Skip to main content
SpringerLink
Log in

Genomic variations of Oenococcus oeni strains and the potential to impact on malolactic fermentation and aroma compounds in wine

  • Mini-Review
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Malolactic fermentation (MLF) is the bacterially driven decarboxylation of l-malic acid to l-lactic acid and carbon dioxide, and brings about deacidification, flavour modification and microbial stability of wine. The main objective of MLF is to decrease wine sourness by a small increase in wine pH via the metabolism of l-malic acid. Oenococcus oeni is the main lactic acid bacterium to conduct MLF in virtually all red wine and an increasing number of white and sparkling wine bases. Over the last decade, it is becoming increasingly recognized that O. oeni exhibits a diverse array of secondary metabolic activities during MLF which can modify the sensory properties of wine. These secondary activities include the metabolism of organic acids, carbohydrates, polysaccharides and amino acids, and numerous enzymes such as glycosidases, esterases and proteases, which generate volatile compounds well above their odour detection threshold. Phenotypic variation between O. oeni strains is central for producing different wine styles. Recent studies using array-based comparative genome hybridization and genome sequencing of three O. oeni strains have revealed the large genomic diversity within this species. This review will explore the links between O. oeni metabolism, genomic diversity and wine sensory attributes.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Amerine MA, Roessler EB (1983) Wines—their sensory evaluation, 2nd edn. Freeman, San Francisco

    Google Scholar 

  • Assad-Garcia 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(4):333–338

    Article  CAS  Google Scholar 

  • Bartowsky EJ (2005) Oenococcus oeni and malolactic fermentation—moving into the molecular arena. Aust J Grape Wine Res 11(2):174–187

    Article  CAS  Google Scholar 

  • Bartowsky EJ, Henschke PA (1995) Malolactic fermentation and wine flavour. Aust Grapegrower Winemaker 378a:83–94

    Google Scholar 

  • Bartowsky EJ, Henschke PA (2004) The ‘buttery’ attribute of wine—diacetyl—desirability, spoilage and beyond. Int J Food Microbiol 96:235–252

    Article  CAS  Google Scholar 

  • Bartowsky EJ, Henschke PA (2008) Acetic acid bacteria spoilage of bottled red wine—a review. Int J Food Microbiol 125:60–70

    Article  CAS  Google Scholar 

  • Bartowsky EJ, Pretorius IS (2008) Microbial formation and modification of flavour and off-flavour compounds in wine. In: König H, Unden G, Fröhlich J (eds) Biology of microorganisms on grapes, in must and wine. Springer, Heidelberg, pp 211–233

    Google Scholar 

  • Bartowsky E, Costello P, Henschke P (2002a) Management of malolactic fermentation—wine flavour manipulation. Aust Grapegrower Winemaker 461a:7–12

    Google Scholar 

  • Bartowsky EJ, Francis IL, Bellon JR, Henschke PA (2002b) Is buttery aroma perception in wines predictable from diacetyl concentration? Aust J Grape Wine Res 8:180–185

    Article  CAS  Google Scholar 

  • Bartowsky E, Costello P, McCarthy J (2008) MLF—adding an ‘extra dimension’ to wine flavour and quality. Aust NZ Grapegrower Winemaker 533a:60–65

    Google Scholar 

  • Bartowsky E, Costello P, Krieger-Weber S, Markides A, Francis L, Travis B (2010) Influence of malolactic fermentation on the fruity characters of red wine—bringing wine chemistry and sensory together. In: International Intervitis Interfructa Congress 2010, Stuttgart, Germany, 24–28 March 2010. pp 52–59

  • Beltramo C, Oraby M, Bourel G, Garmyn D, Guzzo J (2004) A new vector, pGID052, for genetic transfer in Oenococcus oeni. FEMS Microbiol Lett 236(1):53–60

    CAS  Google Scholar 

  • Bon E, Delaherche A, Bilhere E, De Daruvar A, Lonvaud-Funel A, Le Marrec C (2009) Oenococcus oeni genome plasticity is associated with fitness. App Environ Microbiol 75(7):2079–2090

    Article  CAS  Google Scholar 

  • Borneman AR, Bartowsky EJ, McCarthy J, Chambers PJ (2010) Genotypic diversity in Oenococcus oeni by high-density microarray comparative genome hybridization and whole genome sequencing. Appl Microbiol Biotechnol 86(2):681–691. doi:10.1007/s00253-009-2425-6

    Article  CAS  Google Scholar 

  • Canas PMI, Perez PR, Prieto SS, Herreros MLP (2009) Ecological study of lactic acid microbiota isolated from Tempranillo wines of Castilla-La Mancha. J Biosci Bioeng 108(3):220–224

    Article  CAS  Google Scholar 

  • Capaldo A, Walker ME, Ford CM, Jiranek V (2011) beta-Glucoside metabolism in Oenococcus oeni: cloning and characterisation of the phospho-beta-glucosidase bgID. Food Chem 125(2):476–482

    Article  CAS  Google Scholar 

  • Capozzi V, Russo P, Beneduce L, Weidmann S, Grieco F, Guzzo J, Spano G (2010) Technological properties of Oenococcus oeni strains isolated from typical southern Italian wines. Lett Appl Microbiol 50(3):327–334

    Article  CAS  Google Scholar 

  • Caspritz G, Radler F (1983) Malolactic enzyme of Lactobacillus plantarum. Purification, properties, and distribution among bacteria. J Biol Chem 258:4907–4910

    CAS  Google Scholar 

  • Chambers PJ, Pretorius IS (2010) Fermenting knowledge: the history of winemaking, science and yeast research. EMBO Rep 11(12):914–920

    Article  CAS  Google Scholar 

  • Cogan TM (1995) Flavour production by dairy starter cultures. J Appl Bacteriol Symp Suppl 79:49S–64S

    Google Scholar 

  • Curtin CD, Bellon JR, Henschke PA, Godden P, de Barros LM (2007) Genetic diversity of Dekkera bruxellensis yeasts isolated from Australian wineries. FEMS Yeast Res 7(3):471–481

    Article  CAS  Google Scholar 

  • Dicks LMT (1994) Transformation of Leuconostoc oenos by electroporation. Biotechnol Tech 8(12):901–904

    Article  CAS  Google Scholar 

  • Dicks LMT, Dellaglio F, Collins MD (1995) Proposal to reclassify Leuconostoc oenos as Oenococcus oeni [corrig.] gen. nov., comb. nov. Int J Sys Evol Bacteriol 45(2):395–397

    Article  CAS  Google Scholar 

  • D'Incecco N, Bartowsky E, Kassara S, Lante A, Spettolli P, Henschke P (2004) Release of glycosidically bound flavour compounds of Chardonnay by Oenococcus oeni during malolactic fermentation. Food Microbiol 21(3):257–265

    Article  Google Scholar 

  • Endo A, Okada S (2006) Oenococcus kitaharae sp nov., a non-acidophilic and non-malolactic-fermenting oenococcus isolated from a composting distilled shochu residue. Int J Sys Evol Microbiol 56:2345–2348. doi:10.1099/ijs.0.64288-0

    Article  CAS  Google Scholar 

  • Eom HJ, Cho SK, Park MS, Ji GE, Han NS (2010) Characterization of Leuconostoc citreum plasmid pCB18 and development of broad host range shuttle vector for lactic acid bacteria. Biotechnol Bioprocess Eng 15(6):946–952. doi:10.1007/s12257-010-0089-9

    Article  CAS  Google Scholar 

  • Francis IL, Newton JL (2005) Determining wine aroma from compositional data. Aust J Grape Wine Res 11(2):114–126

    Article  CAS  Google Scholar 

  • Garmyn D, Monnet C, Martineau B, Guzzo J, Cavin J-F, Diviès C (1996) Cloning and sequencing of the gene encoding α-acetolactate decarboxylase from Leuconostoc oenos. FEMS Microbiol Lett 145:445–450

    CAS  Google Scholar 

  • Garvie EI (1967) Leuconostoc oenos sp.nov. J Gen Microbiol 48(3):431–438. doi:10.1099/00221287-48-3-431

    CAS  Google Scholar 

  • Gerbaux V, Briffox C, Dumont A, Krieger S (2009) Influence of inoculation with malolactic bacteria on volatile phenols in wines. Am J Enol Vitic 60(2):233–235

    CAS  Google Scholar 

  • 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(4):362–369

    CAS  Google Scholar 

  • Grimaldi A, Bartowsky E, Jiranek V (2005) A survey of glycosidase activities of commercial wine strains of Oenococcus oeni. Int J Food Microbiol 105(2):233–244

    Article  CAS  Google Scholar 

  • Gunata Z, Bitteur S, Brillouet J-M, Bayonove C, Cordonnier R (1988) Sequential enzymatic hydrolysis of potentially aromatic glycosides from grape. Carbohyd Res 184:139–149

    Article  CAS  Google Scholar 

  • Gunata YZ, Bayonove CL, Tapiero C, Cordonnier RE (1990) Hydrolysis of grape monoterpenyl β-D-glucosides by various β-glucosidases. J Agric Food Chem 38:1232–1236

    Article  CAS  Google Scholar 

  • Guth H (1997a) Identification of character impact odorants of different white wine varieties. J Agric Food Chem 45(8):3022–3026

    Article  CAS  Google Scholar 

  • Guth H (1997b) Quantitation and sensory studies of character impact odorants of different white wine varieties. J Agric Food Chem 45(8):3027–3032

    Article  CAS  Google Scholar 

  • Henick-Kling T (1993) Malolactic fermentation. In: Fleet GH (ed) Wine microbiology and biotechnology. Harwood Academic Publisher, Amsterdam, pp 289–326

    Google Scholar 

  • Iland P, Gago P, Caillard A, Dry P (2009) A taste of the world of wine. Patrick Iland Wine Promotions Pty Ltd, Campbelltown

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Kunkee RE (1991) Some roles of malic acid in the malolactic fermentation in wine making. FEMS Microbiol Rev 88:55–72

    Article  CAS  Google Scholar 

  • Labarre C, Divies C, Guzzo J (1996a) Genetic organization of the mle locus and identification of a mleR-like gene from Leuconostoc oenos. App Environ Microbiol 62(12):4493–4498

    CAS  Google Scholar 

  • Labarre C, Guzzo J, Cavin JF, Divies C (1996b) Cloning and characterization of the genes encoding the malolactic enzyme and the malate permease of Leuconostoc oenos. App Environ Microbiol 62(4):1274–1282

    CAS  Google Scholar 

  • Laurent M-H, Henick-Kling T, Acree TE (1994) Changes in the aroma and odor of Chardonnay wine due to malolactic fermentation. Vitic Enol Sci 49:3–10

    CAS  Google Scholar 

  • Li H, Zhang CH, Liu YL (2006) Species attribution and distinguishing strains of Oenococcus oeni isolated from Chinese wines. World J Microb Biot 22(5):515–518

    Article  CAS  Google Scholar 

  • Lonvaud-Funel A (2001) Biogenic amines in wines: role of lactic acid bacteria. FEMS Microbiol Lett 199(1):9–13

    Article  CAS  Google Scholar 

  • Lonvaud-Funel A, Strasser de Saad AM (1982) Purification and properties of a malolactic enzyme from a strain of Leuconostoc mesenteroides isolated from grapes. App Environ Microbiol 43:357–361

    CAS  Google Scholar 

  • Loureiro V, Malfeito-Ferreira M (2003) Spoilage yeasts in the wine industry. Int J Food Microbiol 86:23–50

    Article  CAS  Google Scholar 

  • Martineau B, Henick-Kling T (1995) Performance and diacetyl production of commercial strains of malolactic bacteria in wine. J Appl Bacteriol 78:526–536

    Article  CAS  Google Scholar 

  • Martineau B, Acree TE, Henick-Kling T (1995) Effect of wine type on the detection threshold for diacetyl. Food Res Int 28(2):139–143

    Article  CAS  Google Scholar 

  • 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. App Environ Microbiol 70(10):5715–5731. doi:10.1128/aem.70.10.5715-5731.2004

    Article  CAS  Google Scholar 

  • Michlmayr H, Schumann C, da Silva N, Kulbe KD, del Hierro AM (2010a) Isolation and basic characterization of a beta-glucosidase from a strain of Lactobacillus brevis isolated from a malolactic starter culture. J Appl Microbiol 108(2):550–559. doi:10.1111/j.1365-2672.2009.04461.x

    Article  CAS  Google Scholar 

  • Michlmayr H, Schumann C, Wurbs P, da Silva N, Rogl V, Kulbe KD, del Hierro AM (2010b) A beta-glucosidase from Oenococcus oeni ATCC BAA-1163 with potential for aroma release in wine: cloning and expression in E. col. World J Microb Biot 26(7):1281–1289

    Article  CAS  Google Scholar 

  • Michlmayr H, Schumann C, Kulbe KD, del Hierro AM (2011) Heterologously expressed family 51 α-L-arabinofurnaosidases from Oenococcus oeni and Lactobacillus brevis. App Environ Microbiol 77(4):1528–1531

    Article  CAS  Google Scholar 

  • 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 29:465–475

    CAS  Google Scholar 

  • Möslinger (1901) Über die Säuren des Weines und den Säurerückgang. Zeitschr f Untersuchung d Nahr Genussmittel 4:1120–1130

    Google Scholar 

  • Müller-Thurgau H (1891) Über die Ergebnisse neuer Untersuchungen auf den Gebiete der Weinbereitung. Ber XII Dtsch Weinbaukong (Worms):128

  • Müller-Thurgau H, Osterwalder A (1913) Die Bakterien im Wein und Obstwein und die dadurch verursachten Veränderungen. Zentr Bakt Parasitenk Hyg Abt 2(36):129–338

    Google Scholar 

  • Naouri P, Chagnaud P, Arnaud A, Galzy P (1990) Purification and properties of a malolactic enzyme from Leuconostoc oenos ATCC-23278. J Basic Microb 30(8):577–585

    Article  CAS  Google Scholar 

  • Nielsen JC, Prahl C, Lonvaud-Funel A (1996) Malolactic fermentation in wine by direct inoculation with freeze-dried Leuconostoc oenos cultures. Am J Enol Vitic 47(1):42–48

    CAS  Google Scholar 

  • Pasteur L (1873) Études sur le Vin, 2nd edn. Savy, Paris

    Google Scholar 

  • Pineau B, Barbe JC, Van Leeuwen C, Dubourdieu D (2009) Examples of perceptive interactions involved in specific “red-” and “black-berry” aromas in red wines. J Agric Food Chem 57(9):3702–3708

    Article  CAS  Google Scholar 

  • Pineau B, Barbe JC, van Leeuwen C, Dubourdieu D (2010) Olfactory specificity of red- and black-berry fruit aromas in red wines and contribution to the red Bordeaux wine concept. Journal International Des Sciences De La Vigne Et Du Vin 44(1):39–49

    CAS  Google Scholar 

  • Ramos A, Poolman B, Santos H, Lolkema JS, Konings WN (1994) Uniport of anionic citrate and proton consumption in citrate metabolism generates a proton motive force in Leuconostoc oenos. J Bacteriol 176(16):4899–4905

    CAS  Google Scholar 

  • Ramos A, Lolkema JS, Konings WN, Santos H (1995) Enzyme basis for pH regulation of citrate and pyruvate metabolism by Leuconostoc oenos. App Environ Microbiol 61(4):1303–1310

    CAS  Google Scholar 

  • Renouf V, Claisse O, Lonvaud-Funel A (2007) Inventory and monitoring of wine microbial consortia. Appl Microbiol Biotechnol 75(1):149–164

    Article  CAS  Google Scholar 

  • Ruiz P, Izquierdo PM, Sesena S, Palop ML (2010) Selection of autochthonous Oenococcus oeni strains according to their oenological properties and vinification results. Int J Food Microbiol 137(2–3):230–235

    Article  CAS  Google Scholar 

  • Schmid F, Li Y, Liebich B, Culbert J, Day C, Jiranek V (2007) Evaluation of red wine made on a small scale utilizing frozen must. J Agric Food Chem 55(17):7156–7161

    Article  CAS  Google Scholar 

  • Segurel MA, Razungles AJ, Riou C, Salles M, Baumes RL (2004) Contribution of dimethyl sulfide to the aroma of Syrah and Grenache Noir wines and estimation of its potential in grapes of these varieties. J Agric Food Chem 52(23):7084–7093

    Article  CAS  Google Scholar 

  • Sico MA, Bonomo MG, Salzano G (2008) Isolation and characterization of Oenococcus oeni from Aglianico wines. World J Microb Biot 24(9):1829–1835

    Article  Google Scholar 

  • Siebert TE, Smythe 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 381:937–947

    Article  CAS  Google Scholar 

  • Smit G, Smit BA, Engels WJM (2005) Flavour formation by lactic acid bacteria and biochemical flavour profiling of cheese products. FEMS Microbiol Rev 29(3):591–610

    Article  CAS  Google Scholar 

  • Solieri L, Genova F, De Paola M, Giudici P (2010) Characterization and technological properties of Oenococcus oeni strains from wine spontaneous malolactic fermentations: a framework for selection of new starter cultures. J Appl Microbiol 108(1):285–298

    Article  CAS  Google Scholar 

  • Spettoli P, Nuti MP, Zamorani A (1984) Properties of malolactic activity purified from Leuconostoc oenos ML34 by affinity chromatography. App Environ Microbiol 9:184–189

    Google Scholar 

  • Sponholz W-R (1993) Wine spoilage by microorganisms. In: Fleet GH (ed) Wine microbiology and technology. Harwood Academic Publishing, Amsterdam, pp 395–420

    Google Scholar 

  • 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):139–173

    Article  CAS  Google Scholar 

  • 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 Agric Food Chem 53(26):10134–10139

    Article  CAS  Google Scholar 

  • 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(14):2468–2476. doi:10.1002/jsfa.2650

    Article  CAS  Google Scholar 

  • Ugliano M, Genovese A, Moio L (2003) Hydrolysis of wine aroma precursors during malolactic fermentation with four commercial starter cultures of Oenococcus oeni. J Agric Food Chem 51(17):5073–5078. doi:10.1021/jf0342019

    Article  CAS  Google Scholar 

  • Vigentini I, Picozzi C, Tirelli A, Giugni A, Foschino R (2009) Survey on indigenous Oenococcus oeni strains isolated from red wines of Valtellina, a cold climate wine-growing Italian area. Int J Food Microbiol 136(1):123–128

    Article  CAS  Google Scholar 

  • Williams PJ, Strauss CR, Wilson B, Massy-Westropp RA (1982) Novel monoterpene disaccharide glycosides of Vitis vinifera grapes and wines. Phytochemistry 21:2013–2020

    Article  CAS  Google Scholar 

  • Williams PJ, Sefton MA, Wilson B (1989) Nonvolatile conjugates of secondary metabolites as precursors of varietal grape flavour components. In: Teranishi R, Buttery RG, Shahisi R (eds) Flavour chemistry, trends and developments, ACS symposium series no 388. American Chemical Society, Washington DC, pp 35–48

    Chapter  Google Scholar 

  • Yanagida F, Srionnual S, Chen YS (2008) Isolation and characteristics of lactic acid bacteria from koshu vineyards in Japan. Lett Appl Microbiol 47(2):134–139. doi:10.1111/j.1472-765X.2008.02398.x

    Article  CAS  Google Scholar 

  • Ze-Ze L, Teneiro R, Brito L, Santos MA, Paveia H (1998) Physical map of the genome of Oenococcus oeni PSU-1 and localization of genetic markers. Microbiology 144:1145–1156

    Article  CAS  Google Scholar 

  • Ze-Ze L, Teneiro R, Paveia H (2000) The Oenococcus oeni genome: physical and genetic map of strain GM and comparison with the genome of a ‘divergent’ strain, PSU-1. Microbiology 146(12):3195–3204

    CAS  Google Scholar 

  • 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(4):237–244

    CAS  Google Scholar 

Download references

Acknowledgements

The authors thank Dr. Paul Chambers for discussions during the preparation of this mini review and Lallemand SA for allowing us to use data presented in Fig. 2 from a project for which they provided financial support. The Australian Wine Research Institute (AWRI) is supported by Australian grapegrowers and winemakers through their investment agency, the Grape and Wine Research and Development Corporation, with matching funds from the Australian Government. The AWRI is a member of the Wine Innovation Cluster in Adelaide.

Author information

Authors and Affiliations

  1. The Australian Wine Research Institute, PO Box 197, Glen Osmond, Adelaide, SA, 5064, Australia

    Eveline J. Bartowsky & Anthony R. Borneman

Authors
  1. Eveline J. Bartowsky
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Anthony R. Borneman
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Eveline J. Bartowsky.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bartowsky, E.J., Borneman, A.R. Genomic variations of Oenococcus oeni strains and the potential to impact on malolactic fermentation and aroma compounds in wine. Appl Microbiol Biotechnol 92, 441–447 (2011). https://doi.org/10.1007/s00253-011-3546-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-011-3546-2

Keywords

Search

Navigation