Applied Microbiology and Biotechnology

, Volume 98, Issue 19, pp 8111–8132 | Cite as

Implications of new research and technologies for malolactic fermentation in wine

  • Krista M. Sumby
  • Paul R. Grbin
  • Vladimir Jiranek
Mini-Review

Abstract

The initial conversion of grape must to wine is an alcoholic fermentation (AF) largely carried out by one or more strains of yeast, typically Saccharomyces cerevisiae. After the AF, a secondary or malolactic fermentation (MLF) which is carried out by lactic acid bacteria (LAB) is often undertaken. The MLF involves the bioconversion of malic acid to lactic acid and carbon dioxide. The ability to metabolise l-malic acid is strain specific, and both individual Oenococcus oeni strains and other LAB strains vary in their ability to efficiently carry out MLF. Aside from impacts on acidity, LAB can also metabolise other precursors present in wine during fermentation and, therefore, alter the chemical composition of the wine resulting in an increased complexity of wine aroma and flavour. Recent research has focused on three main areas: enzymatic changes during MLF, safety of the final product and mechanisms of stress resistance. This review summarises the latest research and technological advances in the rapidly evolving study of MLF and investigates the directions that future research may take.

Keywords

Oenococcus oeni Lactobacillus Malolactic fermentation Wine 

References

  1. Abrahamse C, Bartowsky E (2012) Timing of malolactic fermentation inoculation in Shiraz grape must and wine: influence on chemical composition. World J Microbiol Biotechnol 28:255–265PubMedGoogle Scholar
  2. Agouridis N, Kopsahelis N, Plessas S, Koutinas AA, Kanellaki M (2008) Oenococcus oeni cells immobilized on delignified cellulosic material for malolactic fermentation of wine. Bioresour Technol 99:9017–9020PubMedGoogle Scholar
  3. Alegría GE, López I, Ruiz JI, Sáenz J, Fernández E, Zarazaga M, Dizy M, Torres C, Ruiz-Larrea F (2004) High tolerance of wild Lactobacillus plantarum and Oenococcus oeni strains to lyophilisation and stress environmental conditions of acid pH and ethanol. FEMS Microbiol Lett 230:53–61Google Scholar
  4. Ancín-Azpilicueta C, González-Marco A, Jiménez-Moreno N (2008) Current knowledge about the presence of amines in wine. Crit Rev Food Sci Nutr 48:257–275PubMedGoogle Scholar
  5. Araque I, Bordons A, Reguant C (2013) Effect of ethanol and low pH on citrulline and ornithine excretion and arc gene expression by strains of Lactobacillus brevis and Pediococcus pentosaceus. Food Microbiol 33:107–113PubMedGoogle 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. J Agric Food Chem 57:1841–1847PubMedGoogle Scholar
  7. Arena ME, Lisi MS, Manca de Nadra MC, Alberto MR (2013) Wine composition plays an important role in the control of carcinogenic precursor formation by Lactobacillus hilgardii X1B. J Sci Food Agric 93:142–148Google Scholar
  8. Arevalo-Villena M, Bartowsky EJ, Capone D, Sefton MA (2010) Production of indole by wine-associated microorganisms under oenological conditions. Food Microbiol 27:685–690PubMedGoogle Scholar
  9. Assad-García JS, Bonnin-Jusserand M, Garmyn D, Guzzo J, Alexandre H, Grandvalet C (2008) An improved protocol for electroporation of Oenococcus oeni ATCC BAA-1163 using ethanol as immediate membrane fluidizing agent. Lett Appl Microbiol 47:333–338PubMedGoogle Scholar
  10. Augagneur Y, Ritt J-F, 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 188:147–157PubMedGoogle Scholar
  11. Bachmann H, Starrenburg MJC, Molenaar D, Kleerebezem M, van Hylckama Vlieg JET (2012) Microbial domestication signatures of Lactococcus lactis can be reproduced by experimental evolution. Genome Res 22:115–124PubMedPubMedCentralGoogle Scholar
  12. Bartowsky E (2005) Oenococcus oeni and malolactic fermentation—moving into the molecular arena. Aust J Grape Wine Res 11:174–187Google Scholar
  13. Bartowsky E, Borneman A (2011) Genomic variations of Oenococcus oeni strains and the potential to impact on malolactic fermentation and aroma compounds in wine. Appl Microbiol Biotechnol 92:441–447PubMedGoogle Scholar
  14. Bartowsky E, Stockley C (2011) Histamine in Australian wines—a survey between 1982 and 2009. Ann Microbiol 61:167–172Google Scholar
  15. Beltramo C, Desroche N, Tourdot-Marechal R, Grandvalet C, Guzzo J (2006) Real-time PCR for characterizing the stress response of Oenococcus oeni in a wine-like medium. Res Microbiol 157:267–274PubMedGoogle Scholar
  16. Beltramo C, Grandvalet C, Pierre F, Guzzo J (2004a) Evidence for multiple levels of regulation of Oenococcus oeni clpP-clpL locus expression in response to stress. J Bacteriol 186:2200–2205PubMedPubMedCentralGoogle Scholar
  17. Beltramo C, Oraby M, Bourel G, Garmyn D, Guzzo J (2004b) A new vector, pGID052, for genetic transfer in Oenococcus oeni. FEMS Microbiol Lett 236:53–60PubMedGoogle Scholar
  18. Beneduce L, Romano A, Capozzi V, Lucas P, Barnavon L, Bach B, Vuchot P, Grieco F, Spano G (2010) Biogenic amine in wines. Ann Microbiol 60:573–578Google Scholar
  19. Betteridge AL, Grbin PR, Jiranek V (2013) Enhanced winemaking efficiency: evolution of a superior lactic acid bacteria. Conference proceedings, 15th Aust Wine Ind Tech Confer, Sydney NSW, 13–18th JulyGoogle Scholar
  20. Bisson LF (1999) Stuck and sluggish fermentations. Am J Enol Vitic 50:107–119Google Scholar
  21. Bock A, Sparks T, Estrella N, Menzel A (2011) Changes in the phenology and composition of wine from Franconia, Germany. Clim Res 50:69–81Google Scholar
  22. Boekhorst J, Siezen RJ, Zwahlen M-C, Vilanova D, Pridmore RD, Mercenier A, Kleerebezem M, de Vos WM, Brüssow H, Desiere F (2004) The complete genomes of Lactobacillus plantarum and Lactobacillus johnsonii reveal extensive differences in chromosome organization and gene content. Microbiol 150:3601–3611Google Scholar
  23. Bon E, Delaherche A, Bilhere E, De Daruvar A, Lonvaud-Funel A, Le Marrec C (2009) Oenococcus oeni genome plasticity is associated with fitness. Appl Environ Microbiol 75:2079–2090PubMedPubMedCentralGoogle Scholar
  24. Borneman A, Bartowsky E, McCarthy J, Chambers P (2010) Genotypic diversity in Oenococcus oeni by high-density microarray comparative genome hybridization and whole genome sequencing. Appl Microbiol Biotechnol 86:681–691PubMedGoogle Scholar
  25. Borneman AR, McCarthy JM, Chambers PJ, Bartowsky EJ (2012a) Comparative analysis of the Oenococcus oeni pan genome reveals genetic diversity in industrially-relevant pathways. BMC Genomics 13, doi:10.1186/1471-2164-1113-1373Google Scholar
  26. Borneman AR, McCarthy JM, Chambers PJ, Bartowsky EJ (2012b) Functional divergence in the genus Oenococcus as predicted by genome sequencing of the newly-described species, Oenococcus kitaharae. PLoS ONE 7:e29626. doi:10.1371/journal.pone.0029626 PubMedPubMedCentralGoogle Scholar
  27. Bourdineaud J-P (2006) Both arginine and fructose stimulate pH-independent resistance in the wine bacteria Oenococcus oeni. Int J Food Microbiol 107:274–280PubMedGoogle Scholar
  28. Bourdineaud J-P, Nehme B, Tesse S, Lonvaud-Funel A (2003) The ftsH gene of the wine bacterium Oenococcus oeni is involved in protection against environmental stress. Appl Environ Microbiol 69(5):2512–2520. doi:10.1128/AEM.69.5.2512-2520.2003 PubMedPubMedCentralGoogle Scholar
  29. Bourdineaud J-P, Nehme B, Tesse S, Lonvaud-Funel A (2004) A bacterial gene homologous to ABC transporters protect Oenococcus oeni from ethanol and other stress factors in wine. Int J Food Microbiol 92:1–14PubMedGoogle Scholar
  30. Branco P, Francisco D, Chambon C, Hébraud M, Arneborg N, Almeida M, Caldeira J, Albergaria H (2014) Identification of novel GAPDH-derived antimicrobial peptides secreted by Saccharomyces cerevisiae and involved in wine microbial interactions. Appl Microbiol Biotechnol 98:843–853PubMedGoogle Scholar
  31. Bravo-Ferrada B, Hollmann A, Delfederico L, Valdés La Hens D, Caballero A, Semorile L (2013) Patagonian red wines: selection of Lactobacillus plantarum isolates as potential starter cultures for malolactic fermentation. World J Microbiol Biotechnol 29(9):1537–1549. doi:10.1007/s11274-013-1337-x. Epub 2013 Apr 2 PubMedGoogle Scholar
  32. Britz TJ, Tracey RP (1990) The combination effect of pH, SO2 ethanol and temperature on the growth of Leuconostoc oenos. J Appl Bacteriol 68:23–31Google Scholar
  33. Buron N, Coton M, Legendre P, Ledauphin J, Kientz-Bouchart V, Guichard H (2012) Implications of Lactobacillus collinoides and Brettanomyces/Dekkera anomala in phenolic off-flavour defects of ciders. Int J Food Microbiol 153(1–2):159–165PubMedGoogle Scholar
  34. Cabras P, Meloni M, Melis M, Farris GA, Budroni M, Satta T (1994) Interactions between lactic bacteria and fungicides during lactic fermentation. J Wine Res 5(1):53–59Google Scholar
  35. Cafaro C, Bonomo MG, Salzano G (2014) Adaptive changes in geranylgeranyl pyrophosphate synthase gene expression level under ethanol stress conditions in Oenococcus oeni. J Appl Microbiol 116:71–80PubMedGoogle Scholar
  36. CDFA, California Agricultural Statistics Service (2013) California Department of Food and Agriculture Grape Crush Report Final 2012 Crop. www.nass.usda.gov/ca
  37. Campos FM, Couto JA, Figueiredo AR, Tóth IV, Rangel AOSS, Hogg TA (2009) Cell membrane damage induced by phenolic acids on wine lactic acid bacteria. Int J Food Microbiol 135:144–151PubMedGoogle Scholar
  38. Campos FM, Couto JA, Hogg TA (2003) Influence of phenolic acids on growth and inactivation of Oenococcus oeni and Lactobacillus hilgardii. J Appl Microbiol 94:167–174PubMedGoogle Scholar
  39. Canas BJ, Joe FL Jr, Diachenko GW, Burns G (1994) Determination of ethyl carbamate in alcoholic beverages and soy sauce by gas chromatography with mass selective detection: collaborative study. J AOAC Int 77(6):1530–1536PubMedGoogle Scholar
  40. Cañas PMI, Romero EG, Pérez-Martín F, Seseña S, Palop ML (2014) Sequential inoculation versus co-inoculation in Cabernet Franc wine fermentation. Food Sci Technol Int. doi:10.1177/1082013214524585 PubMedGoogle Scholar
  41. Cañas PMI, Pérez-Martín F, Romero EG, Prieto SS, Herreros M (2012) Influence of inoculation time of an autochthonous selected malolactic bacterium on volatile and sensory profile of Tempranillo and Merlot wines. Int J Food Microbiol 156:245–254Google Scholar
  42. Capaldo A, Walker ME, Ford CM, Jiranek V (2011a) Beta-glucoside metabolism in Oenococcus oeni: cloning and characterisation of the phospho-beta-glucosidase bgID. Food Chem 125:476–482Google Scholar
  43. Capaldo A, Walker ME, Ford CM, Jiranek V (2011b) Beta-glucoside metabolism in Oenococcus oeni: cloning and characterization of the phospho-beta-glucosidase CelD. J Mol Catal B Enzym 69:27–34Google Scholar
  44. Capone DL, Van Leeuwen KA, Pardon KH, Daniel MA, Elsey GM, Coulter AD, Sefton MA (2010) Identification and analysis of 2-chloro-6-methylphenol, 2,6-dichlorophenol and indole: causes of taints and off-flavours in wines. Aust J Grape Wine Res 16:210–217Google Scholar
  45. Capozzi V, Russo P, Ladero V, Fernández M, Fiocco D, Alvarez MA, Grieco F, Spano G (2012) Biogenic amines degradation by Lactobacillus plantarum: toward a potential application in wine. Front Microbiol 3:122. doi:10.3389/fmicb.2012.00122 PubMedPubMedCentralGoogle Scholar
  46. Cappello MS, Stefani D, Grieco F, Logrieco A, Zapparoli G (2008) Genotyping by amplified fragment length polymorphism and malate metabolism performances of indigenous Oenococcus oeni strains isolated from Primitivo wine. Int J Food Microbiol 127:241–245PubMedGoogle Scholar
  47. Capucho I, San Romão MV (1994) Effect of ethanol and fatty acids on malolactic activity of Leuconostoc oenos. Appl Microbiol Biotechnol 42:391–395Google Scholar
  48. Carr FJ, Chill D, Maida N (2002) The lactic acid bacteria: a literature survey. Crit Rev Microbiol 28:281–370PubMedGoogle Scholar
  49. Carrillo JD, Tena MT (2007) Determination of ethylphenols in wine by in situ derivatisation and headspace solid-phase microextraction-gas chromatography–mass spectrometry. Anal Bioanal Chem 387(7):2547–2558PubMedGoogle Scholar
  50. Chambers P (2011) From omics to systems biology: towards a more complete description and understanding of biology. Microbiol Aust 32:141–143Google Scholar
  51. Chatonnet P, Dubourdieu D, Boidron JN, Pons M (1992) The origin of ethylphenols in wines. J Sci Food Agric 60:165–178Google Scholar
  52. Chatonnet P, Dubourdieu D, Boidron JN (1995) The influence of Brettanomyces/Dekkera sp. yeasts and lactic acid bacteria on the ethylphenol content of red wines. Am J Enol Vitic 46:463–468Google Scholar
  53. Chatonnet P, Viala C, Dubourdieu D (1997) Influence of polyphenolic components of red wines on the microbial synthesis of volatile phenols. Am J Enol Vitic 48:443–448Google Scholar
  54. Chen H, Zhao Y, Song Y, Jiang L (2008) One-step multicomponent encapsulation by compound-fluidic electrospray. J Am Chem Soc 130:7800–7801PubMedGoogle Scholar
  55. Chu-Ky S, Tourdot-Marechal R, Marechal PA, Guzzo J (2005) Combined cold, acid, ethanol shocks in Oenococcus oeni: effects on membrane fluidity and cell viability. Biochim Biophys Acta - Biomemb 1717:118–124Google Scholar
  56. Claisse O, Lonvaud-Funel A (2012) Development of a multilocus variable number of tandem repeat typing method for Oenococcus oeni. Food Microbiol 30:340–347PubMedGoogle Scholar
  57. Claisse O, Lonvaud-Funel A (2014) Multiplex variable number of tandem repeats for Oenococcus oeni and applications. Food Microbiol 38:80–86PubMedGoogle Scholar
  58. Clauditz A, Resch A, Wieland KP, Peschel A, Gotz F (2006) Staphyloxanthin plays a role in the fitness of Staphylococcus aureus and its ability to cope with oxidative stress. Infect Immum 74:4950–4953Google Scholar
  59. Comitini F, Ciani M (2007) The inhibitory activity of wine yeast starters on malolactic bacteria. Ann Microbiol 57:61–66Google Scholar
  60. 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. J Appl Microbiol 99:105–111PubMedGoogle Scholar
  61. Costantini A, Pietroniro R, Doria F, Pessione E, Garcia-Moruno E (2013) Putrescine production from different amino acid precursors by lactic acid bacteria from wine and cider. Int J Food Microbiol 165:11–17PubMedGoogle Scholar
  62. Coton E, Coton M (2009) Evidence of horizontal transfer as origin of strain to strain variation of the tyramine production trait in Lactobacillus brevis. Food Microbiol 26:52–57PubMedGoogle Scholar
  63. Crapisi A, Nuti MP, Zamorani A, Spettoli P (1987) Improved stability of immobilized Lactobacillus sp. cells for the control of malolactic fermentation in wine. Am J Enol Vitic 38:310–312Google Scholar
  64. Curtin CD, Langhans G, Henschke PA, Grbin PR (2013) Impact of Australian Dekkera bruxellensis strains grown under oxygen-limited conditions on model wine composition and aroma. Food Microbiol 36(2):241–247PubMedGoogle Scholar
  65. Couto JA, Campos FM, Figueiredo AR, Hogg TA (2006) Ability of lactic acid bacteria to produce volatile phenols. Am J Enol Vitic 57:166–171Google Scholar
  66. Dähne L, Peyratout CS (2004) Tailor-made polyelectrolyte microcapsules: from multilayers to smart containers. Angew Chem Int Ed 43:3762–3783Google Scholar
  67. Da Silveira MG, Baumgärtner M, Rombouts FM, Abee T (2004) Effect of adaptation to ethanol on cytoplasmic and membrane protein profiles of Oenococcus oeni. Appl Environ Microbiol 70:2748–2755PubMedPubMedCentralGoogle Scholar
  68. Davis CR, Wibowo D, Eschenbruch R, Lee TH, Fleet GH (1985) Practical implications of malolactic fermentation: a review. Am J Enol Vitic 36:290–301Google Scholar
  69. de las Rivas B, Marcobal A, Muñoz R (2004) Allelic diversity and population structure in Oenococcus oeni as determined from sequence analysis of housekeeping genes. Appl Environ Microbiol 70:7210–7219PubMedCentralGoogle Scholar
  70. Desroche N, Beltramo C, Guzzo J (2005) Determination of an internal control to apply reverse transcription quantitative PCR to study stress response in the lactic acid bacterium Oenococcus oeni. J Microbiol Methods 60:325–333PubMedGoogle Scholar
  71. Dicks L (1994) Transformation of Leuconostoc oenos by electroporation. Biotechnol Tech 8:901–904Google Scholar
  72. Di Gennaro SF, Matese A, Primicerio J, Genesio L, Sabatini F, Di Blasi S, Vaccari FP (2013) Wireless real-time monitoring of malolactic fermentation in wine barrels: the Wireless Sensor Bung system. Aust J Grape Wine Res 19:20–24Google Scholar
  73. Dott W, Heinzel M, Trüper H (1976) Sulfite formation by wine yeasts. Arch Microbiol 107:289–292Google Scholar
  74. Dragosits M, Mattanovich D (2013) Adaptive laboratory evolution—principles and applications for biotechnology. Microb Cell Fact 12:64. doi:10.1186/1475-2859-12-64 PubMedPubMedCentralGoogle Scholar
  75. du Plessis HW, Dicks LMT, Pretorius IS, Lambrechts MG, du Toit M (2004) Identification of lactic acid bacteria isolated from South African brandy base wines. Int J Food Microbiol 91:19–29PubMedGoogle Scholar
  76. du Toit M, Engelbrecht L, Lerm E, Krieger-Weber S (2011) Lactobacillus: the next generation of malolactic fermentation starter cultures—an overview. Food Bioprocess Technol 4:876–906Google Scholar
  77. El Gharniti F, Dols-Lafargue M, Bon E, Claisse O, Miot-Sertier C, Lonvaud A, Le Marrec C (2012) IS30 elements are mediators of genetic diversity in Oenococcus oeni. Int J Food Microbiol 158:14–22PubMedGoogle Scholar
  78. Eom H-J, Cho S, Park M, Ji G, Han N (2010) Characterization of Leuconostoc citreum plasmid pCB18 and development of broad host range shuttle vector for lactic acid bacteria. Biotechnol Bioprocess Eng 15:946–952Google Scholar
  79. Figueiredo AR, Campos F, de Freitas V, Hogg T, Couto JA (2008) Effect of phenolic aldehydes and flavonoids on growth and inactivation of Oenococcus oeni and Lactobacillus hilgardii. Food Microbiol 25:105–112PubMedGoogle Scholar
  80. Fiocco D, Capozzi V, Goffin P, Hols P, Spano G (2007) Improved adaptation to heat, cold, and solvent tolerance in Lactobacillus plantarum. Appl Microbiol Biotechnol 77:909–915PubMedGoogle Scholar
  81. Formisyn P, Vaillant H, Laintreibecq F, Bourgois J (1997) Development of an enzymatic reactor for initiating malolactic fermentation in wine. Am J Enol Vitic 48:345–351Google Scholar
  82. Fortier LC, Tourdot-Marechal R, Divies C, Lee BH, Guzzo J (2003) Induction of Oenococcus oeni H+-ATPase activity and mRNA transcription under acidic conditions. FEMS Microbiol Lett 222:165–169PubMedGoogle Scholar
  83. Foster PL (1999) Mechanisms of stationary phase mutation: a decade of adaptive mutation. Annu Rev Genet 33:57–88PubMedPubMedCentralGoogle Scholar
  84. Fras P, Campos F, Hogg T, Couto J (2014) Production of volatile phenols by Lactobacillus plantarum in wine conditions. Biotechnol Lett 36:281–285PubMedGoogle Scholar
  85. Gagne S, Lucas PM, Perello MC, Claisse O, Lonvaud-Funel A, de Revel G (2011) Variety and variability of glycosidase activities in an Oenococcus oeni strain collection tested with synthetic and natural substrates. J Appl Microbiol 110:218–228PubMedGoogle Scholar
  86. Gamella M, Campuzano S, Conzuelo F, Curiel JA, Muñoz R, Reviejo AJ, Pingarrón JM (2010) Integrated multienzyme electrochemical biosensors for monitoring malolactic fermentation in wines. Talanta 81:925–933PubMedGoogle Scholar
  87. García-Ruiz A, González-Rompinelli EM, Bartolomé B, Moreno-Arribas MV (2011) Potential of wine-associated lactic acid bacteria to degrade biogenic amines. Int J Food Microbiol 148:115–120PubMedGoogle Scholar
  88. Genisheva Z, Mussatto SI, Oliveira JM, Teixeira JA (2013) Malolactic fermentation of wines with immobilised lactic acid bacteria—influence of concentration, type of support material and storage conditions. Food Chem 138:1510–1514PubMedGoogle Scholar
  89. Godoy L, Martinez C, Carrasco N, Ganga M (2008) Purification and characterization of a p-coumarate decarboxylase and a vinylphenol reductase from Brettanomyces bruxellensis. Int J Food Microbiol 127:6–11PubMedGoogle Scholar
  90. González-Arenzana L, López R, Santamaría P, López-Alfaro I (2013a) Dynamics of lactic acid bacteria populations in Rioja wines by PCR-DGGE, comparison with culture-dependent methods. Appl Microbiol Biotechnol 97(15):6931–6941PubMedGoogle Scholar
  91. González-Arenzana L, Santamaría P, López R, López-Alfaro I (2013b) Indigenous lactic acid bacteria communities in alcoholic and malolactic fermentations of Tempranillo wines elaborated in ten wineries of La Rioja (Spain). Food Res Int 50:438–445Google Scholar
  92. González-Arenzana L, Santamaría P, López R, López-Alfaro I (2014) Oenococcus oeni strain typification by combination of multilocus sequence typing and pulsed field gel electrophoresis analysis. Food Microbiol 38:295–302PubMedGoogle Scholar
  93. Gosalbes MJ, Esteban CD, Galán JL, Pérez-Martínez G (2000) Integrative food-grade expression system based on the lactose regulon of Lactobacillus casei. Appl Environ Microbiol 66(11):4822–4828PubMedPubMedCentralGoogle Scholar
  94. Grandvalet C, Assad-Garcia JS, Chu-Ky S, Tollot M, Guzzo J, Gresti J, Tourdot-Marechal R (2008) Changes in membrane lipid composition in ethanol- and acid-adapted Oenococcus oeni cells: characterization of the cfa gene by heterologous complementation. Microbiol 154:2611–2619Google Scholar
  95. Grandvalet C, Coucheney F, Beltramo C, Guzzo J (2005) CtsR is the master regulator of stress response gene expression in Oenococcus oeni. J Bacteriol 187:5614–5623PubMedPubMedCentralGoogle Scholar
  96. Grimaldi A, Bartowsky E, Jiranek V (2005a) Screening of Lactobacillus spp. and Pediococcus spp. for glycosidase activities that are important in oenology. J Appl Microbiol 99:1061–1069PubMedGoogle Scholar
  97. Grimaldi A, Bartowsky E, Jiranek V (2005b) A survey of glycosidase activities of commercial wine strains of Oenococcus oeni. Int J Food Microbiol 105:233–244PubMedGoogle Scholar
  98. Grimaldi A, McLean H, Jiranek V (2000) Identification and partial characterization of glycosidic activities of commercial strains of the lactic acid bacterium, Oenococcus oeni. Am J Enol Vitic 51:362–369Google Scholar
  99. Grobler J, Bauer F, Subden RE, Van Vuuren HJJ (1995) The mae1 gene of Schizosaccharomyces pombe encodes a permease for malate and other C4 dicarboxylic acids. Yeast 11:1485–1491PubMedGoogle Scholar
  100. Guzzo J, Jobin M-P, Delmas F, Fortier L-C, Garmyn D, Tourdot-Marechal R, Lee B, Divies C (2000) Regulation of stress response in Oenococcus oeni as a function of environmental changes and growth phase. Int J Food Microbiol 55:27–31PubMedGoogle Scholar
  101. Guzzon R, Carturan G, Krieger-Weber S, Cavazza A (2012) Use of organo-silica immobilized bacteria produced in a pilot scale plant to induce malolactic fermentation in wines that contain lysozyme. Ann Microbiol 62:381–390Google Scholar
  102. Hagi T, Kobayashi M, Kawamoto S, Shima J, Nomura M (2013) Expression of novel carotenoid biosynthesis genes from Enterococcus gilvus improves the multistress tolerance of Lactococcus lactis. J Appl Microbiol 114:1763–1771PubMedGoogle Scholar
  103. Harris V, Ford CM, Jiranek V, Grbin PR (2008) Survey of enzyme activity responsible for phenolic off-flavour production by Dekkera and Brettanomyces yeast. Appl Microbiol Biotechnol 81(6):1117–1127PubMedGoogle Scholar
  104. Henschke PA, Jiranek V (1993) Yeasts—metabolism of nitrogen compounds. In: Fleet GH (ed) Wine microbiology and biotechnology. Harwood Academic, Chur, pp 77–163Google Scholar
  105. Heresztyn T (1986) Metabolism of volatile phenolic compounds from hydroxycinnamic acids by Brettanomyces yeast. Arch Microbiol 146:96–98Google Scholar
  106. Husnik JI, Delaquis PJ, Cliff MA, van Vuuren HJJ (2007) Functional analysis of the malolactic wine yeast ML01. Am J Enol Vitic 58:42–52Google Scholar
  107. Husnik JI, Volschenk H, Bauer J, Colavizza D, Luo Z, van Vuuren HJJ (2006) Metabolic engineering of malolactic wine yeast. Metabolic Eng 8:315–323Google Scholar
  108. Ilabaca C, Jara C, Romero J (2014) The rapid identification of lactic acid bacteria present in Chilean winemaking processes using culture-independent analysis. Ann Microbiol. doi:10.1007/s13213-014-0810-6
  109. Izquierdo PM, Garcia E, Martinez J, Chacon JL (2004) Selection of lactic bacteria to induce malolactic fermentation in red wine of cv. Cencibel. Vitis 43:149–153Google Scholar
  110. Jackowetz JN, Mira de Orduña R (2012) Metabolism of SO2 binding compounds by Oenococcus oeni during and after malolactic fermentation in white wine. Int J Food Microbiol 155:153–157PubMedGoogle Scholar
  111. Jackowetz JN, Mira de Orduña R (2013) Survey of SO2 binding carbonyls in 237 red and white table wines. Food Control 32:687–692Google Scholar
  112. Jaomanjaka F, Ballestra P, Dols-lafargue M, Le Marrec C (2013) Expanding the diversity of oenococcal bacteriophages: insights into a novel group based on the integrase sequence. Int J Food Microbiol 166:331–340PubMedGoogle Scholar
  113. Jobin MP, Delmas F, Garmyn D, Divies C, Guzzo J (1997) Molecular characterization of the gene encoding an 18-kilodalton small heat shock protein associated with the membrane of Leuconostoc oenos. Appl Environ Microbiol 63:609–614PubMedPubMedCentralGoogle Scholar
  114. Jobin MP, Garmyn D, Divies C, Guzzo J (1999) Expression of the Oenococcus oeni trxA gene is induced by hydrogen peroxide and heat shock. Microbiol-Sgm 145:1245–1251Google Scholar
  115. Jones G, White M, Cooper O, Storchmann K (2005) Climate change and global wine quality. Clim Chang 73:319–343Google Scholar
  116. Juega M, Costantini A, Bonello F, Cravero MC, Martinez-Rodriguez AJ, Carrascosa AV, Garcia-Moruno E (2014) Effect of malolactic fermentation by Pediococcus damnosus on the composition and sensory profile of Albariño and Caiño white wines. J Appl Microbiol 116:586–595Google Scholar
  117. Jussier D, Morneau DA, de Orduña RM (2006) Effect of simultaneous inoculation with yeast and bacteria on fermentation kinetics and key wine parameters of cool-climate Chardonnay. Appl Environ Microbiol 72(1):221–227PubMedPubMedCentralGoogle Scholar
  118. Kandler O (1983) Carbohydrate metabolism in lactic acid bacteria. A van Leeuw J Microb 49:209–224Google Scholar
  119. Knoll C, Fritsch S, Schnell S, Grossmann M, Krieger-Weber S, du Toit M, Rauhut D (2012) Impact of different malolactic fermentation inoculation scenarios on Riesling wine aroma. World J Microbiol Biotechnol 28:1143–1153PubMedGoogle Scholar
  120. Köhler V, Wilson YM, Dürrenberger M, Ghislieri D, Churakova E, Quinto T, Knörr L, Häussinger D, Hollmann F, Turner NJ, Ward TR (2013) Synthetic cascades are enabled by combining biocatalysts with artificial metalloenzymes. Nat Chem. doi:10.1038/NCHEM.1498 PubMedGoogle Scholar
  121. Krajewska B (2004) Application of chitin- and chitosan-based materials for enzyme immobilizations: a review. Enzyme Microb Technol 35:126–139Google Scholar
  122. Labarre C, Guzzo J, Cavin JF, Diviès C (1996) Cloning and characterization of the genes encoding the malolactic enzyme and the malate permease of Leuconostoc oenos. Appl Environ Microbiol 62:1274–1282PubMedPubMedCentralGoogle Scholar
  123. Larsen JT, Nielsen J-C, Kramp B, Richelieu M, Bjerring P, Riisager MJ, Arneborg N, Edwards CG (2003) Impact of different strains of Saccharomyces cerevisiae on malolactic fermentation by Oenococcus oeni. Am J Enol Vitic 54:246–251Google Scholar
  124. 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. J Agric Food Chem 57:10772–10783PubMedGoogle Scholar
  125. Lerm E, Engelbrecht L, du Toit M (2011) Selection and characterisation of Oenococcus oeni and Lactobacillus plantarum South African wine isolates for use as malolactic fermentation starter cultures. S Afric J Enol Vitic 32:280–295Google Scholar
  126. Liu S, Pritchard GG, Hardman MJ, Pilone GJ (1995) Occurrence of arginine deiminase pathway enzymes in arginine catabolism by wine lactic bacteria. Appl Environ Microbiol 61:310–316PubMedPubMedCentralGoogle Scholar
  127. Lonvaud-Funel A (2001) Biogenic amines in wines: role of lactic acid bacteria. FEMS Microbiol Lett 199:9–13PubMedGoogle Scholar
  128. Lonvaud-Funel A, Joyeux A, Desens C (1988) Inhibition of malolactic fermentation of wines by products of yeast metabolism. J Sci Food Agric 44:183–191Google Scholar
  129. Lopez I, Lopez R, Santamaria P, Torres C, Ruiz-Larrea F (2008a) Performance of malolactic fermentation by inoculation of selected Lactobacillus plantarum and Oenococcus oeni strains isolated from Rioja red wines. Vitis 47:123–129Google Scholar
  130. Lopez I, Torres C, Ruiz-Larrea F (2008b) Genetic typification by pulsed-field gel electrophoresis (PFGE) and randomly amplified polymorphic DNA (RAPD) of wild Lactobacillus plantarum and Oenococcus oeni wine strains. Eur Food Res Technol 227:547–555Google Scholar
  131. Mahillon J, Chandler M (1998) Insertion sequences. Microbiol Molec Biol Rev 62:725–774Google Scholar
  132. Maicas S, Pardo I, Ferrer S (2001) The potential of positively-charged cellulose sponge for malolactic fermentation of wine, using Oenococcus oeni. Enzyme Microb Technol 28:415–419PubMedGoogle Scholar
  133. Main GL, Threlfall RT, Morris JR (2007) Reduction of malic acid in wine using natural and genetically enhanced microorganisms. Am J Enol Vitic 58:341–345Google Scholar
  134. Maintz L, Novak N (2007) Histamine and histamine intolerance. Am J Clin Nutr 85:1185–96PubMedGoogle Scholar
  135. Maischberger T, Mierau I, Peterbauer CK, Hugenholtz J, Haltrich D (2010) High-level expression of Lactobacillus β-galactosidases in Lactococcus lactis using the food-grade, nisin-controlled expression system NICE. J Agric Food Chem 58:2279–2287PubMedGoogle Scholar
  136. Maitre M, Weidmann S, Dubois-Brissonnet F, David V, Covès J, Guzzo J (2014) Adaptation of the wine bacterium Oenococcus oeni to ethanol stress: role of the small heat shock protein Lo18 in membrane integrity. Appl Environ Microbiol. doi:10.1128/aem.04178-13 PubMedGoogle Scholar
  137. Makarova K, Slesarev A, Wolf Y, Sorokin A, Mirkin B, Koonin E, Pavlov A, Pavlova N, Karamychev V, Polouchine N, Shakhova V, Grigoriev I, Lou Y, Rohksar D, Lucas S, Huang K, Goodstein DM, Hawkins T, Plengvidhya V, Welker D, Hughes J, Goh Y, Benson A, Baldwin K, Lee J-H, Díaz-Muñiz I, Dosti B, Smeianov V, Wechter W, Barabote R, Lorca G, Altermann E, Barrangou R, Ganesan B, Xie Y, Rawsthorne H, Tamir D, Parker C, Breidt F, Broadbent J, Hutkins R, O’Sullivan D, Steele J, Unlu G, Saier M, Klaenhammer T, Richardson P, Kozyavkin S, Weimer B, Mills D (2006) Comparative genomics of the lactic acid bacteria. Proc Natl Acad Sci U S A 103:15611–15616PubMedPubMedCentralGoogle Scholar
  138. Makarova KS, Koonin EV (2007) Evolutionary genomics of lactic acid bacteria. J Bacteriol 189:1199–1208PubMedPubMedCentralGoogle Scholar
  139. Malherbe S, Tredoux A, Nieuwoudt H, du Toit M (2012) Comparative metabolic profiling to investigate the contribution of O. oeni MLF starter cultures to red wine composition. J Ind Microbiol Biotechnol 39:477–494PubMedGoogle Scholar
  140. Marcobal A, de las Rivas B, Moreno-Arribas MV, Munoz R (2006) Evidence for horizontal gene transfer as origin of putrescine production in Oenococcus oeni RM83. Appl Environ Microbiol 72:7954–7958PubMedPubMedCentralGoogle Scholar
  141. Marcobal AM, Sela DA, Wolf YI, Makarova KS, Mills DA (2008) Role of hypermutability in the evolution of the genus Oenococcus. J Bacteriol 190:564–570PubMedPubMedCentralGoogle Scholar
  142. Martuscelli M, Arfelli G, Manetta AC, Suzzi G (2013) Biogenic amines content as a measure of the quality of wines of Abruzzo (Italy). Food Chem 140(3):590–597PubMedGoogle Scholar
  143. Masqué MC, Soler M, Zaplana B, Franquet R, Rico S, Elorduy X, Puig A, Bertran E, Capdevila F, Palacios AT, Romero SV, Heras JM, Krieger-Weber S (2011) Ethyl carbamate content in wines with malolactic fermentation induced at different points in the vinification process. Ann Microbiol 61:199–206Google Scholar
  144. 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. Appl Environ Microbiol 70:5715–5731PubMedPubMedCentralGoogle Scholar
  145. Mendoza LM, de Nadra MCM, Farías ME (2010) Antagonistic interaction between yeasts and lactic acid bacteria of oenological relevance: partial characterization of inhibitory compounds produced by yeasts. Food Res Int 43:1990–1998Google Scholar
  146. Michlmayr H, Nauer S, Brandes W, Schümann C, Kulbe KD, del Hierro AM, Eder R (2012) Release of wine monoterpenes from natural precursors by glycosidases from Oenococcus oeni. Food Chem 135:80–87Google Scholar
  147. Miller B, Franz C, Cho G-S, du Toit M (2011) Expression of the malolactic enzyme gene from Lactobacillus plantarum under winemaking conditions. Curr Microbiol 62:1682–1688PubMedGoogle Scholar
  148. Mills DA, Rawsthorne H, Parker C, Tamir D, Makarova K (2005) Genomic analysis of Oenococcus oeni PSU-1 and its relevance to winemaking. FEMS Microbiol Rev 29:465–475PubMedGoogle Scholar
  149. Mira de Orduña R (2010) Climate change associated effects on grape and wine quality and production. Food Res Int 43:1844–1855Google Scholar
  150. Nehme N, Mathieu F, Taillandier P (2010) Impact of the co-culture of Saccharomyces cerevisiae and Oenococcus oeni on malolactic fermentation and partial characterization of a yeast-derived inhibitory peptidic fraction. Food Microbiol 27:150–157PubMedGoogle Scholar
  151. Nguyen T-T, Mathiesen G, Fredriksen L, Kittl R, Nguyen T-H, Eijsink VGH, Haltrich D, Peterbauer CK (2011) A food-grade system for inducible gene expression in Lactobacillus plantarum using an alanine racemase-encoding selection marker. J Agric Food Chem 59:5617–5624PubMedGoogle Scholar
  152. Novoa-Díaz D, Rodríguez-Nogales JM, Fernández-Fernández E, Vila-Crespo J, García-Álvarez J, Amer MA, Chávez JA, Turó A, García-Hernández MJ, Salazar J (2014) Ultrasonic monitoring of malolactic fermentation in red wines. Ultrasonics http://dx.doi.org/10.1016/j.ultras.2014.04.004.
  153. Olguín N, Bordons A, Reguant C (2009) Influence of ethanol and pH on the gene expression of the citrate pathway in Oenococcus oeni. Food Microbiol 26:197–203PubMedGoogle Scholar
  154. Osborne JP, Dubé Morneau A, Mira de Orduña R (2006) Degradation of free and sulfur-dioxide-bound acetaldehyde by malolactic lactic acid bacteria in white wine. J Appl Microbiol 101:474–479PubMedGoogle Scholar
  155. Osborne JP, Mira de Orduna R, Pilone GJ, Liu SQ (2000) Acetaldehyde metabolism by wine lactic acid bacteria. FEMS Microbiol Lett 191:51–55PubMedGoogle Scholar
  156. Osborne JP, Edwards CG (2007) Inhibition of malolactic fermentation by a peptide produced by Saccharomyces cerevisiae during alcoholic fermentation. Int J Food Microbiol 118(1):27–34PubMedGoogle Scholar
  157. Ough CS, Crowel EA, Gutlove BR (1988) Carbamyl compound reactions with ethanol. Am J Enol Vitic 39:239–242Google Scholar
  158. Papagianni M (2012) Metabolic engineering of lactic acid bacteria for the production of industrially important compounds. Comput Struct Biotechnol J 3:e201210003. doi:10.5936/csbj.201210003 PubMedPubMedCentralGoogle Scholar
  159. Patrignani F, Ndagijimana M, Belletti N, Gardini F, Vernocchi P, Lanciotti R (2012) Biogenic amines and ethyl carbamate in Primitivo wine: survey of their concentrations in commercial products and relationship with the use of malolactic starter. J Food Protect 75:591–596Google Scholar
  160. Perfeito L, Fernandes L, Mota C, Gordo I (2007) Adaptive mutations in bacteria: high rate and small effects. Science 317:813–815PubMedGoogle Scholar
  161. Peterbauer C, Maischberger T, Haltrich D (2011) Food-grade gene expression in lactic acid bacteria. Biotechnol J 6:1147–1161PubMedGoogle Scholar
  162. Polo L, Ferrer S, Peña-Gallego A, Hernández-Orte P, Pardo I (2011) Biogenic amine synthesis in high quality Tempranillo wines. Relationship with lactic acid bacteria and vinification conditions. Ann Microbiol 61:191–198Google Scholar
  163. Redzepovic S, Orlic S, Majdak A, Kozina B, Volschenk H, Viljoen-Bloom M (2003) Differential malic acid degradation by selected strains of Saccharomyces during alcoholic fermentation. Int J Food Microbiol 83:49–61PubMedGoogle Scholar
  164. Reguant C, Bordons A (2003) Typification of Oenococcus oeni strains by multiplex RAPD-PCR and study of population dynamics during malolactic fermentation. J Appl Microbiol 95:344–353PubMedGoogle Scholar
  165. Renouf V, Delaherche A, Claisse O, Lonvaud-Funel A (2008) Correlation between indigenous Oenococcus oeni strain resistance and the presence of genetic markers. J Ind Microbiol Biotechnol 35:27–33PubMedGoogle Scholar
  166. Ribereau-Gayon P, Glories Y, Maujean A, Dubourdieu D (2000) Handbook of enology, volume 2: the chemistry of wine and stabilization and treatments. Wiley, New YorkGoogle Scholar
  167. Rodas AM, Ferrer S, Pardo I (2005) Polyphasic study of wine Lactobacillus strains: taxonomic implications. Int J Syst Evol Microbiol 55:197–207PubMedGoogle Scholar
  168. Rodríguez-Nogales JM, Vila-Crespo J, Fernández-Fernández E (2013) Immobilization of Oenococcus oeni in Lentikats® to develop malolactic fermentation in wines. Biote chnol Prog 29:60–65Google Scholar
  169. Rodriguez SB, Thornton RJ (2008) Use of flow cytometry with fluorescent antibodies in real-time monitoring of simultaneously inoculated alcoholic-malolactic fermentation of Chardonnay. Lett Appl Microbiol 46:38–42PubMedGoogle Scholar
  170. Rosenberg SM (2001) Evolving responsively: adaptive mutation. Nat Rev Genet 2:504–515PubMedGoogle Scholar
  171. Rossouw D, du Toit M, Bauer FF (2012) The impact of co-inoculation with Oenococcus oeni on the transcriptome of Saccharomyces cerevisiae and on the flavour-active metabolite profiles during fermentation in synthetic must. Food Microbiol 29:121–131PubMedGoogle Scholar
  172. Ruediger GA, Pardon KH, Sas AN, Godden PW, Pollnitz AP (2005) Fate of pesticides during the winemaking process in relation to malolactic fermentation. J Agric Food Chem 53:3023–3026PubMedGoogle Scholar
  173. Sánchez A, Coton M, Coton E, Herrero M, García LA, Díaz M (2012) Prevalent lactic acid bacteria in cider cellars and efficiency of Oenococcus oeni strains. Food Microbiol 32:32–37PubMedGoogle Scholar
  174. Sauer U (2001) Evolutionary engineering of industrially important microbial phenotypes. In: Nielsen J (ed) Advances in Biochemical Engineering/Biotechnology Vol 73. Springer-Verlag Berlin Heidelberg, pp 129–169Google Scholar
  175. Schümann C, Michlmayr H, del Hierro AM, Kulbe KD, Jiranek V, Eder R, Nguyen T-H (2013) Malolactic enzyme from Oenococcus oeni: heterologous expression in Escherichia coli and biochemical characterization. Bioeng 4:147–152Google Scholar
  176. Schumann C, Michlmayr H, Eder R, del Hierro A, Kulbe K, Mathiesen G, Nguyen T-H (2012) Heterologous expression of Oenococcus oeni malolactic enzyme in Lactobacillus plantarum for improved malolactic fermentation. AMB Express 2:19. doi:10.1186/2191-0855-2-19 PubMedPubMedCentralGoogle Scholar
  177. Servetas I, Berbegal C, Camacho N, Bekatorou A, Ferrer S, Nigam P, Drouza C, Koutinas AA (2013) Saccharomyces cerevisiae and Oenococcus oeni immobilized in different layers of a cellulose/starch gel composite for simultaneous alcoholic and malolactic wine fermentations. Process Biochem 48:1279–1284Google Scholar
  178. Shareck J, Young C, Byong L, Miguez CB (2004) Cloning vectors based on cryptic plasmids isolated from lactic acid bacteria: their characteristics and potential applications in biotechnology. Crit Rev Biotechnol 24:155–208PubMedGoogle Scholar
  179. Sico MA, Bonomo MG, D’Adamo A, Bochicchio S, Salzano G (2009) Fingerprinting analysis of Oenococcus oeni strains under stress conditions. FEMS Microbiol Lett 296:11–17PubMedGoogle Scholar
  180. Siebert TE, Smyth HE, Capone DL, Neuwöhner C, Pardon KH, Skouroumounis GK, Herderich MJ, Sefton MA, Pollnitz AP (2005) Stable isotope dilution analysis of wine fermentation products by HS-SPME-GC-MS. Anal Bioanal Chem 381:937–947PubMedGoogle Scholar
  181. Sieiro C, Cansado J, Agrelo D, Velázquez JB, Villa TG (1990) Isolation and enological characterization of malolactic bacteria from the vineyards of northwestern Spain. Appl Environ Microbiol 56:2936–2938PubMedPubMedCentralGoogle Scholar
  182. Silva I, Campos FM, Hogg T, Couto JA (2011) Wine phenolic compounds influence the production of volatile phenols by wine-related lactic acid bacteria. J Appl Microbiol 111:360–370PubMedGoogle Scholar
  183. Smit A, du Toit M (2013) Evaluating the influence of malolactic fermentation inoculation practices and ageing on lees on biogenic amine production in wine. Food Bioprocess Technol 6:198–206Google Scholar
  184. Smit AY, du Toit WJ, Stander M, du Toit M (2013) Evaluating the influence of maceration practices on biogenic amine formation in wine. LWT - Food Sci Tech 53:297–307Google Scholar
  185. Smit AY, Engelbrecht L, duToit M (2012) Managing your wine fermentation to reduce the risk of biogenic amine formation. Front Microbiol 3:1–10Google Scholar
  186. Solieri L, Giudici P (2010) Development of a sequence-characterized amplified region marker-targeted quantitative PCR assay for strain-specific detection of Oenococcus oeni during wine malolactic fermentation. Appl Environ Microbiol 76:7765–7774PubMedPubMedCentralGoogle Scholar
  187. Sørvig E, Grönqvist S, Naterstad K, Mathiesen G, Eijsink VGH, Axelsson L (2003) Construction of vectors for inducible gene expression in Lactobacillus sakei and L. plantarum. FEMS Microbiol Lett 229:119–126PubMedGoogle Scholar
  188. Spano G, Chieppa G, Beneduce L, Massa S (2004) Expression analysis of putative arcA, arcB and arcC genes partially cloned from Lactobacillus plantarum isolated from wine. J Appl Microbiol 96:185–193PubMedGoogle Scholar
  189. Spano G, Russo P, Lonvaud-Funel A, Lucas P, Alexandre H, Grandvalet C, Coton E, Coton M, Barnavon L, Bach B, Rattray F, Bunte A, Magni C, Ladero V, Alvarez M, Fernández M, Lopez P, de Palencia PF, Corbi A, Trip H, Lolkema JS (2010) Biogenic amines in fermented foods. Eur J Clin Nutr 64:S95–S100PubMedGoogle Scholar
  190. Spettoli P, Bottacin A, Nuti MP, Zamorani A (1982) Immobilization of Leuconostoc oenos ML34 in calcium alginate gels and its application to wine technology. Am J Enol Vitic 22:1–5Google Scholar
  191. Sumby KM, Grbin PR, Jiranek V (2010) Microbial modulation of aromatic esters in wine: current knowledge and future prospects. Food Chem 121:1–16Google Scholar
  192. Sumby KM, Grbin PR, Jiranek V (2012a) Characterisation of EstCOo8 and EstC34, intracellular esterases, from the wine associated lactic acid bacterium Oenococcus oeni and Lactobacillus hilgardii. J Appl Microbiol 114:413–422PubMedGoogle Scholar
  193. Sumby KM, Grbin PR, Jiranek V (2012b) Validation of the use of multiple internal control genes, and the application of real-time quantitative PCR, to study esterase gene expression in Oenococcus oeni. Appl Microbiol Biotechnol 96(4):1039–1047PubMedGoogle Scholar
  194. Sumby KM, Grbin PR, Jiranek V (2013) Ester synthesis and hydrolysis in an aqueous environment, and strain specific changes during malolactic fermentation in wine with Oenococcus oeni. Food Chem 141:1673–1680PubMedGoogle Scholar
  195. Sumby KM, Matthews AH, Grbin PR, Jiranek V (2009) Cloning and characterization of an intracellular esterase from the wine-associated lactic acid bacterium Oenococcus oeni. Appl Environ Microbiol 75:6729–6735PubMedPubMedCentralGoogle Scholar
  196. Swiegers J, Bartowsky E, Henschke P, Pretorius I (2005) Yeast and bacterial modulation of wine aroma and flavour. Aust J Grape Wine Res 11:139–173Google Scholar
  197. Taddei F, Radman M, Maynard-Smith J, Toupance B, Gouyon P, Godelle B (1997) Role of mutator alleles in adaptive evolution. Nature 387:700–702PubMedGoogle Scholar
  198. Tchobanov I, Gal L, Guilloux-Benatier M, Remize F, Nardi T, Guzzo J, Serpaggi V, Alexandre H (2008) Partial vinylphenol reductase purification and characterization from Brettanomyces bruxellensis. FEMS Microbiol Lett 284(2):213–217PubMedGoogle Scholar
  199. Teusink B, Wiersma A, Jacobs L, Notebaart RA, Smid EJ (2009) Understanding the adaptive growth strategy of Lactobacillus plantarum by in silico optimisation. PLoS Comput Biol 5:e1000410. doi:10.1371/journal.pcbi.1000410. font PubMedPubMedCentralGoogle Scholar
  200. Tonon T, Bourdineaud JP, Lonvaud-Funel A (2001) The arcABC gene cluster encoding the arginine deiminase pathway of Oenococcus oeni, and arginine induction of a CRP-like gene. Res Microbiol 152:653–661PubMedGoogle Scholar
  201. Tourdot-Maréchal R, Cavin J-F, Drici-Cachon Z, Diviès C (1993) Transport of malic acid in Leuconostoc oenos strains defective in malolactic fermentation: a model to evaluate the kinetic parameters. Appl Microbiol Biotechnol 39:499–505Google Scholar
  202. Tourdot-Marechal R, Gaboriau D, Beney L, Divies C (2000) Membrane fluidity of stressed cells of Oenococcus oeni. Int J Food Microbiol 55:269–273PubMedGoogle Scholar
  203. Ugliano M, Moio L (2006) The influence of malolactic fermentation and Oenococcus oeni strain on glycosidic aroma precursors and related volatile compounds of red wine. J Sci Food Agric 86:2468–2476Google Scholar
  204. Vailiant H, Formisyn P, Gerbaux V (1995) Malolactic fermentation of wine: study of the influence of some physico-chemical factors by experimental design assays. J Appl Bacteriol 79:640–650Google Scholar
  205. Vidal MT, Poblet M, Constantí M, Bordons A (2001) Inhibitory effect of copper and dichlofluanid on Oenococcus oeni and malolactic fermentation. Am J Enol Vitic 52:223–229Google Scholar
  206. Viti C, Giovannetti L, Granchi L, Ventura S (1996) Species attribution and strain typing of Oenococcus oeni (formerly Leuconostoc oenos) with restriction endonuclease fingerprints. Res Microbiol 147:651–660PubMedGoogle Scholar
  207. 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). J Sci Food Agric 80:1675–1678Google Scholar
  208. Volschenk H, Viljoen M, Grobler J, Bauer F, Lonvaud-Funel A, Denayrolles N, Subden RE, van Vuuren HJJ (1997a) Malolactic fermentation in grape must by a genetically engineered strain of Saccharomyces cerevisiae. Am J Enol Vitic 48:193–197Google Scholar
  209. Volschenk H, Viljoen M, Grobler J, Petzold B, Bauer F, Subden RE, Young RA, Lonvaud A, Denayrolles M, van Vuuren HJJ (1997b) Engineering pathways for malate degradation in Saccharomyces cerevisiae. Nat Biotechnol 15:253–257PubMedGoogle Scholar
  210. Volschenk H, Vuuren HJJ, Viljoen–Bloom M (2003) Malo-ethanolic fermentation in Saccharomyces and Schizosaccharomyces. Curr Genet 43(Viljoen–Bloom M):379–391PubMedGoogle Scholar
  211. Wells A, Osborne JP (2011) Production of SO2 binding compounds and SO2 by Saccharomyces during alcoholic fermentation and the impact on malolactic fermentation. S Afr J Enol Vitic 32:267–279Google Scholar
  212. Wells A, Osborne JP (2012) Impact of acetaldehyde- and pyruvic acid-bound sulphur dioxide on wine lactic acid bacteria. Lett Appl Microbiol 54:187–194PubMedGoogle Scholar
  213. Wen-ying Z, Zhen-kui K (2013) Advanced progress on adaptive stress response of Oenococcus oeni. J North Agric Univ (English Edition) 20:91–96Google Scholar
  214. Wu C, Huang J, Zhou R (2014) Progress in engineering acid stress resistance of lactic acid bacteria. Appl Microbiol Biotechnol 98:1055–1063PubMedGoogle Scholar
  215. Yang D, Woese CR (1989) Phylogenetic structure of the “Leuconostocs”: an interesting case of a rapidly evolving organism. Syst Appl Microbiol 12:145–149Google Scholar
  216. Zapparoli G, Tosi E, Azzolini M, Vagnoli P, Krieger S (2009) Bacterial inoculation strategies for the achievement of malolactic fermentation in high-alcohol wines. S Afr J Enol Vitic 30(1):49–55Google Scholar
  217. Zapparoli G, Moser M, Dellaglio F, Tourdot-Marechal R, Guzzo J (2004) Typical metabolic traits of two Oenococcus oeni strains isolated from Valpolicella wines. Lett Appl Microbiol 39:48–54PubMedGoogle Scholar
  218. Zapparoli G, Reguant C, Bordons A, Torriani S, Dellaglio F (2000) Genomic DNA fingerprinting of Oenococcus oeni strains by pulsed-field gel electrophoresis and randomly amplified polymorphic DNA-PCR. Curr Microbiol 40:351–355PubMedGoogle Scholar
  219. Zavaleta AI, Martinez-Murcia AJ, Rodriguez-Valera F (1997) Intraspecific genetic diversity of Oenococcus oeni as derived from DNA fingerprinting and sequence analysis. Appl Environ Microbiol 63:1261–1267PubMedPubMedCentralGoogle Scholar
  220. Ze-Ze L, Chelo IM, Tenreiro R (2008) Genome organization in Oenococcus oeni strains studied by comparison of physical and genetic maps. Int Microbiol 11:237–244PubMedGoogle Scholar
  221. Zhang J, Wu C, Du G, Chen J (2012) Enhanced acid tolerance in Lactobacillus casei by adaptive evolution and compared stress response during acid stress. Biotechnol Bioprocess Eng 17:283–289Google Scholar
  222. Zhang X, Hou X, Liang F, Chen F, Wang X (2013) Surface display of malolactic enzyme from Oenococcus oeni on Saccharomyces cerevisiae. Appl Biochem Biotech 169:2350–2361Google Scholar
  223. Zúñiga M, Pardo I, Ferrer S (2003) Conjugative plasmid pIP501 undergoes specific deletions after transfer from Lactococcus lactis to Oenococcus oeni. Arch Microbiol 180:367–373PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Krista M. Sumby
    • 1
  • Paul R. Grbin
    • 1
  • Vladimir Jiranek
    • 1
  1. 1.School of Agriculture, Food and WineThe University of AdelaideGlen OsmondAustralia

Personalised recommendations