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Influence of glycosides on behavior of Oenococcus oeni in wine conditions: growth, substrates and aroma compounds

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Abstract

Autochthonous Oenococcus oeni strains (MS9, MS20 and MS46) with good malolactic performance and yielding adequate diacetyl levels, were selected to investigate the effect of synthetic and grape glycosides on bacterial growth, substrate utilization and β-glucosidase (βGlu), α-arabinofuranosidase (αAra) and α-rhamnopyranosidase (αRha) activities in a wine-like medium containing 6% ethanol, pH 4.0 (WBM). Then, changes in the volatile compounds profile were evaluated at the end of malolactic fermentation (MLF) carried out by the MS46 strain in WBM containing 1 mg L−1 of natural glycoside. All strains grew and efficiently degraded l-malic acid in WBM where βGlu and αAra activities were found but not αRha. In presence of a synthetic glycoside (eriodictyol 7-O-β-rutinoside) βGlu activity was significantly enhanced for two of the cultures tested (MS20 and MS460) while a low αRha activity was induced, presenting MS46 the better performance. Glycosides extracted from fermented grape musts under different conditions allowed maximum growths, l-malic acid utilization rates and glycosidase activities in the MS46 strain. Thus, βGlu, αAra and αRha activities increased between 30–50 and 3–11% respectively. This indirectly correlated to significant changes in total esters and higher alcohols at the end of MLF, which increased by up to 140 and 30% respectively. Moreover, ethyl and acetate esters formed up to 100-fold than alcohols or esters degraded highlighted the main role of this microorganism in the esters synthesis. Results obtained encourage the potential use of selected indigenous O. oeni strains as a tool to enhance wine complexity through MLF, mainly on highly fruity aroma.

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References

  • Amoroso MJ, Saguir FM, Manca de Nadra MC (1993) Variation of nutritional requirements of Leuconostoc oenos by organic acids. J Int Sci Vigne Vin 27:135–144

    Google Scholar 

  • Barbagallo R, Spagna G, Palmeri R, Torriani S (2004) Assessment of β-glucosidase activity in selected wild strains of Oenococcus oeni for malolactic fermentation. Enzyme Microb Technol 34:292–296

    Article  CAS  Google Scholar 

  • Bartowsky EJ, Costello PJ, Henschke PA (2002) Management of malolactic fermentation-wine flavour manipulation. Aust N Z Grapegrow Winemak 461:7–12

    Google Scholar 

  • Bloem A, Lonvaud-Funel A, de Revel G (2008) Hydrolysis of glycosidically bound flavor compounds from oak wood by Oenococcus oeni. Food Microbiol 25:99–104

    Article  CAS  Google Scholar 

  • Boido E, Lloret A, Medina K, Carrai 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

    Article  CAS  Google Scholar 

  • Bravo-Ferrada BM, Delfederico L, Hollmann A, La Valdés Hens D, Curilén Y, Caballero A, Semorile L (2011) Oenococcus oeni from Patagonian red wines: isolation, characterization and technological properties. Int J Microbiol Res 3:48–55

    Article  Google Scholar 

  • Campbell-Sills H, Capozzi V, Romano A, Cappellin L, Breniaux M, Lucas P, Biasioli F (2016) Advances in wine analysis by PTR-ToF-MS: optimization of the method and discrimination of wines from different geographical origins and fermented with different malolactic starters. Int J Mass Spectrom 397–398:42–51

    Article  Google Scholar 

  • 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. Appl Microbiol 114:797–806

    Article  CAS  Google Scholar 

  • De Man JC, Rogosa M, Sharpe MR (1960) A medium for the cultivation of lactobacilli. J Appl Bacteriol 23:130–135

    Article  Google Scholar 

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

    Article  Google Scholar 

  • da Silveira MG, Golovina EA, Hoekstra FA, Rombouts FM, Abee T (2003) Membrane fluidity adjustments in ethanol-stressed Oenococcus oeni cells. Appl Environ Microbiol 69:5826–5832

    Article  Google Scholar 

  • Davis CR, Wibowo D, Eschenbruch R, Lee TH, Fleet GH (1985) Practical implications of malolactic fermentation: a review. Am J Enol Vitic 36:290–301

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Gagné S, Lucas PM, Perello MC, Claisse O, Lonvaud-Funel A, de Revel G (2011) Variety and variability of glycosidase activities in an Oenococcus oeni strain collection tested with synthetic and natural substrates. J Appl Microbiol 110:218–228

    Article  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 51:362–369

    CAS  Google Scholar 

  • Grimaldi A, Bartowsky E, Jiranek V (2005a) Screening of Lactobacillus spp. and Pediococcus spp. for glycosidase activities that are important in oenology. J Appl Microbiol 99:1061–1069

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Gruninger RJ, Gong X, Forster RJ, McAllister TA (2014) Biochemical and kinetic characterization of the multifunctional β-glucosidase/β-xylosidase/α-arabinosidase, Bgxa1. Appl Microbiol Biotechnol 98:3003–3012

    Article  CAS  Google Scholar 

  • Guilloux-Benatier M, Guerreau J, Feuillat M (1995) Influence of initial colloid content on yeast macromolecule production and on the metabolism of wine microorganisms. Am J Enol Vitic 46:486–492

    CAS  Google Scholar 

  • Günata ZY, Bitteur S, Brillouet JM, Voirin S, Baumes R, Cordonnier RE (1988) Sequential enzymatic hydrolysis of potentially aromatic glycosides from grapes. Carbohydr Res 184:139–149

    Article  Google Scholar 

  • Hernandez-Orte P, Cersosimo M, Loscos N, Cacho J, Garcia-Moruno E, Ferreira V (2009) Aroma development from non-floral grape precursors by wine lactic acid bacteria. Food Res Int 42:773–781

    Article  CAS  Google Scholar 

  • Izquierdo PM, García E, Martínez J, Chacón JL (2004) Selection of lactic bacteria to induce malolactic fermentation in red wine of cv. Cencibel. VITIS 43:149–153

    Google Scholar 

  • Izquierdo Cañas PM, García Romero E, Gómez Alonso S, Palop Herreros ML (2008) Changes in the aromatic composition of Tempranillo wines during spontaneous malolactic fermentation. J Food Compos Anal 21:724–730

    Article  Google Scholar 

  • Lambrechts MG, Pretorius IS (2000) Yeast and its importance to wine aroma—a review. S Afr J Enol Vitic 21:97–129

    CAS  Google Scholar 

  • Liu S (2002) A review: malolactic fermentation in wine—beyond deacidification. J Appl Microbiol 92:589–601

    Article  CAS  Google Scholar 

  • Lombardi SJ, Tremonte P, Succi M, Testa B, Pannella G, Tipaldi L, Sorrentino E, Coppola R, Iorizzo M (2012) Effect of phenolic compounds on the growth and l-malic acid metabolism of Oenococcus oeni. J Life Sci 6:1225–1231

    CAS  Google Scholar 

  • Lu Y, Chua J, Huang D, Lee P, Liu S (2016) Biotransformation of chemical constituents of durian wine with simultaneous alcoholic fermentation by Torulaspora delbrueckii. Appl Microbiol Biotechnol 100:8877–8888

    Article  CAS  Google Scholar 

  • Maicas S, Gil JV, Pardo I, Ferrer S (1999) Improvement of volatile composition of wines by controlled addition of malolactic bacteria. Food Res Int 32:491–496

    Article  CAS  Google Scholar 

  • Mansfield AK, Zoecklein BW, Whiton RS (2002) Quantification of glycoside activity in selected strains of Brettanomyces bruxellensis and Oenococcus oeni. Am J Enol Vitic 53:303–307

    CAS  Google Scholar 

  • Massera A, Assof M, Sturm ME, Sari S, Jofré V, Cordero-Otero R, Combina M (2012) Selection of indigenous Saccharomyces cerevisiae strains to ferment red musts at low temperature. Ann Microbiol 62:367–380

    Article  Google Scholar 

  • Matthews A, Grbin P, Jiranek V (2006) A survey of lactic acid bacteria for enzymes of interest to oenology. Aust J Grape Wine Res 12:235–244

    Article  CAS  Google Scholar 

  • Matthews A, Grbin P, Jiranek V (2007) Biochemical characterisation of the esterase activities of wine lactic acid bacteria. Appl Microbiol Biotechnol 77:329–337

    Article  CAS  Google Scholar 

  • Maturano YP, Assof M, Fabani MP, Nally MC, Jofré V, Rodriguez Assaf LA, Toro ME, Castellanos de Figueroa LI, Vazquez F (2015) Enzymatic activities produced by mixed Saccharomyces and non-Saccharomyces cultures: relationship with wine volatile composition. Anton Leeuw Int J G 108:1239–1256

    Article  CAS  Google Scholar 

  • Maturano C, Rivero LV, Rodríguez Vaquero MJ, Saguir FM (2016) The effect of organic acids and sulfur dioxide on C4 compound production and β-glucosidase activity of Oenococcus oeni from wines under acidic conditions. Int J Wine Res 8:1–10

    Article  Google Scholar 

  • McMahon H, Zoecklein BW, Fugelsang K, Jasinsky Y (1999) Quantification of glycosidase activities in selected yeasts and lactic acid bacteria. J Ind Microbiol Biotechnol 23:198–203

    Article  CAS  Google Scholar 

  • Mendoza LM, Manca de Nadra MC, Farías MF (2007) Kinetics and metabolic behavior of a composite culture of Kloeckera apiculata and Saccharomyces cerevisiae wine related strains. Biotechnol Lett 29:1057–1063

    Article  CAS  Google Scholar 

  • Miyake Y, Yamamoto K, Osawa T (1997) Isolation of eriocitrin (eriodictiol 7-rutinoside) from lemon fruit (Citrus lemon BURM. f.) and its antioxidative activity. Food Sci Technol Int 3:84–89

    Article  CAS  Google Scholar 

  • 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 28:1443–1449

    Article  CAS  Google Scholar 

  • Orrillo AG, Ledesma P, Delgado OD, Spagna G, Breccia JD (2007) Cold-active α-l-rhamnosidase from psychrotolerant bacteria isolated from a sub-Antarctic ecosystem. Enzyme Microb Technol 40:236–241

    Article  CAS  Google Scholar 

  • Palmeri R, Spagna G (2007) β-Glucosidase in cellular and acellular form for winemaking application. Enzyme Microb Technol 40:382–389

    Article  CAS  Google Scholar 

  • Pérez-Martín F, Seseña S, Izquierdo PM, Palop ML (2013) Esterase activity of lactic acid bacteria isolated from malolactic fermentation of red wines. Int J Food Microbiol 163:153–158

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Reguant C, Bordons A, Arola L, Rozés N (2000) Influence of phenolic compounds on the physiology of Oenococcus oeni from wine. J Appl Microbiol 88:1065–1071

    Article  CAS  Google Scholar 

  • Saguir FM, Manca de Nadra MC (1996) Organic acids metabolism under different glucose concentrations of Leuconostoc oenos from wine. J Appl Bacteriol 81:393–397

    CAS  Google Scholar 

  • Saguir FM, Manca de Nadra MC (2002) Effect of l-malic and citric acids metabolism on the essential amino acid requirements for Oenococcus oeni growth. J Appl Microbiol 93:295–301

    Article  CAS  Google Scholar 

  • Saguir FM, Loto Campos IE, Manca de Nadra MC (2008) Utilization of amino acids and dipeptides by Lactobacillus plantarum from orange in nutritionally stressed conditions. J Appl Microbiol 104:1597–1604

    Article  CAS  Google Scholar 

  • Saguir FM, Loto Campos I, Maturano C, Manca de Nadra MC (2009) Identification of dominant lactic acid bacteria isolated from grape juices. Assessment of its biochemical activities, relevant to flavor development in wine. Int J Wine Res 1:175–185

    CAS  Google Scholar 

  • Sarry JM, Günata Z (2004) Plant and microbial glycoside hydrolases: volatile release from glycosidic aroma precursors. Food Chem 87:509–521

    Article  CAS  Google Scholar 

  • Schwab W, Scheller G, Schreier P (1990) Glycosidically bound aroma components from sour cherry. Phytochemistry 29:607–612

    Article  CAS  Google Scholar 

  • Segurel MA, Baumes RL, Riou C, Razungles AJ (2009) Role of glycosidic aroma precursors on the odorant profiles of Grenache noir and Syrah wines from the Rhone valley. Part 1: sensory study. J Int Sci Vigne Vin 43:199–211

    CAS  Google Scholar 

  • Spano G, Massa S (2006) Environmental stress response in wine lactic acid bacteria: beyond Bacillus subtilis. Crit Rev Microbiol 32:77–86

    Article  CAS  Google Scholar 

  • Sumby KM, Matthews AH, Grbin PR, Jiranek V (2009) Cloning and characterization of an intracellular esterase from the wine-associated lactic acid bacterium Oenococcus oeni. Appl Environ Microbiol 75:6729–6735

    Article  CAS  Google Scholar 

  • Sumby KM, Grbin PR, Jiranek V (2010) Microbial modulation of aromatic esters in wine: current knowledge and future prospects. Food Chem 121:1–16

    Article  CAS  Google Scholar 

  • Tristezza M, di Feo L, Tufariello M, Grieco F, Capozzi V, Spano G, Mita G, Grieco F (2016) Simultaneous inoculation of yeast and lactic acid bacteria: effects on fermentation dynamics and chemical composition of Negroamaro wine. LWT Food Sci Technol 66:406–412.

    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 53:10134–10139

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Voirin SG, Baumes RL, Sapis JC, Bayonove CL (1992) Analytical methods for monoterpene glycosides in grape and wine. Part 2: qualitative and quantitative determination of glycosides in grape. J Chromatogr 595:269–281

    Article  CAS  Google Scholar 

  • Williams P, Cynkar W, Francis I, Gray J, Iland P, Coombe B (1995) Quantification of glycosides in grapes, juices, and wines through a determination of glycosyl glucose. J Agric Food Chem 43:121–128

    Article  CAS  Google Scholar 

  • Yang Y, Zhang X, Yin Q, Fang W, Fang Z, Wang X, Xiao Y (2015) A mechanism of glucose tolerance and stimulation of GH1 β-glucosidases. Sci Rep 5:17296

    Article  CAS  Google Scholar 

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Acknowledgements

The authors are appreciative of Dr. Viviana Jofré (Laboratorio de Aromas y Sustancias Naturales, Estación Experimental Agropecuaria Mendoza, INTA) and Dr Silvana del Mónaco (Ingeniería de Procesos, Biotecnología y Energías Alternativas, PROBIEN) for technical assistance and comments during the preparation of this manuscript. This work was supported by grants from Consejo Nacional de Investigaciones Científicas y Técnicas (PIP-CONICET) and Consejo de Investigaciones de la Universidad Nacional de Tucumán (PIUNT). Carmen Maturano is postdoctoral fellow and Fabiana María Saguir is investigator in CONICET, Argentina.

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Correspondence to Fabiana María Saguir.

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Maturano, C., Saguir, F.M. Influence of glycosides on behavior of Oenococcus oeni in wine conditions: growth, substrates and aroma compounds. World J Microbiol Biotechnol 33, 151 (2017). https://doi.org/10.1007/s11274-017-2316-4

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  • DOI: https://doi.org/10.1007/s11274-017-2316-4

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