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.
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References
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):255–265
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
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):12371–12383
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
Barata A, Malfeito-Ferreira M, Loureiro V (2012) The microbial ecology of wine grape berries. Int J Food Microbiol 153(3):243–259
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):441–447
Bartowsky EJ, Costello PJ, Chambers PJ (2015) Emerging trends in the application of malolactic fermentation. Aust J Grape Wine Res 21(S1):663–669
Bartowsky EJ, Henschke PA (2004) The “buttery” attribute of wine—diacetyl—desirability, spoilage and beyond. Int J Food Microbiol 96(3):235–252
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):9510–9523
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):28–31
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
Betteridge A, Grbin P, Jiranek V (2015) Improving Oenococcus oeni to overcome challenges of wine malolactic fermentation. Trends Biotechnol 33(9):547–553
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 102:921–932
Bisson LF (1999) Stuck and sluggish fermentations. Am J Enol Vitic 50(1):107–119
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):3311–3321
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
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 82:15–21
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 50:2344–2349
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
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):73–79
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):2875–2882
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):2854–2866
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
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 B2
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 106:22–28
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 69:211–216
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
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):130–137
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
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
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):245–254
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
Cappello MS, Zapparoli G, Logrieco A, Bartowsky EJ (2017) Linking wine lactic acid bacteria diversity with wine aroma and flavour. Int J Food Microbiol 243:16–27
Capucho I, San Romão MV (1994) Effect of ethanol and fatty acids on malolactic activity of Leuconostoc oenos. Appl Microbiol Biotechnol 42:391–395
Caspritz G, Radler F (1983) Malolactic enzyme of Lactobacillus plantarum. Purification, properties, and distribution among bacteria. J Biol Chem 258:4907–4910
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
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
Comitini F, Ciani M (2007) The inhibitory activity of wine yeast starters on malolactic bacteria. Ann Microbiol 57(1):61–66
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 99:105–111
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 246:12–19
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):287–301
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):797–806
Couto JA, Campos FM, Figueiredo AR, Hogg TA (2006) Ability of lactic acid bacteria to produce volatile phenols. Am J Enol Vitic 57(2):166–171
Curioni PMG, Bosset JO (2002) Key odorants in various cheese types as determined by gas chromatography–olfactometry. Int Dairy J 12(12):959–984
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):811–821
Davis CR, Wibowo D, Eschenbruch R, Lee TH, Fleet GH (1985) Practical implications of malolactic fermentation: a review. Am J Enol Vitic 36(4):290–301
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):539–545
Davis CR, Wibowo D, Fleet GH, Lee TH (1988) Properties of wine lactic acid bacteria: their potential enological significance. Am J Enol Vitic 39:137–142
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):42–48
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):490–494
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 53:10–17
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
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):3783–3792
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
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
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):698–702
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
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):5118–5125
Fleet GH (2003) Yeast interactions and wine flavour. Int J Food Microbiol 86(1):11–22
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 73:489–496
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 81:326–334
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):1973–1979
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):27–32
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):925–933
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 239:252–259
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):4046–4057
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 954:105–113
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
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):200–209
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 217:110–116
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 269:19–26
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):233–244
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):1061–1069
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 20:144–149
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):133–141
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):805–808
Henick-Kling T (1993) Malolactic fermentation. In: Fleet GH (ed) Wine microbiology and biotechnology. Harwood Academic Publishers, Chur, Switzerland, pp 289–326
Henick-Kling T, Lee TH, Nicholas DJD (1986) Inhibition of bacterial growth and malolactic fermentation in wine by bacteriophage. J Appl Bacteriol 61(4):287–293
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):1–10
Hugenholtz J (1993) Citrate metabolism in lactic acid bacteria. FEMS Microbiol Rev 12:165–178
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 73:557–566
Jenkins DE, Schultz JE, Matin A (1988) Starvation-induced cross protection against heat or H2O2 challenge in Escherichia coli. J Bacteriol 170(9):3910–3914
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 73:150–159
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):586–595
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):983–991
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):2077–2086
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):1051–1060
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):1143–1153
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):4493–4498
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 79:5509–5518
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):1569–1574
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):84–95
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):2163–2173
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
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):10772–10783
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):115–123
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
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):49–61
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):856–873
Lonvaud-Funel A (1995) Microbiology of the malolactic fermentation: molecular aspects. FEMS Microbiol Lett 126:209–214
Lonvaud-Funel A (1999) Lactic acid bacteria in the quality improvement and depreciation of wine. Antonie Van Leeuwenhoek 76:317–331
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 43:357–361
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):811–817
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):15–21
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
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):1587–1595
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):491–496
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
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 46:442–448
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
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):5715–5731
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):235–244
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):1990–1998
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):258–268
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
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
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
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
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):23–26
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
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 99:1–51
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
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 108:1389–1397
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):1443–1449
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 45:59–66
Naouri P, Chagnaud P, Arnaud A, Galzy P (1990) Purification and properties of a malolactic enzyme from Leuconostoc oenos ATCC 23278. J Basic Microbiol 30:577–585
Nehme N, Mathieu F, Taillandier P (2008) Quantitative study of interactions between Saccharomyces cerevisiae and Oenococcus oeni strains. J Ind Microbiol Biotechnol 35(7):685–693
Nielsen JC, Richelieu M (1999) Control of flavor development in wine during and after malolactic fermentation by Oenococcus oeni. Appl Environ Microbiol 65(2):740–745
Ojha KS, Mason TJ, O’Donnell CP, Kerry JP, Tiwari BK (2017) Ultrasound technology for food fermentation applications. Ultrason Sonochem 34:410–417
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 Campus
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 12:69–78
Osborne JP, Mira de Orduna R, Pilone GJ, Liu SQ (2000) Acetaldehyde metabolism by wine lactic acid bacteria. FEMS Microbiol Lett 191(1):51–55
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
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):119–130
Pasteris SE, Strasser de Saad AM (2009) Sugar−glycerol cofermentations by Lactobacillus hilgardii isolated from wine. J Agric Food Chem 57(9):3853–3858
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
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
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
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
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 72:317–321
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):8729–8735
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):1176–1184
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
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):49–61
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 171:3108–3114
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 11:316–327
Renouf V, Claisse O, Lonvaud-Funel A (2007) Inventory and monitoring of wine microbial consortia. Appl Microbiol Biotechnol 75:149–164
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
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):429–441
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
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 276:643–651
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
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
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 257:216–224
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 67:188–198
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
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
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
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
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
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
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 259:99–104
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 66:406–412
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
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):68–78
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):1833–1840
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):640–650
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):876–882
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):291–299
Volschenk H, van Vuuren HJJ, Viljoen-Bloom M (2003) Malo-ethanolic fermentation in Saccharomyces and Schizosaccharomyces. Curr Genet 43(6):379–391
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):123–136
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
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 108:254–263
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):302–313
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 264:377–385
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):1145–1156
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):3195–3204
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/).
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Sumby, K.M., Bartle, L., Grbin, P.R. et al. Measures to improve wine malolactic fermentation. Appl Microbiol Biotechnol 103, 2033–2051 (2019). https://doi.org/10.1007/s00253-018-09608-8
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DOI: https://doi.org/10.1007/s00253-018-09608-8