Wibowo D Et Al (1985) Occurrence and Growth of Lactic-acid Bacteria in Wine – a Review
Introduction
Wine is the effect of the alcoholic fermentation (AF) driven out by oenological yeasts in a complex microbial environs (Constantí et al., 1997; Beltran et al., 2002). Apart from Saccharomyces cerevisiae, recognized as the main agent of this procedure, other yeast species, known every bit non-Saccharomyces yeasts, such equally Hanseniaspora/Kloeckera, Pichia, Candida, or Metschnikowia are implicated in early stages of the AF (Fleet et al., 1984). After the AF, the resultant vino can undergo the malolactic fermentation (MLF), which consists on a adequately simple reaction: a unique enzymatic decarboxylation of the 50-malic acid to L-lactic acid (Liu, 2002). It is usually performed in red wines or high acidity white wines. This fermentation is carried out by lactic acid bacteria (LAB). Four LAB genera are usually found in wine: Lactobacillus, Pediococcus, Leuconostoc, and Oenococcus; and particularly, the main ascendant species in wine is Oenococcus oeni (Wibowo et al., 1985; Lonvaud-Funel, 1999; Liu, 2002). MLF is related to a quality comeback in wine since this biotransformation leads to a pH increment, enhanced organoleptic properties and a microbial stabilization (Lonvaud-Funel, 1999). During MLF, LAB swallow L-malic acid and other nutrients, impoverishing vino and avoiding the development of contaminant microorganisms.
In the last few years the involvement on the use of not-Saccharomyces yeasts in winemaking has increased (Padilla et al., 2016; Petruzzi et al., 2017), due to the detail enzymatic activities that catalyze the liberation of aromas from their non-volatile precursors (Belda et al., 2017). Generally, these yeasts are inoculated to first the AF of must and later Southward. cerevisiae is inoculated to cease the process. This type of sequential inoculation with non-Saccharomyces undergoes chemical changes in vino which modulate the organoleptic contour of wines (Fleet, 2008; Padilla et al., 2016). What is more, this chemical modulation presents new scenery in which MLF may take place.
The purpose of this mini review is to summarize the current knowledge nigh the compounds responsible for the interactions that may take place betwixt oenological yeasts and LAB during winemaking, highlighting the new scenery of non-Saccharomyces fermentations.
Yeast-Lab Interactions: Oenological Context
The performance of MLF by LAB is highly affected past the physicochemical intrinsic properties of vino, such as pH, ethanol, and then2 (Carreté et al., 2002; Arnink and Henick-Kling, 2005). Moreover, since MLF takes identify usually after the AF, it is besides influenced by yeast metabolism. Those interactions range from inhibitory, to neutral and stimulatory. There is not much literature about this topic, only information technology is agreed that the blazon and impact of the interactions is dependent on several factors like (I) the initial must composition, (II) the yeast/bacteria strain combination, (3) the uptake and release of nutrients by yeasts, and (IV) the power of yeasts to produce metabolites that affect somehow LAB (King and Beelman, 1986; Lonvaud-Funel et al., 1988; Alexandre et al., 2004; Du Plessis et al., 2017). There are some compounds which mediate these interactions (Figure i) but, yet the available information is not sufficient.
Effigy 1. Compounds produced by yeast that can mediate inhibitory, stimulatory, or unknown consequence in Oenococcus oeni growth or MLF operation.
Up to date, some strategies have been developed to mitigate the possible yeast- O. oeni inhibitory interactions (Sumby et al., 2014). Specifically, coinoculation of yeast and O. oeni has been proposed every bit a promising strategy to reduce the length of MLF (Izquierdo Cañas et al., 2014). In this mode, the simultaneous AF and MLF co-immobilized in alginate beads is a technique currently in study (Bleve et al., 2016). Another classical approach to bargain with the MLF difficulties is to select specific strains from the nature (Campbell-Sills et al., 2017; Petruzzi et al., 2017). The purpose of this selection is to identify the virtually relevant microorganisms related with the fermentation process in a particular expanse and apply them as culture starters (Portillo et al., 2016; Franquès et al., 2017; Petruzzi et al., 2017).
Above the direct yeasts issue upon LAB and MLF operation, the must, and the winemaking practices, accept a strong impact in how these interactions take place (Arnink and Henick-Kling, 2005; Tristezza et al., 2016).
Beyond the detail product of certain compounds (Tabular array i), yeast metabolism exhausts the nutrients of the medium. LAB take complex nutrient requirements (Garvie, 1967; Fourcassie et al., 1992; Terrade and Mira de Orduña, 2009), then their growth is highly dependent on the nutrients consumption during AF past yeasts (Ivey et al., 2013). The upshot of these inhibitory interactions could be explained as the result of nutrient competition, such as yeast assimilable nitrogen (YAN) or amino acids (Costello et al., 2003). Therefore, yeast strains with circuitous nutrient requirements would showroom an increased combative human relationship with LAB (Costello et al., 2003). In this fashion, it has been recently described that coinoculation of Southward. cerevisiae with other non-Saccharomyces yeasts result in a metabolic stimulation of glucose and nitrogen uptake past yeasts, which could lead to a more impoverished medium for LAB (Curiel et al., 2017).
TABLE i. Master compounds affected (variation in content, negative or positive) by the utilise of non-Saccharomyces in alcoholic fermentation regarding to S. cerevisiae every bit sole starter.
Moreover, it has been reported that the employ of some yeast strains (Su et al., 2014) can cause a decrease in L-malic acid, the prior substrate of LAB in wine, which can negatively bear on the MLF performance. Especially, the use of non-Saccharomyces leads a higher consumption of L-malic acid, equally it has been described with Torulaspora delbrueckii (Belda et al., 2015), Starmerella bacillaris (syn. Candida zemplinina) (Tofalo et al., 2012; Du Plessis et al., 2017), M. pulcherrima (Du Plessis et al., 2017), and Issatchenkia orientalis (Kim et al., 2008). There is also some other non-Saccharomyces yeast that actually consumes L-malic acid to dryness (Du Plessis et al., 2017). Schizosaccharomyces spp. can develop the maloalcoholic fermentation by consuming both sugars and 50-malic acid (Benito et al., 2013, 2014).
Alcoholic fermentation of grape must undergoes deep chemical changes enhanced past ethanol and sulfur dioxide. Long ago, it is agreed that concentrations over 4% (v/v) of ethanol inhibit the growth of most LAB (Capucho and San Romao, 1994). Also, a more recent study reported the triad of ethanol, SO2 and medium chain fatty acids (MCFAs) as the main inhibitor compounds in the animosity between yeast and O. oeni (Nehme et al., 2008). The main functional categories of genes affected by ethanol are metabolite transport and cell wall and membrane biogenesis (Olguín et al., 2015). Present, some non-Saccharomyces yeasts are currently used in mixed fermentations to decrease the alcoholic content of wines (Giaramida et al., 2013; Loira et al., 2014; Ciani et al., 2016), such as M. pulcherrima (Contreras et al., 2014), T. delbrueckii (Belda et al., 2015), C. stellata (Ferraro et al., 2000) and Southward. bacillaris (Englezos et al., 2016a), possibly mitigating the negative event of ethanol upon LAB growth.
The role of SO2 equally an antimicrobial compound is known since aboriginal Romans that used to add together this chemical to forestall food and beverage from spoilage. Its active mechanism affects O. oeni membrane and causes an ATPase action subtract (Carreté et al., 2002), causing a delay or the failure of MLF (Lonvaud-Funel et al., 1988). It is customary to use this compound to control microbial communities since vineyard to wine in the winemaking. Moreover, yeasts are able to produce this compound as result of their metabolism (Wells and Osborne, 2011). The common corporeality of SO2 produced by Due south. cerevisiae strains is less than 30 mg/50, but some strains tin produce more than 100 mg/L of this compound (Suzzi et al., 1985; Rankine, 1968). When it comes to non-Saccharomyces yeasts, there is no much information about their Thentwo production since they are more than affected by this compound (Jolly et al., 2014). However, information technology has to exist pointed that the utilise of T. delbrueckii as sole starter increased the Sotwo concentration of the final wine (Belda et al., 2015). Apart from the cited strain effect, the medium has great influence in the production of SO2 by yeasts. Higher concentration of YAN in must ends on higher amount of Then2 (Osborne and Edwards, 2006), equally upshot of the metabolism of the sulfured amino acids.
Medium Chain Fatty Acids (MCFAs)
During AF, yeasts produce different compounds as result of their growth metabolism that can inhibit O. oeni growth and MLF. MCFA (C8–Cfourteen) institute a grouping of organic molecules that can limit O. oeni growth and fifty-fifty subtract their 50-malic consumption (Edwards and Beelman, 1987; Lonvaud-Funel et al., 1988). It has to exist mentioned the strong effect of winemaking practices in fatty acids metabolism by yeasts (Guilloux-Benatier et al., 1998). These authors related a fine MLF operation with a large pre fermentative maceration, possibly due to the high macromolecules concentration and long chain fatty acid extraction (Guilloux-Benatier et al., 1995, 1998). The outcome of using non-Saccharomyces yeasts in the production of MCFA is variable. Strains belonging to M. pulcherrima, C. stella, and Pichia fermentans increment the final concentration of MCFA (Liu P.-T. et al., 2016). In contrast, mixed fermentations with H. uvarum, I. orientalis nowadays the contrary beliefs (Liu P.-T. et al., 2016). Also, a significant subtract in MCFA concentration has been reported past Lanchacea thermotolerans as sole starter (Shekhawat et al., 2017). Hu et al. (2018) reported a strong influence in MCFA concentration related with the inoculation timing of H. uvarum in mixed fermentation with Due south. cerevisiae. In this experiment inoculation timing seem to determine the increase or decrease in MCFA concentration regarding to S. cerevisiae traditional fermentation. Generally, C12 and C14, as free fatty acids, are the almost toxic MCFA for O. oeni (Guilloux-Benatier et al., 1998). Moreover, the esterified forms are even more toxic than free fatty acids, being the most toxic esterified MCFA C10, C12, and C14 (Guilloux-Benatier et al., 1998). So, depending on the particular MCFA and its concentration, the inhibitory effect can go lethal to LAB (Edwards and Beelman, 1987).
Organic Acids Similar to L-Malic Acid
Malolactic fermentation is the effect of a unique enzymatic activity performed by the malolactic enzyme. Accordingly, structurally like organic acids will human action equally competitive inhibitors for the active site of the malolactic enzyme (Lonvaud-Funel and Strasser de Saad, 1982) and probably they will filibuster the MLF elapsing. Early studies in this subject related this effect with succinic acid, fumaric acid, citric acid, and tartaric acid (Lonvaud-Funel and Strasser de Saad, 1982; Davis et al., 1985). Amidst these acids, succinic acid is the most studied since oenological yeasts can largely produce this compound. First studies related the inhibition of MLF past criotolerant S. cerevisiae strains which are characterized past high product of succinic acid and β-phenylethanol (Caridi and Corte, 1997). More recent studies agreed with the inhibition issue of succinic acrid (Son et al., 2009), and not with its role every bit MLF extender.
Citric Acid
Even though citric acrid is considered as inhibitor of the malolactic enzyme (Lonvaud-Funel and Strasser de Saad, 1982), citric acid tin be catabolized by LAB (Liu, 2002). This metabolic activity is establish in some O. oeni strains equally response to acerbity or ethanol stress (Olguín et al., 2009). Due to the consumption of citric acid, diacetyl is produced (Swiegers et al., 2005). Information technology is normally desirable to accept strains which can consume citric acid due to the organoleptic complexity that is achieved (Lonvaud-Funel, 1999). In this way, a high concentration of diacetyl is reported every bit undesirable (Davis et al., 1985; Bartowsky and Henschke, 2004). Moreover, due to the citric acid metabolism, O. oeni increases the volatile acidity (Lonvaud-Funel, 1999; Liu, 2002). Even thought, citric acid increases the transmembrane gradient which generate energy in terms of proton-motive force for O. oeni (Liu Y. et al., 2016).
Anyhow, since citric acid concentration is unremarkably not very high, acetic acid does non increase very much. Citric acid production past yeast is highly species and strain dependent (Fleet, 2008). On the peak of that, mixed fermentations with different non-Saccharomyces species exhibit particular citric acid production (Jussier et al., 2006; Giaramida et al., 2013; Izquierdo Cañas et al., 2014). For the moment the only mixed fermentation that clearly increased citric acid concentration is with S. bacillaris (Giaramida et al., 2013).
Pyruvic Acid
Pyruvic acid is an intermediary produced by yeast during the AF. This chemical compound tin amend MLF performance by O. oeni. Information technology acts as external electron acceptor, facilitating the regeneration of NAD+ (Maicas et al., 2002). It tin can besides promote diacetyl product (Mink et al., 2015). Related to increasing the concentration of this compound, Belda et al. (2015) reported higher production of pyruvic acid when T. delbrueckii was used as sole or mixed civilization starter with S. cerevisiae. Benito et al. (2016) reported similar results using L. thermotolerans.
Glycerol
The production of glycerol is directly related with the activity of yeasts by the glyceropyruvic fermentation pathway (Ciani and Maccarelli, 1998). Glycerol can exist alloyed and degraded by some spoiling Lactobacillus in wine (Liu, 2002). On the opposite, there is no literature that reports this behavior when it comes to O. oeni. It is unclear how can affect glycerol to O. oeni, since it does non assimilate it, neither dethrone it. Usually, non-Saccharomyces yeasts exhibit higher metabolic activity of this pathway (Ciani and Maccarelli, 1998; Jolly et al., 2006, 2014). Specifically, T. delbrueckii (Belda et al., 2015) and C. stellata (Soden et al., 2000; Jolly et al., 2006) have been reported as big glycerol and pyruvic acid producers as result of their high glyceropyruvic fermentation action. Also, mixed fermentations with Southward. bacillaris and L. thermotolerans showroom higher production of glycerol in regards to a conventional S. cerevisiae fermentation (Benito et al., 2016; Englezos et al., 2016b).
Compounds Derived of Yeast Autolysis
One of the about known positive furnishings upon MLF performance is its development in presence of yeast lees (Guilloux-Benatier et al., 1995). It has been reported that the inhibitory interactions between yeasts and LAB is counteracted by the presence of yeast lees, and even more, the positive interactions are enlarged (Patynowski et al., 2002). During aging, yeasts undergo an autolytic procedure that result in the release of different compounds. Nitrogenated compounds, such every bit amino acids, peptides and proteins, are mainly released as event of yeast autolysis (Guilloux-Benatier et al., 1995; Martínez-Rodriguez et al., 2001). The release of such compounds tin can help to enrich the previously exhausted medium by yeasts (Costello et al., 2003), stimulating the growth of LAB and MLF performance (Guilloux-Benatier et al., 1995; Diez et al., 2010).
Other molecules like glucans and mannoproteins are as well released due to this mentioned process and tin stimulate LAB growth (Diez et al., 2010). These authors realized that the presence of mannoproteins simply exhibited its positive effect on LAB growth when ethanol was present. O. oeni can catabolize these mannoproteins and release mannose, which tin be substrate of the phosphotransferase organization that helps the adaptation of O. oeni to the medium (Jamal et al., 2013). Besides this, the touch on of the mannoproteins upon LAB was yeast-LAB strain dependent. Recently, it has been reported that some non-Saccharomyces strains belonging to M. pulcherrima and T. delbrueckii release more mannoproteins than S. cerevisiae (Belda et al., 2016). Moreover, these molecules could help hijack MCFA present in wine, stimulating LAB growth (Guilloux-Benatier et al., 1995). Information technology has been besides been reported that during AF those cited macromolecules are released, depending in the initial colloidal concentration (Guilloux-Benatier et al., 1995). Still, the same report states that the amount of macromolecules released during yeast growth is insignificant in regards to yeast autolysis.
Autonomously from the mentioned compounds, there are more released compounds during yeast autolysis, such every bit vitamins, nucleotides and long chain fatty acids, which could be also stimulatory to LAB (Alexandre et al., 2004). Unfortunately, there is no literature currently available about the possible event of these compounds.
Other Compounds
In regards to the possible incompatibility between oenological yeasts and LAB, autonomously from metabolite compounds, the production of antimicrobial proteinaceous compounds past some S. cerevisiae strains has been reported. Dick et al. (1992) firstly studied these compounds. They discovered ii cationic proteins which were effective against LAB. More recently, some other inhibitory protein fraction produced by Southward. cerevisiae CCMI 885 and active against LAB was identified (Branco et al., 2014). In this work, an exhaustive characterization was performed, which resulted in the identification of glyceraldehyde iii-phosphate dehydrogenase (GAPDH) protein fragments. This newly identified antimicrobial peptides with 2–x kDa size agreed with previously reported antimicrobial peptides (Comitini et al., 2005; Osborne and Edwards, 2007).
There are no studies well-nigh these compounds produced past not-Saccharomyces yeasts, but some species could present such antimicrobial compounds, like Thou. pulcherrima that produce pulcherrimic acid (Oro et al., 2014), active confronting other yeasts.
Futurity Perspectives
The increasing number of not-Saccharomyces species described as beneficial in winemaking demands farther investigation of their metabolism. Many factors tin can influence the event of non-Saccharomyces on wine composition. Besides the yeast species and strain characteristics, the time and the ratio of inoculation, with respect to S. cerevisiae, may modify notably the global outcome on wine of the utilize of non-Saccharomyces. All these variables may also affect the development of O. oeni and MLF. Future research should contribute to a better cognition of metabolic traits of a wider number of non-Saccharomyces strains and their influence on O. oeni performance. Amidst other possible approaches, metabolomics may be a powerful tool to elucidate how the new winemaking scenario of combined yeasts may alter MLF evolution.
Author Contributions
All authors conceived, drafted the manuscript, and approved the last version of the paper.
Funding
This work was supported by grant AGL2015-70378-R awarded by the Castilian Ministry of Economy and Competitiveness. The research leading to these results has received funding from "la Caixa" Foundation and Triptolemos Foundation. AiB was grateful to the predoctoral fellowship from the Universitat Rovira i Virgili.
Conflict of Interest Argument
The authors declare that the research was conducted in the absence of whatsoever commercial or financial relationships that could exist construed every bit a potential conflict of involvement.
Acknowledgments
JB-Thousand wished to limited thanks to the Spanish Government for his postdoctoral enquiry contract (Juan de la Cierva-incorporación).
References
Alexandre, H., Costello, P. J., Remize, F., Guzzo, J., and Guilloux-Benatier, M. (2004). Saccharomyces cerevisiae-Oenococcus oeni interactions in wine: current knowledge and perspectives. Int. J. Food Microbiol. 93, 141–154. doi: 10.1016/j.ijfoodmicro.2003.10.013
PubMed Abstract | CrossRef Full Text | Google Scholar
Arnink, Chiliad., and Henick-Kling, T. (2005). Influence of Saccharomyces cerevisiae and Oenococcus oeni strains on successful malolactic conversion in wine. Am. J. Enol. Vitic. 56, 228–237.
Google Scholar
Bartowsky, E. J., and Henschke, P. A. (2004). The "buttery" attribute of wine - Diacetyl - Desirability, spoilage and across. Int. J. Food Microbiol. 96, 235–252. doi: 10.1016/j.ijfoodmicro.2004.05.013
PubMed Abstract | CrossRef Full Text | Google Scholar
Belda, I., Navascués, E., Marquina, D., Santos, A., Calderon, F., and Benito, S. (2015). Dynamic analysis of physiological properties of Torulaspora delbrueckii in wine fermentations and its incidence on wine quality. Appl. Microbiol. Biotechnol. 99, 1911–1922. doi: 10.1007/s00253-014-6197-2
PubMed Abstract | CrossRef Full Text | Google Scholar
Belda, I., Navascués, Eastward., Marquina, D., Santos, A., Calderón, F., and Benito, S. (2016). Outlining the influence of non-conventional yeasts in wine ageing over lees. Yeast 33, 329–338. doi: 10.1002/yea.3165
PubMed Abstract | CrossRef Total Text | Google Scholar
Belda, I., Ruiz, J., Esteban-Fernández, A., Navascués, E., Marquina, D., Santos, A., et al. (2017). Microbial contribution to Vino smell and its intended utilize for Wine quality improvement. Molecules 22, 1–29. doi: 10.3390/molecules22020189
PubMed Abstract | CrossRef Total Text | Google Scholar
Beltran, Grand., Torija, M. J., Novo, Yard., Ferrer, N., Poblet, Grand., Guillamón, J. K., et al. (2002). Analysis of yeast populations during alcoholic fermentation: a half-dozen year follow-up written report. Syst. Appl. Microbiol. 25, 287–293. doi: x.1078/0723-2020-00097
PubMed Abstract | CrossRef Full Text | Google Scholar
Benito, A., Calderon, F., Palomero, F., and Benito, S. (2016). Quality and composition of Airén wines fermented by sequential inoculation of Lachancea thermotolerans and Saccharomyces cerevisiae. Food Technol. Biotechnol. 54, 135–144. doi: 10.17113/ftb.54.02.sixteen.4220
PubMed Abstract | CrossRef Full Text | Google Scholar
Benito, S., Palomero, F., Gálvez, L., Morata, A., Calderón, F., Palmero, D., et al. (2014). Quality and composition of red wine fermented with Schizosaccharomyces pombe as sole fermentative yeast, and in mixed and sequential fermentations with Saccharomyces cerevisiae. Food Technol. Biotechnol. 52, 376–382.
Google Scholar
Benito, S., Palomero, F., Morata, A., Calderón, F., Palmero, D., and Suárez-Lepe, J. A. (2013). Physiological features of Schizosaccharomyces pombe of interest in making of white wines. Eur. Food Res. Technol. 236, 29–36. doi: 10.1007/s00217-012-1836-two
CrossRef Full Text | Google Scholar
Bleve, G., Tufariello, Thou., Vetrano, C., and Mita Gand Grieco, F. (2016). Simultaneous alcoholic and malolactic fermentations by Saccharomyces cerevisiae and Oenococcus oeni cells co-immobilized in alginate beads. Front. Microbiol. 7:943. doi: 10.3389/fmicb.2016.00943
PubMed Abstract | CrossRef Full Text | Google Scholar
Branco, P., Francisco, D., Chambon, C., Hébraud, M., Arneborg, Due north., Almeida, M. G., et al. (2014). Identification of novel GAPDH-derived antimicrobial peptides secreted by Saccharomyces cerevisiae and involved in wine microbial interactions. Appl. Microbiol. Biotechnol. 98, 843–853. doi: 10.1007/s00253-013-5411-y
PubMed Abstract | CrossRef Total Text | Google Scholar
Campbell-Sills, H., El Khoury, Grand., Gammacurta, M., Miot-Sertier, C., Dutilh, L., Vestner, J., et al. (2017). Two dissimilar Oenococcus oeni lineages are associated to either red or white wines in Burgundy: genomics and metabolomics insights. OENO One 51, 309–322. doi: x.20870/oeno-one.2017.51.4.1861
CrossRef Total Text | Google Scholar
Capucho, I., and San Romao, M. V. (1994). Effect of ethanol and fatty acids on malolactic activity of Leuconostoc oenos. Appl. Microbiol. Biotechnol. 42, 391–395. doi: x.1007/BF00902747
CrossRef Full Text | Google Scholar
Caridi, A., and Corte, V. (1997). Inhibition of malolactic fermentation by cryotolerant yeasts. Biotechnol. Lett. xix, 723–726. doi: 10.1023/A:1018319705617
CrossRef Full Text | Google Scholar
Carreté, R., Vidal, M. T., Bordons, A., and Constantí, M. (2002). Inhibitory effect of sulfur dioxide and other stress compounds in wine on the ATPase activeness of Oenococcus oeni. FEMS Microbiol. Lett. 211, 155–159. doi: ten.1016/S0378-1097(02)00687-0
PubMed Abstract | CrossRef Full Text | Google Scholar
Ciani, M., and Maccarelli, F. (1998). Oenological backdrop of non-Saccharomyces yeasts associated with wine-making. World J. Microbiol. Biotechnol. 14, 199–203. doi: 10.1023/A:1008825928354
CrossRef Full Text | Google Scholar
Ciani, 1000., Morales, P., Comitini, F., Tronchoni, J., Canonico, L., Curiel, J. A., et al. (2016). Non-conventional Yeast Species for Lowering Ethanol Content of Wines. Front end. Microbiol. seven:642. doi: 10.3389/fmicb.2016.00642
PubMed Abstract | CrossRef Total Text | Google Scholar
Comitini, F., Ferretti, R., Clementi, F., Mannazzu, I., and Ciani, M. (2005). Interactions between Saccharomyces cerevisiae and malolactic leaner: preliminary characterization of a yeast proteinaceous compound(s) active against Oenococcus oeni. J. Appl. Microbiol. 99, 105–111. doi: 10.1111/j.1365-2672.2005.02579.x
PubMed Abstract | CrossRef Total Text | Google Scholar
Constantí, Thousand., Poblet, M., Arola, L., Mas, A., and Guillamón, J. M. (1997). Assay of yeast populations during alcoholic fermentation in a newly established winery. Am. J. Enol. Vitic. 48, 339–344.
Google Scholar
Contreras, A., Hidalgo, C., Henschke, P. A., Chambers, P. J., Curtin, C., and Varela, C. (2014). Evaluation of non-Saccharomyces yeasts for the reduction of alcohol content in wine. Appl. Environ. Microbiol. 80, 1670–1678. doi: 10.1128/AEM.03780-13
PubMed Abstract | CrossRef Total Text | Google Scholar
Costello, P. J., Henschke, P., and Markides, J. (2003). Standardised methodology for testing malolactic bacteria and wine yeast compatibility. Aust. J. Grape Wine Res. 9, 127–137. doi: x.1111/j.1755-0238.2003.tb00263.10
CrossRef Full Text | Google Scholar
Curiel, J. A., Morales, P., Gonzalez, R., and Tronchoni, J. (2017). Different non-Saccharomyces yeast species stimulate nutrient consumption in s. cerevisiae mixed cultures. Front. Microbiol. 8:2121. doi: ten.3389/fmicb.2017.02121
PubMed Abstract | CrossRef Full Text | Google Scholar
Davis, C. R., Wibowo, D., Eschenbruch, R., Lee, T. H., and Fleet, G. H. (1985). Practical implications of malolactic fermentation: a review. Am. J. Enol. Vitic. 36, 290–301.
Google Scholar
Dick, Chiliad. J., Molan, P. C., and Eschembruch, R. (1992). The isolation from Saccharomyces cerevisiae of two antibacterial cationic proteins that inhibit malolactic bacteria. Vitis 31, 105–116.
Google Scholar
Diez, L., Guadalupe, Z., Ayestarán, B., and Ruiz-Larrea, F. (2010). Effect of yeast mannoproteins and grape polysaccharides on the growth of wine lactic acid and acerb acrid bacteria. J. Agric. Food Chem. 58, 7731–7739. doi: 10.1021/jf100199n
PubMed Abstract | CrossRef Full Text | Google Scholar
Du Plessis, H. W., du Toit, M., Hoff, J. W., Hart, R. S., Ndimba, B. K., and Jolly, N. P. (2017). Characterisation of not- Saccharomyces yeasts using dissimilar methodologies and evaluation of their compatibility with malolactic fermentation. Southward. Afr. J. Enol. Vitic. 38, 46–63. doi: ten.21548/38-1-819
CrossRef Full Text | Google Scholar
Edwards, C. G., and Beelman, R. (1987). Inhibition of the malolactic bacterium Leuconostoc oenos (PSU-ane) by decanoic acid and subsequent removal of the inhibition past yeast ghosts. Am. J. Enol. Vitic. 38, 239–242.
Google Scholar
Englezos, V., Rantsiou, Yard., Cravero, F., Torchio, F., Ortiz-Julien, A., Gerbi, V., et al. (2016a). Starmerella bacillaris and Saccharomyces cerevisiae mixed fermentations to reduce ethanol content in vino. Appl. Microbiol. Biotechnol. 100, 5515–5526. doi: 10.1007/s00253-016-7413-z
PubMed Abstruse | CrossRef Full Text | Google Scholar
Englezos, 5., Torchio, F., Cravero, F., Marengo, F., Giacosa, S., Gerbi, V., et al. (2016b). Odour contour and composition of Barbera wines obtained by mixed fermentations of Starmerella bacillaris (synonym Candida zemplinina) and Saccharomyces cerevisiae. LWT Food Sci. Technol. 73, 567–575. doi: x.1016/j.lwt.2016.06.063
CrossRef Full Text | Google Scholar
Ferraro, L., Fatichenti, F., and Ciani, M. (2000). Pilot scale vinification process using immobilized Candida stellata cells and Saccharomyces cerevisiae. Procedure. Biochem. 35, 1125–1129. doi: x.1016/S0032-9592(00)00148-v
CrossRef Full Text | Google Scholar
Fleet, G. H., Lafon-Lafourcade, S., and Ribereau-Gayon, P. (1984). Development of yeasts and lactic acrid bacteria during fermentation and storage of Bordeaux wines. Appl. Environ. Microbiol. 48, 1034–1038.
PubMed Abstract | Google Scholar
Fourcassie, P., Belarbi, A., and Maujean, A. (1992). Growth, D-glucose utilization and malolactic fermentation by Leuconostoc śnos strains in xviii media deficient in one amino acid. J. Appl. Bacteriol. 73, 489–496. doi: ten.1111/j.1365-2672.1992.tb05010.ten
CrossRef Total Text | Google Scholar
Franquès, J., Araque, I., Palahí, East., Portillo, Grand. C., Reguant, C., and Bordons, A. (2017). Presence of Oenococcus oeni and other lactic acid leaner in grapes and wines from Priorat (Catalonia, Spain). LWT Food Sci. Technol. 81, 326–334. doi: 10.1016/j.lwt.2017.03.054
CrossRef Total Text | Google Scholar
Garvie, Due east. I. (1967). The growth factor and amino acid requirements of species of the genus Leuconostoc, including Leuconostoc paramesenteroides (sp. nov.) and Leuconostoc oenos. J. Gen. Microbiol. 48, 439–447. doi: 10.1099/00221287-48-3-439
PubMed Abstruse | CrossRef Full Text | Google Scholar
Giaramida, P., Ponticello, Grand., Di Maio, S., Squadrito, M., Genna, K., Barone, Eastward., et al. (2013). Candida zemplinina for product of wines with less alcohol and more than glycerol. S. Afr. J. Enol. Vitic. 34, 204–211.
Google Scholar
Guilloux-Benatier, M., Guerreau, J., and Feuillat, One thousand. (1995). Influence of initial colloid content on yeast macromolecule production and on the metabolism of wine microorganisms. Am. J. Enol. Vitic. 46, 486–492.
Google Scholar
González-Royo, E., Pascual, O., Kontoudakis, Due north., Esteruelas, M., Esteve-Zarzoso, B., Mas, A., et al. (2015). Oenological consequences of sequential inoculation with not-Saccharomyces yeasts (Torulaspora delbrueckii or Metschnikowia pulcherrima) and Saccharomyces cerevisiae in base of operations wine for sparkling vino production. Eur. Food Res. Technol. 240, 999–1012. doi: 10.1007/s00217-014-2404-eight
CrossRef Full Text | Google Scholar
Guilloux-Benatier, M., Le Fur, Y., and 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. doi: 10.1038/sj.jim.2900502
CrossRef Total Text | Google Scholar
Hu, Thou., Jin, G.-J., Mei, W.-C., Li, T., and Tao, Y.-S. (2018). Increase of medium-chain fatty acid ethyl ester content in mixed H. uvarum/S. cerevisiae fermentation leads to wine fruity odor enhancement. Nutrient Chem. 239, 495–501. doi: 10.1016/j.foodchem.2017.06.151
PubMed Abstract | CrossRef Full Text | Google Scholar
Izquierdo Cañas, P. One thousand. I., Romero, E. G., Pérez-Martín, F., Seseña, South., and Palop, M. L. (2014). Sequential inoculation versus co-inoculation in Cabernet Franc wine fermentation. Food Sci. Technol. Int. 21, 203–212. doi: 10.1177/1082013214524585
PubMed Abstract | CrossRef Total Text | Google Scholar
Jamal, Z., Miot-Sertier, C., Thibau, F., Dutilh, Fifty., Lonvaud-Funel, A., Ballestra, P., et al. (2013). Distribution and functions of phosphotransferase arrangement genes in the genome of the lactic acid bacterium Oenococcus oeni. Appl. Environ. Microbiol. 79, 3371–3379. doi: 10.1128/AEM.00380-xiii
PubMed Abstract | CrossRef Full Text | Google Scholar
Jolly, N., Augustyn, O., and Pretorius, I. (2006). The function and use of non-Saccharomyces yeasts in wine production. Southward. Afr. J. Enol. Vitic. 27, fifteen–38.
Google Scholar
Jolly, Northward. P., Varela, C., and Pretorius, I. S. (2014). Not your ordinary yeast: not-Saccharomyces yeasts in wine production uncovered. FEMS Yeast Res. 14, 215–237. doi: 10.1111/1567-1364.12111
PubMed Abstruse | CrossRef Full Text | Google Scholar
Jussier, D., Morneau, A. D., and Mira de Orduña, R. (2006). Result of simultaneous inoculation with yeast and leaner on fermentation kinetics and key vino parameters of cool-climate chardonnay. Appl. Environ. Microbiol. 72, 221–227. doi: 10.1128/AEM.72.one.221
PubMed Abstract | CrossRef Full Text | Google Scholar
Kim, D. H., Hong, Y. A., and Park, H. D. (2008). Co-fermentation of grape must by Issatchenkia orientalis and Saccharomyces cerevisiae reduces the malic acrid content in vino. Biotechnol. Lett. xxx, 1633–1638. doi: x.1007/s10529-008-9726-1
PubMed Abstract | CrossRef Total Text | Google Scholar
Rex, South., and Beelman, R. (1986). Metabolic interactions between Saccharomyces cerevisiae and Leuconostoc oenos in a model grape juice/wine system. Am. J. Enol. Vitic. 37, 53–60.
Google Scholar
Liu, P.-T., Lu, Fifty., Duan, C. Q., and Yan, K. 50. (2016). The contribution of ethnic not-Saccharomyces wine yeast to improved aromatic quality of Cabernet Sauvignon wines by spontaneous fermentation. LWT Food Sci. Technol. 71, 356–363. doi: ten.1016/j.lwt.2016.04.031
CrossRef Full Text | Google Scholar
Liu, Y., Forcisi, S., Harir, M., Deleris-Bou, K., Krieger-Weber, Southward., Lucio, M., et al. (2016). New molecular evidence of wine yeast-bacteria interaction unraveled by non-targeted exometabolomic profiling. Metabolomics 12, one–sixteen. doi: ten.1007/s11306-016-1001-1
CrossRef Total Text | Google Scholar
Loira, I., Vejarano, R., Bañuelos, Chiliad. A., Morata, A., Tesfaye, W., Uthurry, C., et al. (2014). Influence of sequential fermentation with Torulaspora delbrueckii and Saccharomyces cerevisiae on wine quality. LWT Nutrient Sci. Technol. 59, 915–922. doi: 10.1016/j.lwt.2014.06.019
CrossRef Full Text | Google Scholar
Lonvaud-Funel, A., Joyeux, A., and Desens, C. (1988). Inhibition of malolactic fermentation of wines by products of yeast metabolism. J. Sci. Food Agric. 44, 183–191. doi: 10.1002/jsfa.2740440209
CrossRef Full Text | Google Scholar
Lonvaud-Funel, A., and Strasser de Saad, A. Yard. (1982). Purification and properties of a malolactic enzyme from a strain of Leuconostoc mesenteroides isolated from grapes. Appl. Environ. Microbiol. 43, 357–361.
PubMed Abstract | Google Scholar
Maicas, Due south., Ferrer, Due south., and Pardo, I. (2002). NAD(P)H regeneration is the key for heterolactic fermentation of hexoses in Oenococcus oeni. Microbiology 148, 325–332. doi: x.1099/00221287-148-i-325
PubMed Abstract | CrossRef Full Text | Google Scholar
Martínez-Rodriguez, A. J., Carrascosa, A. V., and Polo, One thousand. C. (2001). Release of nitrogen compounds to the extracellular medium by three strains of Saccharomyces cerevisiae during induced autolysis in a model vino system. Int. J. Food Microbiol. 68, 155–160. doi: 10.1016/S0168-1605(01)00486-X
PubMed Abstract | CrossRef Total Text | Google Scholar
Masneuf-Pomarede, I., Juquin, E., Miot-Sertier, C., Renault, P., Laizen, Y., Salin, F., et al. (2015). The yeast Starmerella bacillaris (synonym Candida zemplinina) shows high genetic multifariousness in winemaking environments. FEMS Yeast Res. 15:fov045. doi: 10.1093/femsyr/fov045
PubMed Abstract | CrossRef Full Text | Google Scholar
Mink, R., Kölling, R., Sommer, S., Schmarr, H. Chiliad., and Scharfenberger-Schmeer, Chiliad. (2015). Diacetyl germination by Oenococcus oeni during winemaking induced by exogenous pyruvate. Am. J. Enol. Vitic. 66, 85–90. doi: x.5344/ajev.2014.14056
CrossRef Full Text | Google Scholar
Nehme, Northward., Mathieu, F., and Taillandier, P. (2008). Quantitative study of interactions between Saccharomyces cerevisiae and Oenococcus oeni strains. J. Ind. Microbiol. Biotechnol 35, 685–693. doi: x.1007/s10295-008-0328-7
PubMed Abstruse | CrossRef Total Text | Google Scholar
Olguín, N., Bordons, A., and Reguant, C. (2009). Influence of ethanol and pH on the cistron expression of the citrate pathway in Oenococcus oeni. Food Microbiol. 26, 197–203. doi: ten.1016/j.fm.2008.09.004
PubMed Abstract | CrossRef Full Text | Google Scholar
Olguín, N., Champomier-Vergès, M., Anglade, P., Baraige, F., Cordero-Otero, R., Bordons, A., et al. (2015). Transcriptomic and proteomic analysis of Oenococcus oeni PSU-1 response to ethanol shock. Food Microbiol. 51, 87–95. doi: 10.1016/j.fm.2015.05.005
PubMed Abstract | CrossRef Total Text | Google Scholar
Osborne, J. P., and Edwards, C. Thousand. (2006). Inhibition of malolactic fermentation by Saccharomyces during alcoholic fermentation nether low- and high-nitrogen conditions: a report in constructed media. Aust. J. Grape Wine Res. 12, 69–78. doi: 10.1111/j.1755-0238.2006.tb00045.x
CrossRef Total Text | Google Scholar
Osborne, J. P., and Edwards, C. One thousand. (2007). Inhibition of malolactic fermentation past a peptide produced by Saccharomyces cerevisiae during alcoholic fermentation. Int. J. Food Microbiol. 118, 27–34. doi: ten.1016/j.ijfoodmicro.2007.05.007
PubMed Abstract | CrossRef Total Text | Google Scholar
Padilla, B., Gil, J. V., and Manzanares, P. (2016). Past and hereafter of non-Saccharomyces yeasts: from spoilage microorganisms to biotechnological tools for improving vino aroma complexity. Front. Microbiol. 7:411. doi: 10.3389/fmicb.2016.00411
PubMed Abstract | CrossRef Full Text | Google Scholar
Patynowski, R. J., Jiranek, 5., and Markides, A. J. (2002). Yeast viability during fermentation and sur lie ageing of a defined medium and subsequent growth of Oenococcus oeni. Aust. J. Grape Wine Res. 8, 62–69. doi: 10.1111/j.1755-0238.2002.tb00212.x
CrossRef Full Text | Google Scholar
Petruzzi, 50., Capozzi, V., Berbegal, C., Corbo, One thousand. R., Bevilacqua, A., Spano, M., et al. (2017). Microbial resources and enological significance: opportunities and benefits. Front end. Microbiol. 8:995. doi: 10.3389/fmicb.2017.00995
PubMed Abstract | CrossRef Full Text | Google Scholar
Portillo, M. C., Franquès, J., Araque, I., Reguant, C., and Bordons, A. (2016). Bacterial variety of Grenache and Carignan grape surface from different vineyards at Priorat wine region (Catalonia, Espana). Int. J. Food Microbiol. 219, 56–63. doi: 10.1016/j.ijfoodmicro.2015.12.002
PubMed Abstruse | CrossRef Full Text | Google Scholar
Rankine, B. C. (1968). The importance of yeasts in determining the composition and quality of wines. Vitis vii, 22–49.
Google Scholar
Shekhawat, Thousand., Bauer, F. F., and Setati, M. Eastward. (2017). Bear upon of oxygenation on the operation of three not-Saccharomyces yeasts in co-fermentation with Saccharomyces cerevisiae. Appl. Microbiol. Biotechnol. 101, 2479–2491. doi: 10.1007/s00253-016-8001-y
PubMed Abstruse | CrossRef Full Text | Google Scholar
Soden, A., Fracis, I. Fifty., Oakey, H., and Henschke, P. A. (2000). Effects of co-fermentation with Candida stellata and Saccharomyces cerevisiae on the odor and limerick of Chardonnay vino. Aust. J. Grape Wine Res. vi, 21–30. doi: 10.1111/j.1755-0238.2000.tb00158.10
CrossRef Full Text | Google Scholar
Son, H. Southward., Hwang, Thou. S., Park, Westward. G., Hong, Y. Due south., and Lee, C. H. (2009). Metabolomic characterization of malolactic fermentation and fermentative behaviors of vino yeasts in grape vino. J. Agric. Nutrient Chem. 57, 4801–4809. doi: x.1021/jf9005017
PubMed Abstract | CrossRef Full Text | Google Scholar
Su, J., Wang, T., Wang, Y., Li, Y. Y., and Li, H. (2014). The utilize of lactic acid-producing, malic acrid-producing, ormalic acid-degrading yeast strains for acidity adjustment in the wine manufacture. Appl. Microbiol. Biotechnol. 98, 2395–2413. doi: 10.1007/s00253-014-5508-y
PubMed Abstract | CrossRef Full Text | Google Scholar
Sumby, K. Thousand., Grbin, P. R., and Jiranek, V. (2014). Implications of new research and technologies for malolactic fermentation in vino. Appl. Microbiol. Biotechnol. 98, 8111–8132. doi: 10.1007/s00253-014-5976-0
PubMed Abstract | CrossRef Total Text | Google Scholar
Suzzi, G., Romano, P., and Zambonelli, C. (1985). Saccharomyces strain choice in minimizing SO2 requirements during fermentation. Am. J. Enol. Vitic. 36, 199–202.
Google Scholar
Swiegers, J. H., Bartowsky, E. J., Henschke, P. A., and Pretorius, I. S. (2005). Yeast and bacterial modulation of wine odour and flavour. Aust. J. Grape Wine Res. 11, 139–173. doi: x.1111/j.1755-0238.2005.tb00285.10
CrossRef Full Text | Google Scholar
Terrade, North., and Mira de Orduña, R. (2009). Conclusion of the essential food requirements of vino-related bacteria from the genera Oenococcus and Lactobacillus. Int. J. Food Microbiol. 133, 8–xiii. doi: x.1016/j.ijfoodmicro.2009.03.020
PubMed Abstract | CrossRef Total Text | Google Scholar
Tofalo, R., Schirone, M., Torriani, S., Rantsiou, Chiliad., Cocolin, Fifty., Perpetuini, G., et al. (2012). Variety of Candida zemplinina strains from grapes and Italian wines. Food Microbiol. 29, 18–26. doi: 10.1016/j.fm.2011.08.014
PubMed Abstract | CrossRef Full Text | Google Scholar
Tristezza, M., di Feo, L., Tufariello, M., Grieco, F., Capozzi, Five., Spano, 1000., et al. (2016). Simultaneous inoculation of yeasts and lactic acrid leaner: effects on fermentation dynamics and chemical composition of Negroamaro vino. LWT Food Sci. Technol. 66, 406–412. doi: 10.1016/j.lwt.2015.10.064
CrossRef Total Text | Google Scholar
Wells, A., and Osborne, J. P. (2011). Production of SO2 and SO2 binding compounds by Saccharomyces cerevisiae during the alcoholic fermentation and the impact on wine lactic acid bacteria. Due south. Afr. J. Enol. Vitic. 32, 267–279.
Google Scholar
Wibowo, D., Eschenbruch, R., Davis, C., Fleet, G., and Lee, T. (1985). Occurrence and growth of lactic acid leaner in wine: a review. Am. J. Enol. Vitic. 36, 302–313.
Google Scholar
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