Advertisement

Measures to improve wine malolactic fermentation

  • Krista M. Sumby
  • Louise Bartle
  • Paul R. Grbin
  • Vladimir JiranekEmail author
Mini-Review

Abstract

This review focuses on the considerable amount of research that has been directed towards the improvement of efficiency and reliability of malolactic fermentation (MLF), which is important in winemaking. From this large body of work, it is clear that reliable MLF is essential for process efficiency and prevention of spoilage in the final product. Impediments to successful MLF in wine, the impact of grape and wine ecology and how this may affect MLF outcome are discussed. Further focus is given to how MLF success may be enhanced, via alternative inoculation strategies, MLF progress sensing technologies and the use of different bacterial species. An update of how this information may be used to enhance and improve sensory outcomes through metabolite production during MLF and suggestions for future research priorities for the field are also provided.

Keywords

Oenococcus oeni Lactobacillus Malolactic fermentation Wine 

Notes

Acknowledgments

This review was supported by The Australian Research Council Training Centre for Innovative Wine Production (www.ARCwinecentre.org.au; project number IC170100008) funded by the Australian Government with additional support from Wine Australia and industry partners. The University of Adelaide is a member of the Wine Innovation Cluster (http://www.thewaite.org/waite-partners/wine-innovation-cluster/).

Compliance with ethical standards

This article does not contain any studies with human participants or animals performed by any of the authors.

Conflict of interest

The authors declare that they have no competing interests.

References

  1. Abrahamse CE, Bartowsky EJ (2012) Timing of malolactic fermentation inoculation in shiraz grape must and wine: influence on chemical composition. World J Microbiol Biotechnol 28(1):255–265CrossRefPubMedGoogle Scholar
  2. Al-Attabi Z, D’Arcy BR, Deeth HC (2008) Volatile sulphur compounds in UHT milk. Crit Rev Food Sci Nutr 49(1):28–47.  https://doi.org/10.1080/10408390701764187 CrossRefGoogle Scholar
  3. Antalick G, Perello M-C, de Revel G (2012) Characterization of fruity aroma modifications in red wines during malolactic fermentation. J Agric Food Chem 60(50):12371–12383CrossRefPubMedGoogle Scholar
  4. Arena MP, Capozzi V, Russo P, Drider D, Spano G, Fiocco D (2018) Immunobiosis and probiosis: antimicrobial activity of lactic acid bacteria with a focus on their antiviral and antifungal properties. Appl Microbiol Biotechnol 102:9949–9958.  https://doi.org/10.1007/s00253-018-9403-9 CrossRefPubMedGoogle Scholar
  5. Barata A, Malfeito-Ferreira M, Loureiro V (2012) The microbial ecology of wine grape berries. Int J Food Microbiol 153(3):243–259CrossRefPubMedGoogle Scholar
  6. Bartowsky EJ, Borneman AR (2011) Genomic variations of Oenococcus oeni strains and the potential to impact on malolactic fermentation and aroma compounds in wine. Appl Microbiol Biotechnol 92(3):441–447CrossRefPubMedGoogle Scholar
  7. Bartowsky EJ, Costello PJ, Chambers PJ (2015) Emerging trends in the application of malolactic fermentation. Aust J Grape Wine Res 21(S1):663–669CrossRefGoogle Scholar
  8. Bartowsky EJ, Henschke PA (2004) The “buttery” attribute of wine—diacetyl—desirability, spoilage and beyond. Int J Food Microbiol 96(3):235–252CrossRefPubMedGoogle Scholar
  9. Benito Á, Calderón F, Palomero F, Benito S (2015) Combine use of selected Schizosaccharomyces pombe and Lachancea thermotolerans yeast strains as an alternative to the traditional malolactic fermentation in red wine production. Molecules 20(6):9510–9523CrossRefPubMedPubMedCentralGoogle Scholar
  10. 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. Int J Food Microbiol 137(1):28–31Google Scholar
  11. Berbegal C, Garofalo C, Russo P, Pati S, Capozzi V, Spano G (2017) Use of autochthonous yeasts and bacteria in order to control Brettanomyces bruxellensis in wine. Fermentation 3(4):65.  https://doi.org/10.3390/fermentation3040065 CrossRefGoogle Scholar
  12. Betteridge A, Grbin P, Jiranek V (2015) Improving Oenococcus oeni to overcome challenges of wine malolactic fermentation. Trends Biotechnol 33(9):547–553CrossRefPubMedGoogle Scholar
  13. Betteridge AL, Sumby KM, Sundstrom JF, Grbin PR, Jiranek V (2018) Application of directed evolution to develop ethanol tolerant Oenococcus oeni for more efficient malolactic fermentation. Appl Microbiol Biotechnol 102:921–932CrossRefPubMedGoogle Scholar
  14. Bisson LF (1999) Stuck and sluggish fermentations. Am J Enol Vitic 50(1):107–119Google Scholar
  15. Blazquez Rojas I, Smith PA, Bartowsky EJ (2012) Influence of choice of yeasts on volatile fermentation-derived compounds, colour and phenolics composition in cabernet sauvignon wine. World J Microbiol Biotechnol 28(12):3311–3321CrossRefPubMedGoogle Scholar
  16. Bravo I, Revenga-Parra M, Pariente F, Lorenzo E (2017) Reagent-less and robust biosensor for direct determination of lactate in food samples. Sensors 17(1):144.  https://doi.org/10.3390/s17010144 CrossRefGoogle Scholar
  17. Bravo-Ferrada BM, Gonçalves S, Semorile L, Santos NC, Brizuela NS, Elizabeth Tymczyszyn E, Hollmann A (2018) Cell surface damage and morphological changes in Oenococcus oeni after freeze-drying and incubation in synthetic wine. Cryobiology 82:15–21CrossRefPubMedGoogle Scholar
  18. Boido E, Lloret A, Medina K, Carrau F, Dellacassa E (2002) Effect of β-glycosidase activity of Oenococcus oeni on the glycosylated flavor precursors of Tannat wine during malolactic fermentation. J Agric Food Chem 50:2344–2349CrossRefPubMedGoogle Scholar
  19. Bokulich NA, Collins TS, Masarweh C, Allen G, Heymann H, Ebeler SE, Mills DA (2016) Associations among wine grape microbiome, metabolome, and fermentation behavior suggest microbial contribution to regional wine characteristics. mBio 7(3):e00631–e00616.  https://doi.org/10.1128/mBio.00631-16 CrossRefPubMedPubMedCentralGoogle Scholar
  20. Bokulich NA, Swadener M, Sakamoto K, Mills DA, Bisson LF (2015) Sulfur dioxide treatment alters wine microbial diversity and fermentation progression in a dose-dependent fashion. Am J Enol Vitic 66(1):73–79CrossRefGoogle Scholar
  21. Boles E, de Jong-Gubbels P, Pronk JT (1998) Identification and characterization of MAE1, the Saccharomyces cerevisiae structural gene encoding mitochondrial malic enzyme. J Bacteriol 180(11):2875–2882PubMedPubMedCentralGoogle Scholar
  22. Bondy-Denomy J, Qian J, Westra ER, Buckling A, Guttman DS, Davidson AR, Maxwell KL (2016) Prophages mediate defence against phage infection through diverse mechanisms. The ISME J 10(12):2854–2866CrossRefPubMedGoogle Scholar
  23. Bonomo MG, Di Tomaso K, Calabrone L, Salzano G (2018) Ethanol stress in Oenococcus oeni: transcriptional response and complex physiological mechanisms. J Appl Microbiol 125:2–15.  https://doi.org/10.1111/jam.13711 CrossRefPubMedGoogle Scholar
  24. Bou M, Krieger S IN (2012) Alcohol-tolerant malolactic strains for the maturation of wines with average or high pH. United States patent number US 8,114,449 B2Google Scholar
  25. Brizuela NS, Bravo-Ferrada BM, Pozo-Bayón MÁ, Semorile L, Tymczyszyn E (2018) Changes in the volatile profile of pinot noir wines caused by Patagonian Lactobacillus plantarum and Oenococcus oeni strains. Food Res Int 106:22–28CrossRefPubMedGoogle Scholar
  26. Brandam C, Fahimi N, Taillandier P (2016) Mixed cultures of Oenococcus oeni strains: a mathematical model to test interaction on malolactic fermentation in winemaking. LWT Food Sci Technol 69:211–216CrossRefGoogle Scholar
  27. Burns TR, Osborne JP (2013) Impact of malolactic fermentation on the color and color stability of pinot noir and merlot wine. Am J Enol Vitic DOI 64:370–377.  https://doi.org/10.5344/ajev.2013.13001 CrossRefGoogle Scholar
  28. Burns TR, Osborne JP (2015) Loss of pinot noir wine color and polymeric pigment after malolactic fermentation and potential causes. Am J Enol Vitic 66(2):130–137CrossRefGoogle Scholar
  29. Campbell-Sills H, Lorentzen M, Lucas PM (2017a) Genomic evolution and adaptation to wine of Oenococcus oeni BT—biology of microorganisms on grapes, in must and in wine. In: König H, Unden G, Fröhlich J (eds) . Springer International Publishing, Cham, pp 457–468.  https://doi.org/10.1007/978-3-319-60021-5_19 CrossRefGoogle Scholar
  30. Campbell-Sills H, El Khoury M, Gammacurta M, Miot-Sertier C, Dutilh L, Vestner J, Capozzi V, Sherman D, Hubert C, Claisse O, Spano G, de Revel G, Lucas P (2017b) Two different Oenococcus oeni lineages are associated to either red or white wines in Burgundy: genomics and metabolomics insights. OENO One 51(3):309.  https://doi.org/10.20870/oeno-one.2017.51.4.1861 CrossRefGoogle Scholar
  31. Cañas PMI, Pérez-Martín F, Romero EG, Prieto SS, de los Herreros M LP (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(3):245–254CrossRefGoogle Scholar
  32. 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.  https://doi.org/10.3389/fmicb.2012.00122 CrossRefPubMedPubMedCentralGoogle Scholar
  33. Cappello MS, Zapparoli G, Logrieco A, Bartowsky EJ (2017) Linking wine lactic acid bacteria diversity with wine aroma and flavour. Int J Food Microbiol 243:16–27CrossRefPubMedGoogle Scholar
  34. 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
  35. Caspritz G, Radler F (1983) Malolactic enzyme of Lactobacillus plantarum. Purification, properties, and distribution among bacteria. J Biol Chem 258:4907–4910PubMedGoogle Scholar
  36. Çelik DA, Amer MA, Novoa-Díaz DF, Chávez JA, Turó A, García-Hernández MJ, Salazar J (2018) Design and implementation of an ultrasonic sensor for rapid monitoring of industrial malolactic fermentation of wines. Instrum Sci Technol 46:387–407.  https://doi.org/10.1080/10739149.2017.1394878 CrossRefGoogle Scholar
  37. Cinquanta L, De Stefano G, Formato D, Niro S, Panfili G (2018) Effect of pH on malolactic fermentation in southern Italian wines. Eur Food Res Technol 244:1261–1268.  https://doi.org/10.1007/s00217-018-3041-4 CrossRefGoogle Scholar
  38. Comitini F, Ciani M (2007) The inhibitory activity of wine yeast starters on malolactic bacteria. Ann Microbiol 57(1):61–66CrossRefGoogle Scholar
  39. 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 99:105–111CrossRefPubMedGoogle Scholar
  40. Costantini A, Doria F, Saiz J-C, Garcia-Moruno E (2017) Phage–host interactions analysis of newly characterized Oenococcus oeni bacteriophages: implications for malolactic fermentation in wine. Int J Food Microbiol 246:12–19CrossRefPubMedGoogle Scholar
  41. Costello PJ, Francis IL, Bartowsky EJ (2012) Variations in the effect of malolactic fermentation on the chemical and sensory properties of cabernet sauvignon wine: interactive influences of Oenococcus oeni strain and wine matrix composition. Aust J Grape Wine Res 18(3):287–301CrossRefGoogle Scholar
  42. Costello PJ, Siebert TE, Solomon MR, Bartowsky EJ (2013) Synthesis of fruity ethyl esters by acyl coenzyme A: alcohol acyltransferase and reverse esterase activities in Oenococcus oeni and Lactobacillus plantarum. J Appl Microbiol 114(3):797–806CrossRefPubMedGoogle Scholar
  43. Couto JA, Campos FM, Figueiredo AR, Hogg TA (2006) Ability of lactic acid bacteria to produce volatile phenols. Am J Enol Vitic 57(2):166–171Google Scholar
  44. Curioni PMG, Bosset JO (2002) Key odorants in various cheese types as determined by gas chromatography–olfactometry. Int Dairy J 12(12):959–984CrossRefGoogle Scholar
  45. David V, Terrat S, Herzine K, Claisse O, Rousseaux S, Tourdot-Maréchal R, Masneuf-Pomarede I, Ranjard L, Alexandre H (2014) High-throughput sequencing of amplicons for monitoring yeast biodiversity in must and during alcoholic fermentation. J Ind Microbiol Biotechnol 41(5):811–821CrossRefPubMedGoogle Scholar
  46. Davis CR, Wibowo D, Eschenbruch R, Lee TH, Fleet GH (1985) Practical implications of malolactic fermentation: a review. Am J Enol Vitic 36(4):290–301Google Scholar
  47. Davis CR, Wibowo DJ, Lee TH, Fleet GH (1986) Growth and metabolism of lactic acid bacteria during and after malolactic fermentation of wines at different pH. Appl Environ Microbiol 51(3):539–545PubMedPubMedCentralGoogle Scholar
  48. Davis CR, Wibowo D, Fleet GH, Lee TH (1988) Properties of wine lactic acid bacteria: their potential enological significance. Am J Enol Vitic 39:137–142Google Scholar
  49. Delaquis P, Cliff M, King M, Girard B, Hall J, Reynolds A (2000) Effect of two commercial malolactic cultures on the chemical and sensory properties of chancellor wines vinified with different yeasts and fermentation temperatures. Am J Enol Vitic 51(1):42–48Google Scholar
  50. de las Rivas B, Rodríguez H, Curiel JA, Landete JM, Muñoz R (2009) Molecular screening of wine lactic acid bacteria degrading hydroxycinnamic acids. J Agric Food Chem 57(2):490–494CrossRefPubMedGoogle Scholar
  51. Dimopoulou M, Bardeau T, Ramonet P-Y, Miot-Certier C, Claisse O, Doco T, Petrel M, Lucas P, Dols-Lafargue M (2016) Exopolysaccharides produced by Oenococcus oeni: from genomic and phenotypic analysis to technological valorization. Food Microbiol 53:10–17CrossRefPubMedGoogle Scholar
  52. Dimopoulou M, Raffenne J, Claisse O, Miot-Sertier C, Iturmendi N, Moine V, Coulon J, Dols-Lafargue M (2018) Oenococcus oeni exopolysaccharide biosynthesis, a tool to improve malolactic starter performance. Front Microbiol  https://doi.org/10.3389/fmicb.2018.01276
  53. Douillard FP, Ribbera A, Xiao K, Ritari J, Rasinkangas P, Paulin L, Palva L, Hao Y, de Vos WM (2016) Polymorphisms, chromosomal rearrangements, and mutator phenotype development during experimental evolution of Lactobacillus rhamnosus GG. Appl Environ Microbiol 82(13):3783–3792CrossRefPubMedPubMedCentralGoogle Scholar
  54. du Plessis H, du Toit M, Nieuwoudt H, van der Rijst M, Kidd M, Jolly N (2017) Effect of Saccharomyces, non-Saccharomyces yeasts and malolactic fermentation strategies on fermentation kinetics and flavor of shiraz wines. Fermentation 3(4):64.  https://doi.org/10.3390/fermentation3040064 CrossRefGoogle Scholar
  55. 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 4:876–906.  https://doi.org/10.1007/s11947-010-0448-8
  56. Edwards CG, Haag KM, Collins MD, Hutson RA, Huang YC (2002) Lactobacillus kunkeei sp. nov.: a spoilage organism associated with grape juice fermentations. J Appl Microbiol 84(5):698–702CrossRefGoogle Scholar
  57. El Khoury M, Campbell-Sills H, Salin F, Guichoux E, Claisse O, Lucas PM (2017) Biogeography of Oenococcus oeni reveals distinctive but nonspecific populations in wine-producing regions. Appl Environ Microbiol 83(3):e02322–e02316.  https://doi.org/10.1128/AEM.02322-16 CrossRefPubMedPubMedCentralGoogle Scholar
  58. Esteban-Torres M, Barcenilla JM, Mancheño JM, de las Rivas B, Muñoz R (2014) Characterization of a versatile arylesterase from Lactobacillus plantarum active on wine esters. J Agric Food Chem 62(22):5118–5125CrossRefPubMedGoogle Scholar
  59. Fleet GH (2003) Yeast interactions and wine flavour. Int J Food Microbiol 86(1):11–22CrossRefPubMedGoogle Scholar
  60. Fourcassie P, Makaga-Kabinda-Massard E, Belarbi A, Maujean A (1992) Growth, D-glucose utilization and malolactic fermentation by Leuconostoc oenos strains in 18 media deficient in one amino acid. J Appl Bacteriol 73:489–496CrossRefGoogle Scholar
  61. Franquès J, Araque I, Palahí E, Portillo MDC, Reguant C, Bordons A (2017) Presence of Oenococcus oeni and other lactic acid bacteria in grapes and wines from Priorat (Catalonia, Spain). LWT Food Sci Technol 81:326–334Google Scholar
  62. Galland D, Tourdot-Maréchal R, Abraham M, Son Chu K, Guzzo J (2003) Absence of malolactic activity is a characteristic of H+-ATPase-deficient mutants of the lactic acid bacterium Oenococcus oeni. Appl Environ Microbiol 69(4):1973–1979CrossRefPubMedPubMedCentralGoogle Scholar
  63. Gámbaro A, Boido E, Zlotejablko A, Medina K, Lloret A, Dellacassa E, Carrau F (2001) Effect of malolactic fermentation on the aroma properties of Tannat wine. Aust J GrapeWine Res 7(1):27–32CrossRefGoogle Scholar
  64. 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(3):925–933CrossRefPubMedGoogle Scholar
  65. Gammacurta M, Lytra G, Marchal A, Marchand S, Christophe Barbe J, Moine V, de Revel G (2018) Influence of lactic acid bacteria strains on ester concentrations in red wines: specific impact on branched hydroxylated compounds. Food Chem 239:252–259CrossRefPubMedGoogle Scholar
  66. Gammacurta M, Marchand S, Moine V, de Revel G (2017) Influence of different yeast/lactic acid bacteria combinations on the aromatic profile of red Bordeaux wine. J Sci Food Agric 97(12):4046–4057CrossRefPubMedGoogle Scholar
  67. Giménez-Gómez P, Gutiérrez-Capitán M, Capdevila F, Puig-Pujol A, Fernández-Sánchez C, Jiménez-Jorquera C (2017) Robust L-malate bienzymatic biosensor to enable the on-site monitoring of malolactic fermentation of red wines. Anal Chim Acta 954:105–113CrossRefPubMedGoogle Scholar
  68. Gobert A, Tourdot-Maréchal R, Morge C, Sparrow C, Liu Y, Quintanilla-Casas B, Vichi S, Alexandre H (2017) Non-Saccharomyces yeasts nitrogen source preferences: impact on sequential fermentation and wine volatile compounds profile. Front Microbiol 8:2175.  https://doi.org/10.3389/fmicb.2017.02175 CrossRefPubMedPubMedCentralGoogle Scholar
  69. Gockowiak H, Henschke PA (2008) Interaction of pH, ethanol concentration and wine matrix on induction of malolactic fermentation with commercial “direct inoculation” starter cultures. Aust J Grape Wine Res 9(3):200–209CrossRefGoogle Scholar
  70. Godálová Z, Kraková L, Puškárová A, Bučková M, Kuchta T, Piknová Ľ, Pangallo D (2016) Bacterial consortia at different wine fermentation phases of two typical central European grape varieties: Blaufränkisch (Frankovka modrá) and Grüner Veltliner (Veltlínske zelené). Int J Food Microbiol 217:110–116CrossRefPubMedGoogle Scholar
  71. González-Arenzana L, López-Alfaro I, Garde-Cerdán T, Portu J, López R, Santamaría P (2018) Microbial inactivation and MLF performances of Tempranillo Rioja wines treated with PEF after alcoholic fermentation. Int J Food Microbiol 269:19–26CrossRefPubMedGoogle Scholar
  72. Grimaldi A, Bartowsky E, Jiranek V (2005a) A survey of glycosidase activities of commercial wine strains of Oenococcus oeni. Int J Food Microbiol 105(2):233–244CrossRefPubMedGoogle Scholar
  73. Grimaldi A, Bartowsky E, Jiranek V (2005b) Screening of Lactobacillus spp. and Pediococcus spp. for glycosidase activities that are important in oenology. J Appl Microbiol 99(5):1061–1069CrossRefPubMedGoogle Scholar
  74. Guilloux-Benatier M, Le Fur Y, Feuillat M (1998) Influence of fatty acids on the growth of wine microorganisms Saccharomyces cerevisiae and Oenococcus oeni. J Ind Microbiol Biotechnol 20:144–149CrossRefGoogle Scholar
  75. Guzzon R, Poznanski E, Conterno L, Vagnoli P, Krieger-Weber S, Cavazza A (2009) Selection of a new highly resistant strain for malolactic fermentation under difficult conditions. S Afr J Enol Vitic 30(2):133–141Google Scholar
  76. Guzzon R, Villega TR, Pedron M, Malacarne M, Nicolini G, Larcher R (2013) Simultaneous yeast–bacteria inoculum. A feasible solution for the management of oenological fermentation in red must with low nitrogen content. Ann Microbiol 63(2):805–808CrossRefGoogle Scholar
  77. Henick-Kling T (1993) Malolactic fermentation. In: Fleet GH (ed) Wine microbiology and biotechnology. Harwood Academic Publishers, Chur, Switzerland, pp 289–326Google Scholar
  78. Henick-Kling T, Lee TH, Nicholas DJD (1986) Inhibition of bacterial growth and malolactic fermentation in wine by bacteriophage. J Appl Bacteriol 61(4):287–293CrossRefGoogle Scholar
  79. Huang Y-C, Edwards CG, Peterson JC, Haag KM (1996) Relationship between sluggish fermentations and the antagonism of yeast by lactic acid bacteria. Am J Enol Vitic 47(1):1–10Google Scholar
  80. Hugenholtz J (1993) Citrate metabolism in lactic acid bacteria. FEMS Microbiol Rev 12:165–178CrossRefGoogle Scholar
  81. Iorizzo M, Testa B, Lombardi SJ, García-Ruiz A, Muñoz-González C, Bartolomé B, Moreno-Arribas MV (2016) Selection and technological potential of Lactobacillus plantarum bacteria suitable for wine malolactic fermentation and grape aroma release. LWT Food Sci Technol 73:557–566CrossRefGoogle Scholar
  82. Jenkins DE, Schultz JE, Matin A (1988) Starvation-induced cross protection against heat or H2O2 challenge in Escherichia coli. J Bacteriol 170(9):3910–3914CrossRefPubMedPubMedCentralGoogle Scholar
  83. Jiang J, Sumby KM, Sundstrom JF, Grbin PR, Jiranek V (2018) Directed evolution of Oenococcus oeni strains for more efficient malolactic fermentation in a multi-stressor wine environment. Food Microbiol 73:150–159CrossRefPubMedGoogle Scholar
  84. Juega M, Costantini A, Bonello F, Cravero V, Martinez-Rodriguez V, 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(3):586–595CrossRefPubMedGoogle Scholar
  85. Knoll C, Divol B, du Toit M (2008) Genetic screening of lactic acid bacteria of oenological origin for bacteriocin-encoding genes. Food Microbiol 25(8):983–991CrossRefPubMedGoogle Scholar
  86. Knoll C, Fritsch S, Schnell S, Grossmann M, Rauhut D, du Toit M (2011a) Influence of pH and ethanol on malolactic fermentation and volatile aroma compound composition in white wines. LWT Food Sci Technol 44(10):2077–2086CrossRefGoogle Scholar
  87. Knoll C, du Toit M, Schnell S, Rauhut D, Irmler S (2011b) Cloning and characterisation of a cystathionine β/γ-lyase from two Oenococcus oeni oenological strains. Appl Microbiol Biotechnol 89(4):1051–1060CrossRefPubMedGoogle Scholar
  88. 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(3):1143–1153CrossRefPubMedGoogle Scholar
  89. Labarre C, Diviès C, Guzzo J (1996) Genetic organization of the mle locus and identification of a mleR-like gene from Leuconostoc oenos. Appl Environ Microbiol 62(12):4493–4498PubMedPubMedCentralGoogle Scholar
  90. Landete JM, Ferrer S, Monedero V, Zuniga M (2013) Malic enzyme and malolactic enzyme pathways are functionally linked but independently regulated in Lactobacillus casei BL23. Appl Environ Microbiol 79:5509–5518CrossRefPubMedPubMedCentralGoogle Scholar
  91. Landete JM, Ferrer S, Pardo I (2007) Biogenic amine production by lactic acid bacteria, acetic bacteria and yeast isolated from wine. Food Control 18(12):1569–1574CrossRefGoogle Scholar
  92. Landete JM, García-Haro L, Blasco A, Manzanares P, Berbegal C, Monedero V, Zúñiga M (2010) Requirement of the Lactobacillus casei MaeKR two-component system for L-malic acid utilization via a malic enzyme pathway. Appl Environ Microbiol 76(1):84–95CrossRefPubMedGoogle Scholar
  93. Lasik-Kurdyś M, Gumienna M, Nowak J (2017) Influence of malolactic bacteria inoculation scenarios on the efficiency of the vinification process and the quality of grape wine from the central European region. Eur Food Res Technol 243(12):2163–2173CrossRefGoogle Scholar
  94. Lasik-Kurdyś M, Majcher M, Nowak J (2018) Effects of different techniques of malolactic fermentation induction on diacetyl metabolism and biosynthesis of selected aromatic esters in cool-climate grape wines. Molecules 23(10):2549.  https://doi.org/10.3390/molecules23102549 CrossRefPubMedCentralGoogle Scholar
  95. 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(22):10772–10783CrossRefPubMedGoogle Scholar
  96. Lerena MC, Rojo MC, Sari S, Mercado LA, Krieger-Weber S, Combina M (2016) Malolactic fermentation induced by Lactobacillus plantarum in Malbec wines from Argentina. S Afr J Enol Vitic 37(2):115–123Google Scholar
  97. Liu L, Zhao H, Peng S, Wang T, Su J, Liang Y, Li H, Wang H (2017a) Transcriptomic analysis of Oenococcus oeni SD-2a response to acid shock by RNA-Seq. Front Microbiol 8:1586.  https://doi.org/10.3389/fmicb.2017.01586 CrossRefPubMedPubMedCentralGoogle Scholar
  98. Liu S, Pilone GJ (2000) An overview of formation and roles of acetaldehyde in winemaking with emphasis on microbiological implications. Int J Food Sci Technol 35(1):49–61CrossRefGoogle Scholar
  99. Liu Y, Rousseaux S, Tourdot-Maréchal R, Sadoudi M, Gougeon R, Schmitt-Kopplin P, Alexandre H (2017b) Wine microbiome: a dynamic world of microbial interactions. Crit Rev Food Sci Nutr 57(4):856–873CrossRefPubMedGoogle Scholar
  100. Lonvaud-Funel A (1995) Microbiology of the malolactic fermentation: molecular aspects. FEMS Microbiol Lett 126:209–214CrossRefGoogle Scholar
  101. Lonvaud-Funel A (1999) Lactic acid bacteria in the quality improvement and depreciation of wine. Antonie Van Leeuwenhoek 76:317–331CrossRefPubMedGoogle Scholar
  102. Lonvaud-Funel A, Strasser de Saad AM (1982) Purification and properties of a malolactic enzyme from a strain of Leuconostoc mesenteroides isolated from grapes. Appl Environ Microbiol 43:357–361PubMedPubMedCentralGoogle Scholar
  103. Lucas PM, Claisse O, Lonvaud-Funel A (2008) High frequency of histamine-producing bacteria in the enological environment and instability of the histidine decarboxylase production phenotype. Appl Environ Microbiol 74(3):811–817CrossRefPubMedGoogle Scholar
  104. Lucio O, Pardo I, Heras JM, Krieger-Weber S, Ferrer S (2017) Use of starter cultures of Lactobacillus to induce malolactic fermentation in wine. Aust J Grape Wine Res 23(1):15–21CrossRefGoogle Scholar
  105. Maarman BC (2014) Interaction between wine yeast and malolactic bacteria and the impact on wine aroma and flavour. Thesis (MScAgric) Stellenbosch University http://hdl.handle.net/10019.1/86703
  106. Machielsen R, van Alen-Boerrigter IJ, Koole LA, Bongers RS, Kleerebezem M, Van Hylckama Vlieg JET (2010) Indigenous and environmental modulation of frequencies of mutation in Lactobacillus plantarum. Appl Environ Microbiol 76(5):1587–1595CrossRefPubMedGoogle Scholar
  107. Maicas S, Gil JV, Pardo I, Ferrer S (1999) Improvement of volatile composition of wines by controlled addition of malolactic bacteria. Food Res Int 32(7):491–496CrossRefGoogle Scholar
  108. Marzano M, Fosso B, Manzari C, Grieco F, Intranuovo M, Cozzi G, Mulè G, Scioscia G, Valiente G, Tullo A, Sbisà E, Pesole G, Santamaria M (2016) Complexity and dynamics of the winemaking bacterial communities in berries, musts, and wines from Apulian grape cultivars through time and space. PLoS One 11(6):e0157383.  https://doi.org/10.1371/journal.pone.0157383 CrossRefPubMedPubMedCentralGoogle Scholar
  109. Martineau B, Henick-Kling T (1995) Formation and degradation of diacetyl in wine during alcoholic fermentation with Saccharomyces cerevisiae strain EC 1118 and malolactic fermentation with Leuconostoc oenos strain MCW. Am J Enol Vitic 46:442–448Google Scholar
  110. Martineau B, Acree TE, Henick-Kling T (1995) Effect of wine type on the detection threshold for diacetyl. Food Res Int 28(2):139–143CrossRefGoogle Scholar
  111. 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(10):5715–5731CrossRefPubMedPubMedCentralGoogle Scholar
  112. Matthews A, Grbin PR, Jiranek V (2006) A survey of lactic acid bacteria for enzymes of interest to oenology. Aust J Grape Wine Res 12(3):235–244CrossRefGoogle Scholar
  113. 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(8):1990–1998CrossRefGoogle Scholar
  114. Mesas JM, Rodríguez MC, Alegre MT (2011) Characterization of lactic acid bacteria from musts and wines of three consecutive vintages of Ribeira sacra. Lett Appl Microbiol 52(3):258–268CrossRefPubMedGoogle Scholar
  115. Meyer FM, Stülke J (2013) Malate metabolism in Bacillus subtilis: distinct roles for three classes of malate-oxidizing enzymes. FEMS Microbiol Lett 339(1):17–22.  https://doi.org/10.1111/1574-6968.12041
  116. Miguel-Romero L, Casino P, Landete JM, Monedero V, Zúñiga M, Marina A (2017) The malate sensing two-component system MaeKR is a non-canonical class of sensory complex for C4-dicarboxylates. Sci Report 7(1):2708.  https://doi.org/10.1038/s41598-017-02900-z CrossRefGoogle Scholar
  117. Miller BJ, Franz CM, Cho G-S, du Toit M (2011) Expression of the malolactic enzyme gene (mle) from Lactobacillus plantarum under winemaking conditions. Curr Microbiol 62(6):1682–1688.  https://doi.org/10.1007/s00284-011-9914-4 CrossRefPubMedGoogle Scholar
  118. 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
  119. Mink R, Sommer S, Kölling R, Schmarr H-G, Baumbach L, Scharfenberger-Schmeer M (2013) Diacetyl reduction by commercial Saccharomyces cerevisiae strains during vinification. J Inst Brew 120(1):23–26CrossRefGoogle Scholar
  120. Miranda-Castilleja DE, Martínez-Peniche RÁ, Aldrete-Tapia JA, Soto-Muñoz L, Iturriaga MH, Pacheco-Aguilar JR, Arvizu-Medrano SM (2016) Distribution of native lactic acid bacteria in wineries of Queretaro, Mexico and their resistance to wine-like conditions. Front Microbiol 7:1769.  https://doi.org/10.3389/fmicb.2016.01769 CrossRefPubMedPubMedCentralGoogle Scholar
  121. Monedero V, Revilla-Guarinos A, Zúñiga M (2017) Physiological role of two-component signal transduction systems in food-associated lactic acid bacteria. Adv Appl Microbiol 99:1–51CrossRefPubMedGoogle Scholar
  122. Morgan HH, du Toit M, Setati ME (2017) The grapevine and wine microbiome: insights from high-throughput amplicon sequencing. Front Microbiol 8:820.  https://doi.org/10.3389/fmicb.2017.00820 CrossRefPubMedPubMedCentralGoogle Scholar
  123. Mtshali PS, Divol B, Van Rensburg P, du Toit M (2010) Genetic screening of wine-related enzymes in Lactobacillus species isolated from South African wines. J Appl Microbiol 108:1389–1397CrossRefPubMedGoogle Scholar
  124. Mtshali PS, Divol B, du Toit M (2012) PCR detection of enzyme-encoding genes in Leuconostoc mesenteroides strains of wine origin. World J Microbiol Biotechnol 28(4):1443–1449CrossRefPubMedGoogle Scholar
  125. Muñoz V, Beccaria B, Abreo E (2014) Simultaneous and successive inoculations of yeasts and lactic acid bacteria on the fermentation of an unsulfited Tannat grape must. Braz J Microbiol 45:59–66CrossRefPubMedPubMedCentralGoogle Scholar
  126. Naouri P, Chagnaud P, Arnaud A, Galzy P (1990) Purification and properties of a malolactic enzyme from Leuconostoc oenos ATCC 23278. J Basic Microbiol 30:577–585CrossRefPubMedGoogle Scholar
  127. Nehme N, Mathieu F, Taillandier P (2008) Quantitative study of interactions between Saccharomyces cerevisiae and Oenococcus oeni strains. J Ind Microbiol Biotechnol 35(7):685–693CrossRefPubMedGoogle Scholar
  128. Nielsen JC, Richelieu M (1999) Control of flavor development in wine during and after malolactic fermentation by Oenococcus oeni. Appl Environ Microbiol 65(2):740–745PubMedPubMedCentralGoogle Scholar
  129. Ojha KS, Mason TJ, O’Donnell CP, Kerry JP, Tiwari BK (2017) Ultrasound technology for food fermentation applications. Ultrason Sonochem 34:410–417CrossRefPubMedGoogle Scholar
  130. Ong DY (2010) Co-inoculation of yeast and bacterial starter cultures to achieve concurrent alcoholic and malolactic fermentation. Honours thesis, University of Adelaide, School of Agriculture, Food & Wine, Waite CampusGoogle Scholar
  131. Osborne JP, Edwards CG (2006) Inhibition of malolactic fermentation by Saccharomyces during alcoholic fermentation under low- and high-nitrogen conditions: a study in synthetic media. Aust J Grape Wine Res 12:69–78CrossRefGoogle Scholar
  132. Osborne JP, Mira de Orduna R, Pilone GJ, Liu SQ (2000) Acetaldehyde metabolism by wine lactic acid bacteria. FEMS Microbiol Lett 191(1):51–55CrossRefPubMedGoogle Scholar
  133. Overbeck TJ, Welker DL, Hughes JE, Steele JL, Broadbent JR (2017) Transient MutS-based hypermutation system for adaptive evolution of Lactobacillus casei to low pH. Appl Environ Microbiol 83(20):e01120–e01117.  https://doi.org/10.1128/AEM.01120-17 CrossRefPubMedPubMedCentralGoogle Scholar
  134. Palma M, Barroso CG (2002) Ultrasound-assisted extraction and determination of tartaric and malic acids from grapes and winemaking by-products. Anal Chim Acta 458(1):119–130CrossRefGoogle Scholar
  135. Pasteris SE, Strasser de Saad AM (2009) Sugar−glycerol cofermentations by Lactobacillus hilgardii isolated from wine. J Agric Food Chem 57(9):3853–3858CrossRefPubMedGoogle Scholar
  136. Peter JJ, Watson TL, Walker ME, Gardner JM, Lang TA, Borneman A, Forgan A, Tran T, Jiranek V (2018) Use of a wine yeast deletion collection reveals genes that influence fermentation performance under low-nitrogen conditions. FEMS Yeast Res 18(3):foy009–foy009.  https://doi.org/10.1093/femsyr/foy009 CrossRefGoogle Scholar
  137. Philippe C, Jaomanjaka F, Claisse O, Laforgue R, Maupeu J, Petrel M, Le Marrec C (2017) A survey of oenophages during wine making reveals a novel group with unusual genomic characteristics. Int J Food Microbiol 257:138–147.  https://doi.org/10.1016/j.ijfoodmicro.2017.06.014 CrossRefPubMedGoogle Scholar
  138. Piao H, Hawley E, Kopf S, DeScenzo R, Sealock S, Henick-Kling T, Hess M (2015) Insights into the bacterial community and its temporal succession during the fermentation of wine grapes. Front Microbiol 6:809.  https://doi.org/10.3389/fmicb.2015.00809 CrossRefPubMedPubMedCentralGoogle Scholar
  139. Pinto C, Pinho D, Cardoso R, Custódio V, Fernandes J, Sousa S, Pinheiro M, Egas C, Gomes AC (2015) Wine fermentation microbiome: a landscape from different Portuguese wine appellations. Front Microbiol 6:905.  https://doi.org/10.3389/fmicb.2015.00905 CrossRefPubMedPubMedCentralGoogle Scholar
  140. Portillo MDC, Mas A (2016) Analysis of microbial diversity and dynamics during wine fermentation of Grenache grape variety by high-throughput barcoding sequencing. LWT Food Sci Technol 72:317–321Google Scholar
  141. Pozo-Bayón MA, G-Alegría E, Polo MC, Tenorio C, Martín-Álvarez PJ, Calvo de la Banda MT, Ruiz-Larrea F, Moreno-Arribas MV (2005) Wine volatile and amino acid composition after malolactic fermentation: effect of Oenococcus oeni and Lactobacillus plantarum starter cultures. J Agric Food Chem 53(22):8729–8735CrossRefPubMedGoogle Scholar
  142. Pripis-Nicolau L, Revel G, Bertrand A, Lonvaud-Funel A (2004) Methionine catabolism and production of volatile sulphur compounds by Oenococcus oeni. J Appl Microbiol 96(5):1176–1184CrossRefPubMedGoogle Scholar
  143. Ramakrishnan V, Walker GA, Fan Q, Ogawa M, Luo Y, Luong P, Lucy Joseph CM, Bisson LF (2016) Inter-kingdom modification of metabolic behavior: [GAR+] prion induction in Saccharomyces cerevisiae mediated by wine ecosystem bacteria. Front Ecol Evol 4:137.  https://doi.org/10.3389/fevo.2016.00137 CrossRefGoogle Scholar
  144. 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(1):49–61CrossRefPubMedGoogle Scholar
  145. Renault P, Gaillardin C, Heslot H (1989) Product of the Lactococcus lactis gene required for malolactic fermentation is homologous to a family of positive regulators. J Bacteriol 171:3108–3114CrossRefPubMedPubMedCentralGoogle Scholar
  146. Renouf V, Claisse O, Lonvaud-Funel A (2005) Understanding the microbial ecosystem on the grape berry surface through numeration and identification of yeast and bacteria. Aust J Grape Wine Res 11:316–327CrossRefGoogle Scholar
  147. Renouf V, Claisse O, Lonvaud-Funel A (2007) Inventory and monitoring of wine microbial consortia. Appl Microbiol Biotechnol 75:149–164CrossRefPubMedGoogle Scholar
  148. Romero J, Ilabaca C, Ruiz M, Jara C (2018) Oenococcus oeni in Chilean red wines: technological and genomic characterization. Front Microbiol 9:90.  https://doi.org/10.3389/fmicb.2018.00090 CrossRefPubMedPubMedCentralGoogle Scholar
  149. Santivarangkna C, Higl B, Foerst P (2008) Protection mechanisms of sugars during different stages of preparation process of dried lactic acid starter cultures. Food Microbiol 25(3):429–441CrossRefPubMedGoogle Scholar
  150. Schümann C, Michlmayr H, del Hierro AM, Kulbe KD, Jiranek V, Eder R, Nguyen T-H (2013) Malolactic enzyme from Oenococcus oeni. Bioengineered 4(3):147–152.  https://doi.org/10.4161/bioe.22988 CrossRefPubMedGoogle Scholar
  151. Simó G, Fernández-Fernández E, Vila-Crespo J, Ruipérez V, Rodríguez-Nogales JM (2019) Effect of stressful malolactic fermentation conditions on the operational and chemical stability of silica-alginate encapsulated Oenococcus oeni. Food Chem 276:643–651CrossRefPubMedGoogle Scholar
  152. Smit A, Engelbrecht L, Du Toit M (2012) Managing your wine fermentation to reduce the risk of biogenic amine formation. Front Microbiol 3:76.  https://doi.org/10.3389/fmicb.2012.00076 CrossRefPubMedPubMedCentralGoogle Scholar
  153. Sternes PR, Borneman AR (2016) Consensus pan-genome assembly of the specialised wine bacterium Oenococcus oeni. BMC Genomics 17(1):308.  https://doi.org/10.1186/s12864-016-2604-7 CrossRefPubMedPubMedCentralGoogle Scholar
  154. Sternes PR, Costello PJ, Chambers PJ, Bartowsky EJ, Borneman AR (2017) Whole transcriptome RNAseq analysis of Oenococcus oeni reveals distinct intra-specific expression patterns during malolactic fermentation, including genes involved in diacetyl metabolism. Int J Food Microbiol 257:216–224CrossRefPubMedGoogle Scholar
  155. Strickland MT, Schopp LM, Edwards CG, Osborne JP (2016) Impact of Pediococcus spp. on pinot noir wine quality and growth of Brettanomyces. Am J Enol Vitic 67:188–198CrossRefGoogle Scholar
  156. Sumby KM, Grbin PR, Jiranek V (2010) Microbial modulation of aromatic esters in wine: current knowledge and future prospects. Food Chem 121(1):1–16.  https://doi.org/10.1016/j.foodchem.2009.12.004 CrossRefGoogle Scholar
  157. Sumby KM, Jiranek V, Grbin PR (2013a) Ester synthesis and hydrolysis in an aqueous environment, and strain specific changes during malolactic fermentation in wine with Oenococcus oeni. Food Chem 141(3):1673–1680.  https://doi.org/10.1016/j.foodchem.2013.03.087 CrossRefPubMedGoogle Scholar
  158. Sumby KM, Grbin PR, Jiranek V (2013b) Characterization of EstCOo8 and EstC34, intracellular esterases, from the wine-associated lactic acid bacteria Oenococcus oeni and Lactobacillus hilgardii. J Appl Microbiol 114(2):414–422.  https://doi.org/10.1111/jam.12060 CrossRefGoogle Scholar
  159. Sumby KM, Grbin PR, Jiranek V (2014) Implications of new research and technologies for malolactic fermentation in wine. Appl Microbiol Biotechnol 98(19):8111–8132.  https://doi.org/10.1007/s00253-014-5976-0 CrossRefPubMedGoogle Scholar
  160. 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(21):6729–6735.  https://doi.org/10.1128/AEM.01563-09 CrossRefPubMedPubMedCentralGoogle Scholar
  161. Swiegers JH, Bartowsky EJ, Henschke PA, Pretorius IS (2005) Yeast and bacterial modulation of wine aroma and flavour. Aust J Grape Wine Res 11(2):139–173CrossRefGoogle Scholar
  162. Takase H, Sasaki K, Kiyomichi D, Kobayashi H, Matsuo H, Takata R (2018) Impact of Lactobacillus plantarum on thiol precursor biotransformation leading to production of 3-sulfanylhexan-1-ol. Food Chem 259:99–104CrossRefPubMedGoogle Scholar
  163. Tristezza M, di Feo L, Tufariello M, Grieco F, Capozzi V, Spano G, Mita G (2016) Simultaneous inoculation of yeasts and lactic acid bacteria: effects on fermentation dynamics and chemical composition of Negroamaro wine. LWT-Food Sci Technol 66:406–412CrossRefGoogle Scholar
  164. 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. J Ag Food Chem 53(26):10134–10139.  https://doi.org/10.1021/jf0514672 CrossRefGoogle Scholar
  165. Ultee A, Wacker A, Kunz D, Löwenstein R, König H (2013) Microbial succession in spontaneously fermented grape must before, during and after stuck fermentation. S Afr J Enol Vitic 34(1):68–78Google Scholar
  166. Vallet A, Lucas P, Lonvaud-Funel A, De Revel G (2008) Pathways that produce volatile sulphur compounds from methionine in Oenococcus oeni. J Appl Microbiol 104(6):1833–1840CrossRefPubMedGoogle Scholar
  167. Vailiant H, Formisyn P, Gerbaux V (2008) Malolactic fermentation of wine: study of the influence of some physico-chemical factors by experimental design assays. J Appl Bacteriol 79(6):640–650CrossRefGoogle Scholar
  168. Versari A, Patrizi C, Parpinello G, Mattioli A, Pasini L, Meglioli M, Longhini G (2016) Effect of co-inoculation with yeast and bacteria on chemical and sensory characteristics of commercial cabernet franc red wine from Switzerland. J Chem Technol Biotechnol 91(4):876–882CrossRefGoogle Scholar
  169. Vivas N, Lonvaud-Funel A, Glories Y (1997) Effect of phenolic acids and anthocyanins on growth, viability and malolactic activity of a lactic acid bacterium. Food Microbiol 14(3):291–299CrossRefGoogle Scholar
  170. Volschenk H, van Vuuren HJJ, Viljoen-Bloom M (2003) Malo-ethanolic fermentation in Saccharomyces and Schizosaccharomyces. Curr Genet 43(6):379–391CrossRefPubMedGoogle Scholar
  171. Volschenk H, Van Vuuren HJJ, Viljoen-Bloom M (2006) Malic acid in wine: origin, function and metabolism during vinification. S Afr J Enol Vitic 27(2):123–136Google Scholar
  172. Wade ME, Strickland MT, Osborne JP, Edwards CG (2018) Role of Pediococcus in winemaking. Aust J Grape Wine Res 25:7–24.  https://doi.org/10.1111/ajgw.12366 CrossRefGoogle Scholar
  173. Wang S, Li S, Zhao H, Gu P, Chen Y, Zhang B, Zhu B (2018) Acetaldehyde released by Lactobacillus plantarum enhances accumulation of pyranoanthocyanins in wine during malolactic fermentation. Food Res Int 108:254–263CrossRefPubMedGoogle Scholar
  174. Wibowo D, Eschenbruch R, Davis CR, Fleet GH, Lee TH (1985) Occurrence and growth of lactic acid bacteria in wine: a review. Am J Enol Vitic 36(4):302–313Google Scholar
  175. Yang K, Liu M, Wang J, Hassan H, Zhang J, Qi Y, Wei X, Fan M, Zhang G (2018) Surface characteristics and proteomic analysis insights on the response of Oenococcus oeni SD-2a to freeze-drying stress. Food Chem 264:377–385Google Scholar
  176. Zé-Zé L, Tenreiro R, Brito L, Santos MA, Paveia H (1998) Physical map of the genome of Oenococcus oeni PSU-1 and localization of genetic markers. Microbiology 144(5):1145–1156CrossRefPubMedGoogle Scholar
  177. Zé-Zé L, Tenreiro R, Paveia H (2000) The Oenococcus oeni genome: physical and genetic mapping of strain GM and comparison with the genome of a “divergent” strain, PSU-1. Microbiol 146(12):3195–3204CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Wine and Food Science, School of Agriculture, Food and WineUniversity of Adelaide, Waite CampusAdelaideAustralia
  2. 2.Australian Research Council Training Centre for Innovative Wine Production, University of Adelaide, Waite CampusAdelaideAustralia

Personalised recommendations