and metabolism of Leuconostoc oenos and Lactobacillus plantarum in wine. PhD thesis. University of Adelaide, South Australia.Google Scholar
  103. Henick-Kling, T. (1988). Yeast and bacteria control in winemaking. In H. F. Linskens & J. F. Jackson (Eds.), Modern methods of plant analysis. New series, Volume 6. Wine analysis (pp. 276–315). Berlin: Springer.Google Scholar
  104. Henick-Kling, T. (1993). Malolactic fermentation. In G. H. Fleet (Ed.), Wine microbiology and biotechnology (pp. 289–326). Chur: Harwood Academic.Google Scholar
  105. Henick-Kling, T., & Park, Y. H. (1994). Considerations for the use of yeast and starter cultures: SO2 and timing of inoculation. American Journal of Enology and Viticulture, 45, 464–469.Google Scholar
  106. Henick-Kling, T., Acree, T., Gavitt, B., Krieger, S. A., & Laurent, M. H. (1993). Sensory aspects of malolactic fermentation. In Proceedings of the 8th Australian Wine Industry Technical Conference (pp. 148–152). Adelaide: Winetitles.Google Scholar
  107. Hernández, T., Estrella, I., Pérez-Gordo, M., Alegría, E. G., Tenorio, C., Ruiz-Larrrea, F., et al. (2007). Contribution of malolactic fermentation by Oenococcus oeni and Lactobacillus plantarum to the changes in the nonanthocyanin polyphenolic composition of red wine. Journal of Agricultural and Food Chemistry, 55, 5260–5266.CrossRefGoogle Scholar
  108. Holo, H., Jeknic, Z., Daeschel, M., Stevanovic, S., & Nes, I. F. (2001). Plantaricin W from Lactobacillus plantarum belongs to a new family of two-peptide lantibiotics. Microbiology, 147, 643–651.Google Scholar
  109. Hornsey, I. (2007). Lactic acid bacteria and malo-lactic fermentation. In I. Hornsey (Ed.), The chemistry and biology of winemaking (pp. 203–240). Cambridge: RSC.Google Scholar
  110. Hutkins, R. W., & Nannen, N. (1993). pH homeostasis in lactic acid bacteria. Journal of Dairy Science, 76, 2354–2365.CrossRefGoogle Scholar
  111. Izquierdo Cañas, P. M., García Romero, E., Gómez Alonso, S., Fernández González, M., & Palop Herreros, M. L. L. (2007). Amino acids and biogenic amines during spontaneous malolactic fermentation in Tempranillo red wines. Journal of Food Composition and Analysis, 21, 731–735.CrossRefGoogle Scholar
  112. Izquierdo, P. M., Ruiz, P., Seseña, S., & Palop, M. L. (2009). Ecological study of lactic acid microbiota isolated from Tempranillo wines of Castilla-La Mancha. Journal of Bioscence and Bioengineering, 108, 220–224.CrossRefGoogle Scholar
  113. Jackson, R. S. (2008). Origin and growth of lactic acid bacteria. In R. S. Jackson (Ed.), Wine science: Principles and applications (p. 394). California: Academic.Google Scholar
  114. Jones, G. V. (2009). Climate variability and change: Influences on viticulture and wine production. In: Proceedings 4th International Conferences of the South African Society for Enology and Viticulture, 28–30 July, Cape Town, South Africa.Google Scholar
  115. Julien, A., Roustan, J. L., Dulau, L., & Sablayrolles, J. M. (2000). Characterization of enological yeast strains: Evaluation of their nutrients requirements in nitrogen and oxygen. American Journal of Enology and Viticulture, 51, 302.Google Scholar
  116. King, S. W., & Beelman, R. B. (1986). Metabolic interactions between Saccharomyces cerevisiae and Leuconostoc oenos in a model grape juice/wine system. American Journal of Enology and Viticulture, 37, 53–60.Google Scholar
  117. Knoll, C., Divol, B., & Du Toit, M. (2008). Genetic screening of lactic acid bacteria of oenological origin for bacteriocin-encoding genes. Food Microbiology, 25, 983–991.CrossRefGoogle Scholar
  118. Krieger, S. A. (1989). Optimierung des biologischen Säureabbaus in Wein mit Starterkulturen. PhD thesis. University of Hohenheim, Germany.Google Scholar
  119. Krieling, S. J. (2003). An investigation into lactic acid bacteria as a possible cause of bitterness in wine. MSc Thesis. Institute for Wine Biotechnology, Stellenbosch University, South Africa.Google Scholar
  120. Kunkee, R. E. (1967). Malolactic fermentation. Advances in Applied Microbiology, 9, 235–279.CrossRefGoogle Scholar
  121. Lafon-Lafourcade, S. (1983). In H. J. Rehm & G. Redd (Eds.), Wine and brandy in biotechnology (pp. 81–163). Weinheim: Verlag Chemie.Google Scholar
  122. Lafon-Lafourcade, S., Carre, E., & Ribéreau-Gayon, P. (1983). Occurrence of lactic acid bacteria during different stages of the vinification and conservation of wines. Applied and Environmental Microbiology, 46, 874–880.Google Scholar
  123. Landaud, S., Helinck, S., & Bonnarme, P. (2008). Formation of volatile sulphur compounds and metabolism of methionine and other sulphur compounds in fermented food. Applied Microbiology and Biotechnology, 77, 1191–1205.CrossRefGoogle Scholar
  124. Landete, J. M., Ferrer, S., & Pardo, I. (2005a). Which lactic acid bacteria are responsible for histamine production in wine? Journal of Applied Microbiology, 99, 580–586.CrossRefGoogle Scholar
  125. Landete, J. M., Ferrer, S., Polo, L., & Pardo, I. (2005b). Biogenic amines in wines from three Spanish regions. Journal of Agricultural and Food Chemistry, 53, 1119–1124.CrossRefGoogle Scholar
  126. Landete, J. M., Ferrer, S., & Pardo, I. (2007a). Biogenic amine production by lactic acid bacteria, acetic bacteria and yeast isolated from wine. Food Control, 18, 1569–1574.CrossRefGoogle Scholar
  127. Landete, J. M., Rodriguéz, H., De las Rivas, B., & Muñdoz, R. (2007b). High-added-value antioxidants obtained from the degradation of wine phenolics by Lactobacillus plantarum. Journal of Food Protection, 70, 2670–2675.Google Scholar
  128. Landete, J. M., Pardo, I., & Ferrer, S. (2008). Regulation of hdc expression and HDC activity by enological factors in lactic acid bacteria. Journal of Applied Microbiology, 105, 1544–1551.CrossRefGoogle Scholar
  129. Le Jeune, C., Lonvaud-Funel, A., ten Brink, B., Hofstra, H., & van der Vossen, J. M. B. M. (1995). Development of a detection system for histidine decarboxylating lactic acid bacteria based on DNA probes, PCR and activity test. The Journal of Applied Bacteriology, 78, 316–326.Google Scholar
  130. Lee, J.-E., Hwang, G.-S., Lee, C.-H., & Hong, Y.-S. (2009). Metabolomics reveals alterations in both primary and secondary metabolites by wine bacteria. Journal of Agricultural and Food Chemistry, 57, 10772–10783.CrossRefGoogle Scholar
  131. Liu, S.-Q. (2002). Malolactic fermentation in wine—Beyond deacidification. Journal of Applied Microbiology, 92, 589–601.CrossRefGoogle Scholar
  132. Liu, S.-Q., & Pilone, G. J. (2000). An overview of formation and roles of acetaldehyde in winemaking with emphasis on microbiological implications. International Journal of Food Science & Technology, 35, 49–61.CrossRefGoogle Scholar
  133. Liu, S.-Q., Pritchard, G. G., Hardman, M. J., & Pilone, G. J. (1994). Citrulline production and ethyl carbamate (urethane) precursor formation from arginine degradation by wine lactic acid bacteria Leuconostoc oenos and Lactobacillus buchneri. American Journal of Enology and Viticulture, 45, 235–242.Google Scholar
  134. Liu, S.-Q., Pritchard, G. C., Hardman, M. J., & Pilone, G. J. (1995). Occurrence of arginine deiminase pathway enzymes in arginine catabolism in wine lactic acid bacteria. Applied and Environmental Microbiology, 61, 310–316.Google Scholar
  135. Liu, M., Nauta, A., Francke, C., & Siezen, R. J. (2008). Comparative genomics of enzymes in flavour-forming pathways from amino acids in lactic acid bacteria. Applied and Environmental Microbiology, 74, 4590–4600.CrossRefGoogle Scholar
  136. Lonvaud-Funel, A. (1986). Recherches sur les bactéries lactiques du vin. Fonctions métaboliques, croissance, génétique plasmidique. Thesis, University of Bordeaux, France.Google Scholar
  137. Lonvaud-Funel, A. (1995). Microbiology of the malolactic fermentation: Molecular aspects. FEMS Microbiology Letters, 126, 209–214.CrossRefGoogle Scholar
  138. Lonvaud-Funel, A. (1999). Lactic acid bacteria in the quality improvement and depreciation of wine. Antonie van Leeuwenhoek, 76, 317–331.CrossRefGoogle Scholar
  139. Lonvaud-Funel, A. (2001a). Interactions between lactic acid bacteria of wine and phenolic compounds. In: Nutritional aspects II, synergy between yeast and bacteria, pp. 27–32. Lallemand Technical Meeting, Perugia, Italy, 27–30 April 2001.Google Scholar
  140. Lonvaud-Funel, A. (2001b). Biogenic amines in wine: Role of lactic acid bacteria. FEMS Microbiology Letters, 199, 9–13.CrossRefGoogle Scholar
  141. Lonvaud-Funel, A., & Joyeux, A. (1994). Histamine production by wine lactic acid bacteria: Isolation of a histamine-producing strain of Leuconostoc oenos. The Journal of Applied Bacteriology, 77, 401–407.Google Scholar
  142. Lonvaud-Funel, A., & Strasser de Saad, A. M. (1982). Purification and properties of a malolactic enzyme from a strain of Leuconostoc mesenteroides isolated from grapes. Applied and Environmental Microbiology, 43, 357–361.Google Scholar
  143. Lonvaud-Funel, A., Joyeux, A., & Desens, C. (1988). Inhibition of malolactic fermentation of wines by products of yeast metabolism. Journal of the Science of Food and Agriculture, 44, 183–191.CrossRefGoogle Scholar
  144. Lonvaud-Funel, A., Joyeux, A., & Ledoux, O. (1991). Specific enumeration of lactic acid bacteria in fermenting grape must and wine by colony hybridization with non-isotopic DNA probes. The Journal of Applied Bacteriology, 71, 501–508.Google Scholar
  145. López, I., Tenorio, C., Zarazaga, M., Dizy, M., Torres, C., & Ruiz-Larrea, F. (2007). Evidence of mixed wild populations of Oenococus oeni strains during wine spontaneous malolactic fermentation. European Food Research and Technology, 226, 215–223.CrossRefGoogle Scholar
  146. Lucas, P., & Lonvaud-Funel, A. (2002). Purification and partial gene sequence of the tyrosine decarboxylase of Lactobacillus brevis IOEB 9809. FEMS Microbiology Letters, 211, 85–89.CrossRefGoogle Scholar
  147. Lucas, P., Landete, J., Coton, M., Coton, E., & Lonvaud-Funel, A. (2003). The tyrosine decarboxylase operon of Lactobacillus brevis IOEB 9809: Characterization and conservation in tyramine-producing bacteria. FEMS Microbiology Letters, 229, 65–71.CrossRefGoogle Scholar
  148. Lucas, P. M., Claisse, O., & Lonvaud-Funel, A. (2008). High frequency of histamine-producing bacteria in enological environment and instability of the phenotype. Applied and Environmental Microbiology, 74, 811–817.CrossRefGoogle Scholar
  149. Manca de Nadra, M. C., Farías, M. E., Moreno-Arribas, M. V., Pueyo, E., & Polo, M. C. (1997). Proteolytic activity of Leuconostoc oenos: Effect on proteins and polypeptides from white wine. FEMS Microbiology Letters, 150, 135–139.CrossRefGoogle Scholar
  150. Manca de Nadra, M. C., Farías, M. E., Moreno-Arribas, V., Pueyo, E., & Polo, M. C. (1999). A proteolytic effect of Oenococcus oeni on the nitrogenous macromolecular fraction of red wine. FEMS Microbiology Letters, 174, 41–47.CrossRefGoogle Scholar
  151. Manca de Nadra, M. C., Farías, M. E., Pueyo, E., & Polo, M. C. (2005). Protease activity of Oenococcus oeni viable cells on red wine nitrogenous macromolecular fraction in presence of SO2 and ethanol. Food Control, 16, 851–854.CrossRefGoogle Scholar
  152. Mañes-Lázaro, R., Ferrer, S., Rodas, A. M., Urdiain, M., & Pardo, I. (2008a). Lactobacillus bobalius sp. nov., a lactic acid bacterium isolated from Spanish Bobal grape must. International Journal of Systematic and Evolutionary Microbiology, 58, 2699–2703.CrossRefGoogle Scholar
  153. Mañes-Lázaro, R., Ferrer, S., Rosselló-Mora, R., & Pardo, I. (2008b). Lactobacillus uvarum sp. nov.—A new lactic acid bacterium isolated from Spanish Bobal grape must. Systematic and Applied Microbiology, 31, 425–433.CrossRefGoogle Scholar
  154. Mañes-Lázaro, R., Ferrer, S., Rosselló-Mora, R., & Pardo, I. (2009). Lactobacillus oeni sp. nov., from wine. International Journal of Systematic and Evolutionary Microbiology, 59, 2010–2014.CrossRefGoogle Scholar
  155. Manfroi, L., Silva, P. H. A., Rizzon, L. A., Sabaini, P. S., & Glória, M. B. A. (2009). Influence of alcoholic and malolactic starter cultures on bioactive amines in Merlot wines. Food Chemistry, 116, 208–213.CrossRefGoogle Scholar
  156. Marcobal, Á., De Las Rivas, B., Moreno-Arribas, M. V., & Muñoz, R. (2004). Identification of the ornithine decarboxylase gene in the putrescine-producer Oenococcus oeni BIFI-83. FEMS Microbiology Letters, 239, 213–220.CrossRefGoogle Scholar
  157. Marcobal, Á., De Las Rivas, B., Moreno-Arribas, M. V., & Muñoz, R. (2005). Multiplex PCR method for the simultaneous detection of histamine-, tyramine-, and putrescine producing lactic acid bacteria in foods. Journal of Food Protection, 68, 874–878.Google Scholar
  158. Marcobal, Á., Martín-Álvarez, P. J., Polo, C., Muñoz, R., & Moreno-Arribas, M. V. (2006). Formation of biogenic amines throughout the industrial manufacture of red wine. Journal of Food Protection, 69, 397–404.Google Scholar
  159. Margalit, Y. (1997). In J. D. Crum (Ed.), Concepts in wine chemistry. San Francisco: Wine Appreciation Guild.Google Scholar
  160. Margalith, P. Z. (1981). Flavour microbiology. Springfield: Charles C. Thomas.Google Scholar
  161. Martín-Álvarez, P. J., Marcobal, Á., Polo, C., & Moreno-Arribas, M. V. (2006). Influence of technological practices on biogenic amine contents in red wines. European Food Research and Technology, 222, 420–424.CrossRefGoogle Scholar
  162. Martineau, B., & Henick-Kling, T. (1995). Formation and degradation of diacetyl in wine during alcoholic fermentation with Saccharomyces cerevisiae strain EC1118 and malolactic fermentation with Leuconostoc oenos strain MCW. American Journal of Enology and Viticulture, 46, 442–448.Google Scholar
  163. Martineau, B., & Henick-Kling, T. (1996). Effect of malic acid on citric acid metabolism in Leuconostoc oenos. American Journal of Enology and Viticulture, 47, 229.Google Scholar
  164. Martineau, B., Henick-Kling, T., & Acree, T. (1995a). Reassessment of the influence of malolactic fermentation on the concentration of diacetyl in wines. American Journal of Enology and Viticulture, 46, 385–388.Google Scholar
  165. Martineau, B., Acree, T. E., & Henick-Kling, T. (1995b). Effect of wine type on the detection threshold for diacetyl. Food Research International, 28, 139–143.CrossRefGoogle Scholar
  166. Matthews, A., Grimaldi, A., Walker, M., Bartowsky, E., Grbin, P., & Jiranek, V. (2004). Lactic acid bacteria as a potential source of enzymes for use in vinification. Applied and Environmental Microbiology, 70, 5715–5731.CrossRefGoogle Scholar
  167. Matthews, A., Grbin, P. R., & Jiranek, V. (2007). Biochemical characterisation of the esterase activities of wine lactic acid bacteria. Applied Microbiology and Biotechnology, 77, 329–337.CrossRefGoogle Scholar
  168. Mayer, K., & Vetsch, U. (1973). pH und biologischer Säureabbau in Wein. Schweizer Zeitschrift für Obst- und Weinbau, 109, 635–639.Google Scholar
  169. Mazzoli, R., Lamberti, C., Coisson, J. D., Purrotti, M., Arlorio, M., Guiffrida, M. G., et al. (2009). Influence of ethanol, malate and arginine on histamine production of Lactobacillus hilgardii isolated from Italian red wine. Amino Acids, 36, 81–89.CrossRefGoogle Scholar
  170. McDonald, L. C., Fleming, H. P., & Hassan, H. M. (1990). Acid tolerance of Leuconostoc mesenteroides and Lactobacillus plantarum. Applied and Environmental Microbiology, 56, 2120–2124.Google Scholar
  171. Mira de Orduña, R., Liu, S.-Q., Patchet, M. L., & Pilone, G. J. (2000). Kinetics of the arginine metabolism of malolactic wine lactic acid bacteria Lactobacillus buchneri CUC-3 and Oenococcus oeni LO111. Journal of Applied Microbiology, 89, 547–552.CrossRefGoogle Scholar
  172. Mira de Orduña, R., Patchett, M. L., Liu, S.-Q., & Pilone, G. J. (2001). Growth and arginine metabolism of the wine lactic acid bacteria Lactobacillus buchneri and Oenococcus oeni at different pH values and arginine concentrations. Applied and Environmental Microbiology, 67, 1657–1662.CrossRefGoogle Scholar
  173. Monagas, M., Bartolomé, B., & Gómez-Cordovés, C. (2005). Updated knowledge about the presence of phenolic compounds in wine. Critical Reviews in Food Science and Nutrition, 45, 85–118.CrossRefGoogle Scholar
  174. Monnet, V., Le Bars, D., & Gripon, J. C. (1987). Purification and characterization of a cell wall proteinase from Streptococcus lactis NCDO 763. The Journal of Dairy Research, 54, 247–255.CrossRefGoogle Scholar
  175. Moreira, N., Mendes, F., Pereira, O., Guedes de Pinho, P., Hogg, T., & Vasconcelos, I. (2002). Volatile sulphur compounds in wine related to yeast metabolism and nitrogen composition of grape musts. Analytica Chimica Acta, 458, 157–167.CrossRefGoogle Scholar
  176. Moreno-Arribas, V., & Lonvaud-Funel, A. (1999). Tyrosine decarboxylase activity of Lactobacillus brevis IOEB 9809 isolated from wine and L. brevis ATCC 367. FEMS Microbiology Letters, 180, 55–60.CrossRefGoogle Scholar
  177. Moreno-Arribas, M. V., & Polo, M. C. (2008). Occurrence of lactic acid bacteria and biogenic amines in biologically aged wines. Food Microbiology, 25, 875–881.CrossRefGoogle Scholar
  178. Moreno-Arribas, V., Torlois, S., Joyeux, A., Bertrand, A., & Lonvaud-Funel, A. (2000). Isolation, properties and behaviour of tyramine-producing lactic acid bacteria from wine. Journal of Applied Microbiology, 88, 584–593.CrossRefGoogle Scholar
  179. Moreno-Arribas, V., Polo, M. C., Jorganes, F., & Muñoz, R. (2003). Screening of biogenic amine production by lactic acid bacteria isolated from grape must and wine. International Journal of Food Microbiology, 84, 117–123.CrossRefGoogle Scholar
  180. Morenzoni, R. (2006). Introduction. In R. Morenzoni (Ed.), Malolactic fermentation in wine—Understanding the science and the practice (pp. 2.1–2.2). Montréal: Lallemand.Google Scholar
  181. Mtshali, P. S., Divol, B. T., Van Rensburg, P., & Du Toit, M. (2010). Genetic screening of wine-related enzymes in Lactobacillus species isolated from South African wines. Journal of Applied Microbiology, 108, 1389–1397.CrossRefGoogle Scholar
  182. Navarro, L., Zarazaga, M., Saenz, J. S., Ruiz-Larrea, F., & Torres, C. (2000). Bacteriocin production by lactic acid bacteria isolated from Rioja red wines. Journal of Applied Microbiology, 88, 44–51.CrossRefGoogle Scholar
  183. Nehme, N., Mathieu, F., & Taillandier, P. (2010). Impact of the co-culture of Saccharomyces cerevisiaeOenococcus oeni on malolactic fermentation and partial characterization of a yeast-derived inhibitory peptidic fraction. Food Microbiology, 27, 150–157.CrossRefGoogle Scholar
  184. Nelson, L. (2008). The production of volatile phenols by wine microorganisms. Master Thesis. Department of Viticulture and Oenology, Stellenbosch University, South Africa.Google Scholar
  185. Nielsen, J. C., & Richelieu, M. (1999). Control of flavor development in wine during and after malolactic fermentation by Oenococcus oeni. Applied and Environmental Microbiology, 65, 740–745.Google Scholar
  186. Nieuwoudt, H. H., Prior, B. A., Pretorius, I. S., & Bauer, F. F. (2002). Glycerol in South African table wines: An assessment of its relationship to wine quality. South African Journal of Enology and Viticulture, 23, 22–30.Google Scholar
  187. Nonomura, H., Yamazaki, T., & Ohara, Y. (1967). Die Äpfelsäure-Milchsäure-Bakterien, welche aus französischen und spanischen Weinen isoliert wurden. Mitteilungen Klosterneuburg, 17A, 345–351.Google Scholar
  188. Oelofse, A., Pretorius, I. S., & du Toit, M. (2008). Significance of Brettanomyces and Dekkera during winemaking: A synoptic review. South African Journal of Enology and Viticulture, 29, 128–144.Google Scholar
  189. Oelofse, A., Lonvaud-Funel, A., & du Toit, M. (2009). Molecular identification of Brettanomyces bruxellensis strains isolated from red wines and volatile phenol production. Food Microbiology, 26, 377–385.CrossRefGoogle Scholar
  190. Olsen, E. B., Russel, J. B., & Henick-Kling, T. (1991). Electrogenic L-malate transport in Lactobacillus plantarum, a basis of energy production from malolactic fermentation. Journal of Bacteriology, 173, 6199–6206.Google Scholar
  191. Osborne, J. P., & Charles, G. E. (2007). Inhibition of malolactic fermentation by a peptide produced by Saccharomyces cerevisiae during alcoholic fermentation. International Journal of Food Microbiology, 118, 27–34.CrossRefGoogle Scholar
  192. Osborne, J. P., Mira de Orduña, R., Pilone, G. J., & Liu, S.-Q. (2000). Acetaldehyde metabolism by wine lactic acid bacteria. FEMS Microbiology Letters, 191, 51–55.CrossRefGoogle Scholar
  193. Osborne, J. P., Dubé Morneau, A., & Mira de Orduña, R. (2006). Degradation of free and sulfur-dioxide-bound acetaldehyde by malolactic lactic acid bacteria in white wine. Journal of Applied Microbiology, 101, 474–479.CrossRefGoogle Scholar
  194. Palacios, A. (2006). Organoleptic defects caused by uncontrolled malolactic fermentation. In R. Morenzoni (Ed.), Malolactic fermentation in wine—Understanding the science and the practice (pp. 7.1–7.7). Montréal: Lallemand.Google Scholar
  195. Pasteris, S. E., & Strasser de Saad, A. M. (1997). Enzymatic activities involved in glycerol utilization by Pediococcus pentosaceus from Argentinean wine. Microbiologie, Aliments, Nutrition, 15, 139–145.Google Scholar
  196. Pasteris, S. E., & Strasser de Saad, A. M. (2005). Aerobic glycerol catabolism by Pediococcus pentosaceus from wine. Food Microbiology, 22, 399–407.CrossRefGoogle Scholar
  197. Pasteris, S. E., & Strasser de Saad, A. M. (2009). Sugar-glycerol cofermentations by Lactobacillus hilgardii isolated from wine. Journal of Agricultural and Food Chemistry, 57, 3853–3858.CrossRefGoogle Scholar
  198. Peynaud, E., & Domercq, S. (1967). Etude de quelques coques homolactiques isolés de vins. Revue des Fermentations et des Industries Alimentaires, 22, 133–140.Google Scholar
  199. Peynaud, E., & Domercq, S. (1968). Étude de quatre cents souches de coques hétérolactiques isolés de vins. Annales de l’Institut Pasteur de Lille, 19, 159–170.Google Scholar
  200. Peynaud, E., & Sapis-Domercq, S. (1970). Etude de deux cent cinquante souches de bacilles hétérolactiques isolés de vins. Archives of Microbiology, 70, 348–360.Google Scholar
  201. Phadtare, S., Tyagi, S., Inouye, M., & Severinov, K. (2002). Three amino acids in Escherichia coli CspE surface-exposed aromatic patch are critical for nucleic acid melting activity leading to transcription antitermination and cold acclimation of cells. The Journal of Biological Chemistry, 277, 46706–46711.CrossRefGoogle Scholar
  202. Pilone, G. J., & Kunkee, R. E. (1976). Stimulatory effect of malo-lactic fermentation on the growth rate of Leuconostoc oenos. Applied and Environmental Microbiology, 32, 405–408.Google Scholar
  203. Plumed-Ferrer, C., Koistinen, K. M., Tolonen, T. L., Lehesranta, S. J., Kärenlampi, S. O., Mäkimattila, E., et al. (2008). Comparative study of sugar fermentations and protein expression patterns of two Lactobacillus plantarum strains grown in three different media. Applied and Environmental Microbiology, 74, 5349–5358.CrossRefGoogle Scholar
  204. Powell, C., Van Zandycke, S., & Degré, R. (2006). The microbiology of malolactic fermentation. In R. Morenzoni (Ed.), Malolactic fermentation in wine—Understanding the science and the practice (pp. 5.1–5.11). Montréal: Lallemand.Google Scholar
  205. Pozo-Bayón, M. Á., Pardo, I., Ferrer, S., & Moreno-Arribas, M. V. (2009). Molecular approaches for the identification and characterisation of oenological lactic acid bacteria. African Journal of Biotechnology, 8, 3995–4001.Google Scholar
  206. Prahl, C. (1988). Method of inducing the decarboxylation of malic acid in must or fruit juice. European patent filed 24.01.1989, priority 25.01.1988, International application number PCT/DK89/00009.Google Scholar
  207. Prahl, C. (1989). La décarboxylation de l’acide L-malique dans le moût par l’ensemencement de lactobacilles homofermentaires. Revue des Œnologues, 54, 13–17.Google Scholar
  208. Pressman, D., & Lucas, H. J. (1942). Hydration of unsaturated compounds. XI. Acrolein and acrylic acid. Journal of the American Chemical Society, 64, 1953–1957.CrossRefGoogle Scholar
  209. Pripis-Nicolau, L., De Revel, G., Bertrand, A., & Lonvaud-Funel, A. (2004). Methionine catabolism and production of volatile sulphur compounds by Oenococcus oeni. Journal of Applied Microbiology, 96, 1176–1184.CrossRefGoogle Scholar
  210. Radler, F. (1966). Die mikrobiologischen grundlagen des säureabbaus in wein. Zentralblatt für Bakteriologie, Parasitenkunde, 120, 237–287.Google Scholar
  211. Radler, F. (1990a). Possible use of nisin in winemaking. I. Action of nisin against lactic acid bacteria and wine yeasts in solid and liquid media. American Journal of Enology and Viticulture, 41, 1–6.Google Scholar
  212. Radler, F. (1990b). Possible use of nisin in winemaking. II. Experiments to control lactic acid bacteria in the production of wine. American Journal of Enology and Viticulture, 41, 7–11.Google Scholar
  213. Radler, F., & Yannissis, C. (1972). Weinsäureabbau bei Milchsäurebakterien. Archives of Microbiology, 82, 219–238.Google Scholar
  214. Ramos, A., & Santos, H. (1996). Citrate and sugar cofermentation in Leuconostoc oenos, a 13 C nuclear magnetic resonance study. Applied and Environmental Microbiology, 62, 2577–2585.Google Scholar
  215. Ramos, A., Lolkema, J. S., Konings, W. N., & Santos, H. (1995). Enzyme basis for pH regulation of citrate and pyruvate metabolism by Leuconostoc oenos. Applied and Environmental Microbiology, 61, 1303–1310.Google Scholar
  216. Rankine, B. C., & Pocock, K. F. (1969). Influence of yeast strain on binding sulphur dioxide in wines, and on its formation during fermentation. Journal of the Science of Food and Agriculture, 10, 204–109.Google Scholar
  217. Ribéreau-Gayon, J., Peynaud, E., Ribéreau-Gayon, P., & Sudraud, P. (1975). Sciences et techniques du vin, vol 2. Paris: Dunod.Google Scholar
  218. Ribéreau-Gayon, P., Dubourdieu, D., Donèche, B., & Lonvaud, A. (2006). In P. Ribéreau-Gayon (Ed.), Handbook of enology, vol. 1. The microbiology of wine and vinifications. Chichester: Wiley.CrossRefGoogle Scholar
  219. Riesen, R. (1992). Undesirable fermentation aromas. In T. Henick-Kling (Ed.), Proceedings of the ASEV/ES workshop: Wine aroma defects (pp. 1–43). Corning: American Society of Enology and Viticulture.Google Scholar
  220. Rodas, A. M., Ferrer, S., & Pardo, I. (2003). 16S-ARDRA, a tool for identification of lactic acid bacteria isolated from grape must and wine. Systematic and Applied Microbiology, 26, 412–422.CrossRefGoogle Scholar
  221. Rodas, A. M., Chenoll, E., Macián, M. C., Ferrer, S., Pardo, I., & Aznar, R. (2006). Lactobacillus vini sp. nov., a wine lactic acid bacterium homofermentative for pentoses. International Journal of Systematic and Evolutionary Microbiology, 56, 513–517.CrossRefGoogle Scholar
  222. Rojo-Bezares, B., Saenz, Y., Zarazaga, M., Torres, C., & Ruiz-Larrea, F. (2007). Antimicrobial activity of nisin against Oenococcus oeni and other wine bacteria. International Journal of Food Microbiology, 116, 32–36.CrossRefGoogle Scholar
  223. Rojo-Bezares, B., Sáenz, Y., Navarro, L., Jiménez-Díaz, R., Zarazaga, M., Ruiz-Larrea, F., et al. (2008). Characterization of a new organization of the plantaricin locus in the inducible bacteriocin-producing Lactobacillus plantarum J23 of grape must origin. Archives of Microbiology, 189, 491–499.CrossRefGoogle Scholar
  224. Romero, S. V., Reguant, C., Bordons, A., & Masqué, M. C. (2009). Potential formation of ethyl carbamate in simulated wine inoculated with Oenococcus oeni and Lactobacillus plantarum. International Journal of Food Science & Technology, 44, 1206–1213.CrossRefGoogle Scholar
  225. Rosi, I., Gheri, A., Domizio, P., & Pia, G. (1999). Production de macromolécules pariétales de Saccharomyces cerevisiae au cours de la fermentation et leur influence sur la fermentation malolactique. Revue des Œnologues, 94, 18–20.Google Scholar
  226. Rosi, I., Nannelli, F., & Giovani, G. (2009). Biogenic amine production by Oenococcus oeni during malolactic fermentation of wines obtained using different strains of Saccharomyces cerevisiae. Food Science and Technology, 42, 525–530.Google Scholar
  227. Ruiz, P., Izquierdo, P. M., Seseña, S., & Palop, M. L. (2008). Intraspecific genetic diversity of lactic acid bacteria from malolactic fermentation of Cencibel wines as derived from combined analysis of RAPD-PCR and PFGE pattern. Food Microbiology, 25, 942–948.CrossRefGoogle Scholar
  228. Ruiz, P., Izquierdo, P. M., Seseña, S., & Palop, M. L. (2010). Analysis of lactic acid bacteria populations during spontaneous malolactic fermentation of Tempranillo wines at five wineries during two consecutive vintages. Food Control, 21, 70–75.CrossRefGoogle Scholar
  229. Sáenz, Y., Rojo-Bezares, B., Navarro, L., Díez, L., Somalo, S., Zarazaga, M., et al. (2009). Genetic diversity of the pln locus among oenological Lactobacillus plantarum strains. International Journal of Food Microbiology, 134, 176–183.CrossRefGoogle Scholar
  230. Salado, A. I. C., & Strasser de Saad, A. M. (1995). Glycerol utilization by Pediococcus pentosaceus strains isolated from Argentinean wines. Microbiologie, Aliments, Nutrition, 13, 319–325.Google Scholar
  231. Sauvageot, N., Gouffi, K., Lapace, J.-M., & Auffray, Y. (2000). Glycerol metabolism in Lactobacillus collinoides: Production of 3-hydroxypropionaldehyde, a precursor of acrolein. International Journal of Food Microbiology, 55, 167–170.CrossRefGoogle Scholar
  232. Schütz, H., & Radler, F. (1984). Anaerobic reduction of glycerol to propandiol-1, 3 by Lactobacillus brevis and Lactobacillus buchneri. Systematic and Applied Microbiology, 5, 169–178.Google Scholar
  233. Seaman, V., Charles, M., & Cahill, T. A. (2006). A sensitive method for the quantification of acrolein and other volatile carbonyls in ambient air. Analytical Chemistry, 78, 2405–2412.CrossRefGoogle Scholar
  234. Shalaby, A. R. (1996). Significance of biogenic amines to food safety and human health. Food Research International, 29, 675–690.CrossRefGoogle Scholar
  235. Silva, H. A. D. F. O., & Álvares-Ribeiro, L. M. B. C. (2002). Optimization of a flow injection analysis system for tartaric acid determination in wines. Talanta, 58, 1311–1318.CrossRefGoogle Scholar
  236. Silva, A., Lambri, M., & Fumi, M. D. (2007). Ochratoxin A decontamination by lactic acid bacteria in wine: Adsorption or biodegradation? Proceeding Oeno 2007 VIII Symposium Internationaòl d’Oenologie-Bordeaux, pp. 24–27 Juin Paris Ed Tec & DOC.Google Scholar
  237. Smit, A. Y., Du Toit, W. J., & Du Toit, M. (2008). Biogenic amines in wine: Understanding the headache. South African Journal of Oenology and Viticulture, 29, 109–127.Google Scholar
  238. Snelten, H. J., & Schaafsma, G. (1992). Health aspects of oral sulphite and sulphite in wine. Voeding, 53, 88–90.Google Scholar
  239. Sobolov, M., & Smiley, K. L. (1960). Metabolism of glycerol by an acrolein-forming Lactobacillus. Journal of Bacteriology, 79, 261–266.Google Scholar
  240. Spano, G., & Massa, S. (2006). Environmental stress response in wine lactic acid bacteria: Beyond Bacillus subtilis. Critical Reviews in Microbiology, 32, 77–86.CrossRefGoogle Scholar
  241. Spano, G., Rinaldi, A., Ugliano, M., Moio, L., Beneduce, L., & Massa, S. (2005). A β-glucosidase gene isolated from wine Lactobacillus plantarum is regulated by abiotic stresses. Journal of Applied Microbiology, 98, 855–861.CrossRefGoogle Scholar
  242. Splittstoesser, D. F., & Stoyla, B. A. (1989). Effect of various inhibitors on the growth of lactic acid bacteria in a model grape juice system. Journal of Food Protection, 52, 240–243.Google Scholar
  243. Sponholz, W.-R. (1993). In G. H. Fleet (Ed.), Wine microbiology and technology (pp. 395–420). Amsterdam: Harwood Academic.Google Scholar
  244. Starrenburg, M. J. C., & Hugenholtz, J. (1991). Citrate fermentation by Lactococcus and Leuconostoc spp. Applied and Environmental Microbiology, 57, 3535–3540.Google Scholar
  245. Strasser de Saad, A. M., & Manca de Nadra, M. C. (1993). Characterization of bacteriocin produced by Pediococcus pentosaceus from wine. The Journal of Applied Bacteriology, 74, 406–410.Google Scholar
  246. Straub, B. W., Kicherer, M., Schilcher, S. M., & Hammes, W. P. (1995). The formation of biogenic amines by fermentation organisms. Zeitschrift fur Lebensmittel-Untersuchung und -Forschung, 201, 79–82.CrossRefGoogle Scholar
  247. Swiegers, J. H., Bartowsky, E. J., Henschke, P. A., & Pretorius, I. S. (2005). Yeast and bacterial modulation of wine aroma and flavour. Australian Journal of Grape and Wine Research, 11, 139–173.CrossRefGoogle Scholar
  248. Ten Brink, B., Damink, C., Joosten, H. M. L. J., & Huis in ’t Veld, J. H. J. (1990). Occurrence and formation of biologically active amines in foods. International Journal of Food Microbiology, 11, 73–84.CrossRefGoogle Scholar
  249. Terrade, N., & Mira de Orduña, R. (2009). Determination of the essential nutrient requirements of wine-related bacteria from the genera Oenococcus and Lactobacillus. International Journal of Food Microbiology, 133, 8–13.CrossRefGoogle Scholar
  250. Tonon, T., & Lonvaud-Funel, A. (2002). Arginine metabolism by wine Lactobacilli isolated from wine. Food Microbiology, 19, 451–461.CrossRefGoogle Scholar
  251. Ugliano, M., & Moio, L. (2005). Changes in the concentration of yeast-derived volatile compounds of red wine during malolactic fermentation with four commercial starter cultures of Oenococcus oeni. Journal of Agricultural and Food Chemistry, 53, 10134–10139.CrossRefGoogle Scholar
  252. Uthurry, C. A., Suárez Lepe, J. A., Lombardero, J., & Garcia Del Hierro, J. R. (2006). Ethyl carbamate production by selected yeasts and lactic acid bacteria in red wine. Food Chemistry, 94, 262–270.Google Scholar
  253. Vaillant, H., Formisyn, P., & Gerbaux, V. (1995). Malolactic fermentation of wine: Study of the influence of some physico-chemical factors by experimental design assays. The Journal of Applied Bacteriology, 79, 640–650.Google Scholar
  254. Vallet, A., Lucas, P., Lonvaud-Funel, A., & De Revel, G. (2008). Pathways that produce volatile sulphur compounds from methionine in Oenococcus oeni. Journal of Applied Microbiology, 104, 1833–1840.CrossRefGoogle Scholar
  255. Vallet, A., Santarelli, X., Lonvaud-Funel, A., de Revel, G., & Cabanne, C. (2009). Purification of an alcohol dehydrogenase involved in the conversion of methional to methionol in Oenococcus oeni IOEB 8406. Applied Microbiology and Biotechnology, 82, 87–94.CrossRefGoogle Scholar
  256. Van de Guchte, M., Serror, P., Chervaux, C., Smokvina, T., Ehrlich, S. D., & Maguin, E. (2002). Stress responses in lactic acid bacteria. Antonie van Leeuwenhoek, 82, 187–216.CrossRefGoogle Scholar
  257. Van Vuuren, H. J. J., & Dicks, L. M. T. (1993). Leuconostoc oenos: A review. American Journal of Enology and Viticulture, 44, 99–112.Google Scholar
  258. Vaquero, I., Marcobal, A., & Muñoz, R. (2004). Tannase activity by lactic acid bacteria isolated from grape must and wine. International Journal of Food Microbiology, 96, 199–204.CrossRefGoogle Scholar
  259. Vaughn, R. H. (1955). Bacterial spoilage of wines with special reference to California conditions. Advances in Food Research, 6, 67–108.Google Scholar
  260. Vivas, N., Augustin, M., & Lonvaud-Funel, A. (2000). Influence of oak wood and grape tannins on the lactic acid bacterium Oenococcus oeni (Leuconostoc oenos, 8413). Journal of the Science of Food and Agriculture, 80, 1675–1678.CrossRefGoogle Scholar
  261. Vollenweider, S., Grassi, G., König, I., & Puhan, Z. (2003). Purification and structural characterization of 3-hydroxypropionaldehyde and its derivatives. Journal of Agricultural and Food Chemistry, 51, 3287–3293.CrossRefGoogle Scholar
  262. Volschenk, H., van Vuuren, H. J. J., & Viljoen-Bloom, M. (2006). Malic acid in wine: Origin, function and metabolism during vinification. South African Journal of Enology and Viticulture, 27, 123–136.Google Scholar
  263. Waterhouse, A. L. (2002). Wine phenolics. Annals of the New York Academy of Sciences, 957, 21–36.CrossRefGoogle Scholar
  264. Weimer, B., Seefeldt, K., & Dias, B. (1999). Sulfur metabolism in bacteria associated with cheese. Antonie van Leeuwenhoek, 76, 247–261.CrossRefGoogle Scholar
  265. Wibowo, D., Eschenbruch, R., Davis, D. R., Fleet, G. H., & Lee, T. H. (1985). Occurrence and growth of lactic acid bacteria in wine: A review. American Journal of Enology and Viticulture, 36, 302–313.Google Scholar
  266. Wisselink, H. W., Weusthuis, R. A., Eggink, G., Hugenholtz, J., & Grobben, G. J. (2002). Mannitol production by lactic acid bacteria: A review. International Dairy Journal, 12, 151–161.CrossRefGoogle Scholar
  267. Yurdugül, S., & Bozoglu, F. (2002). Studies on an inhibitor produced by lactic acid bacteria of wines on the control of malolactic fermentation. European Food Research and Technology, 215, 38–41.CrossRefGoogle Scholar

Copyright information

© Springer Science + Business Media, LLC 2010

Authors and Affiliations

  • Maret du Toit
    • 1
  • Lynn Engelbrecht
    • 1
  • Elda Lerm
    • 1
  • Sibylle Krieger-Weber
    • 2
  1. 1.Institute for Wine BiotechnologyStellenbosch UniversityStellenboschSouth Africa
  2. 2.LallemandKorntal-MünchingenGermany

Personalised recommendations