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Enzymatic activities produced by mixed Saccharomyces and non-Saccharomyces cultures: relationship with wine volatile composition

Abstract

During certain wine fermentation processes, yeasts, and mainly non-Saccharomyces strains, produce and secrete enzymes such as β-glucosidases, proteases, pectinases, xylanases and amylases. The effects of enzyme activity on the aromatic quality of wines during grape juice fermentation, using different co-inoculation strategies of non-Saccharomyces and Saccharomyces cerevisiae yeasts, were assessed in the current study. Three strains with appropriate enological performance and high enzymatic activities, BSc562 (S. cerevisiae), BDv566 (Debaryomyces vanrijiae) and BCs403 (Candida sake), were assayed in pure and mixed Saccharomyces/non-Saccharomyces cultures. β-Glucosidase, pectinase, protease, xylanase and amylase activities were quantified during fermentations. The aromatic profile of pure and mixed cultures was determined at the end of each fermentation. In mixed cultures, non-Saccharomyces species were detected until day 4–5 of the fermentation process, and highest populations were observed in MSD2 (10 % S. cerevisiae/90 % D. vanrijiae) and MSC1 (1 % S. cerevisiae/99 % C. sake). According to correlation and multivariate analysis, MSD2 presented the highest concentrations of terpenes and higher alcohols which were associated with pectinase, amylase and xylanase activities. On the other hand, MSC1 high levels of β-glucosidase, proteolytic and xylanolytic activities were correlated to esters and fatty acids. Our study contributes to a better understanding of the effect of enzymatic activities by yeasts on compound transformations that occur during wine fermentation.

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References

  • Andorrà I, Berradre M, Rozès N, Mas A, Guillamón JM, Esteve-Zarzoso B (2010) Effect of pure and mixed cultures of the main wine yeast species on grape must fermentations. Eur Food Res Technol 231:215–224

    Article  Google Scholar 

  • Anfang N, Brajkovich M, Goddard MR (2009) Co-fermentation with Pichia kluyveri increases varietal thiol concentrations in Sauvignon Blanc. Aus J Grape Wine Res 15:1–8

    CAS  Article  Google Scholar 

  • Baroni MV, Nores ML, Díaz MDP, Chiabrand GA, Fassano JP, Costa C, Wunderlin DA (2006) Determination of volatile organic compound patterns characteristic of five unifloral honey by solid-phase microextraction–gas chromatography–mass spectrometry coupled to chemometrics. J Agric Food Chem 54:7235–7241

    CAS  Article  PubMed  Google Scholar 

  • Bely M, Stoeckle P, Masneuf-Pomarède I, Dubourdieu D (2008) Impact of mixed Torulaspora delbrueckiiSaccharomyces cerevisiae culture on high-sugar fermentation. Int J Food Microbiol 122:312–320

    CAS  Article  PubMed  Google Scholar 

  • Bertrand A (1981) Formation des Substances Volatiles au Cours de la Fermentation alcoolique. Incidence sur la Qualité du vin. Colloque Soc. Fr. Microbiol, Reims, pp 251–267

    Google Scholar 

  • Bisson LF, Karpel JE (2010) Genetics of yeast impacting wine quality. Ann Rev Food Sci Technol 1:139–162

    CAS  Article  Google Scholar 

  • Blasco L, Veiga-Crespo P, Poza M, Villa TG (2006) Hydrolases as markers of wine aging. Word J Microbiol Biotechnol 22:1229–1233

    CAS  Article  Google Scholar 

  • Botelho G, Paulino C, Mendes-Faia A, Clímaco MC (2007) A method to analyse bound aroma compounds in non-aromatic red grape juices. Ciência Técnica Vitivinicola 22:21–26

    Google Scholar 

  • Carballeira Lois L, Cortés Diéguez S, Gil de la Peña ML, Fernández Gómez E (2001) SPE-GC determination of aromatic compounds in two varieties of white grape during ripening. Chromatographia 53:350–355

    Article  Google Scholar 

  • Charoenchai C, Flee GH, Henschke PA, Todd BEN (1997) Screening of non-Saccharomyces yeasts for the presence of extracellular hydrolytic enzymes. Aus J Grape Wine Res 3:2–8

    CAS  Article  Google Scholar 

  • Ciani M, Beco L, Comitini F (2006) Fermentation behaviour and metabolic interactions of multistarter wine yeast fermentations. Int J Food Microbiol 108:239–245

    CAS  Article  PubMed  Google Scholar 

  • Comitini F, Gobbi M, Domizio P, Romani C, Lencioni L, Mannazzu I, Ciani M (2011) Selected non-Saccharomyces wine yeasts in controlled multistarter fermentations with Saccharomyces cerevisiae. Food Microbiol 28:873–882

    CAS  Article  PubMed  Google Scholar 

  • Di Paola-Naranjo RD, Baroni MV, Podio NS, Rubinstein HR, Fabani MP, Badini RG, Inga M, Ostera HA, Cagnoni M, Gallego E, Peral-García P, Hoogewerff J, Wunderlin DA (2011) Fingerprints for main varieties of Argentinean wines: terroir differentiation by inorganic, organic and stable isotopic analyses coupled to Chemometrics. J Agric Food Chem 59:7854–7865

    Article  PubMed  Google Scholar 

  • Díaz AB, Caro I, de Ory I, Blandino A (2007) Evaluation of the conditions for the extraction of hydrolitic enzymes obtained by solid state fermentation from grape pomace. Enzym Microb Technol 41:302–306

    Article  Google Scholar 

  • Douaiher MN, Nowak E, Dumortier V, Durand R, Reignault Ph, Halama P (2007) Mycosphaerella graminicola produces a range of cell wall-degrading enzyme activities in vitro that vary with the carbon source. Eur J Plant Pathol 117:71–79

    CAS  Article  Google Scholar 

  • Esteve-Zarzoso B, Belloch C, Uruburu F, Querol A (1999) Identification of yeasts by RFLP analysis of the 5.8 rRNA gene and the two ribosomal internal transcribed spacers. Int J Syst Bacteriol 49:329–337

    CAS  Article  PubMed  Google Scholar 

  • Fia G, Giovani G, Rosi I (2005) Study of β-glucosidase production by wine-related yeasts during alcoholic fermentation. A new rapid fluorimetric method to determine enzymatic activity. J Appl Microbiol 99:509–517

    CAS  Article  PubMed  Google Scholar 

  • Ganga MA, Piñaga F, Vallés S, Ramón D, Querol A (1999) Aroma improving in microvinification processes by the use of a recombinant wine yeast strain expressing the Aspergillus nidulans xlnA gene. Int J Food Microbiol 47:171–178

    CAS  Article  PubMed  Google Scholar 

  • Ganga MA, Pinaga F, Valles S, Ramón D, Querol A (2001) Cell wall-degrading enzymes in the release of grape aroma precursors. Food Sci Technol Int 7:83–87

    CAS  Article  Google Scholar 

  • Gil GF, Pszczòlkowski P (2007) La vid. In: Universidad Católica de Chile (ed) VITICULTURA fundamentos para optimizar producción y calidad. Universidad Catolica de Chile, Santiago, pp 26–75

    Google Scholar 

  • Gil JV, Mateo JJ, Jiménez M, Pastor A, Huerta T (1996) Aroma compounds in wine as influenced by apiculate yeasts. J Food Sci 61:1247–1249

    CAS  Article  Google Scholar 

  • Hernández-Orte P, Cersosimo M, Loscos N, Cacho J, Garcia-Moruno E, Ferreira V (2008) The development of varietal aroma from non-floral grapes by yeast of different genera. Food Chem 107:1064–1077

    Article  Google Scholar 

  • Jolly N, Augustyn OPH, Pretoius IS (2003) The effect on non- Saccharomyces yeasts on fermentation and wine quality. S Afr J Enol Vitic 24:55–62

    CAS  Google Scholar 

  • Jolly NP, Augustyn OPH, Pretorius IS (2006) The role and use of non- Saccharomyces yeasts in wine production. S Afr J Enol Vitic 27:15–39

    CAS  Google Scholar 

  • Kang W, Xu Y, Qin L, Wang Y (2010) Effects of different β-d-glycosidases on bound aroma compounds in muscat grape determined by HS-SPME and GC-MS. J Inst Brew 116:70–77

    CAS  Article  Google Scholar 

  • Kurtzman CP, Fell JW (1998) The yeasts, a taxonomic study, 4th edn. Elsevier Science B.V, Amsterdam

    Google Scholar 

  • Lee PR, Hui S, Kho C, Yu B, Curran P, Liu SQ (2012) Yeast ratio is a critical factor for sequential fermentation of papaya wine by Williopsis saturnus and Saccharomyces cerevisiae. Microbial Biotechnol 6:385–393

    Article  Google Scholar 

  • Louw C, La Grange D, Pretorius IS, van Rensburg P (2006) The effect of polysaccharide-degrading wine yeast transformants on the efficiency of wine processing and wine flavour. J Biotechnol 125:447–461

    CAS  Article  PubMed  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 

  • Maturano YP, Rodríguez L, Toro ME, Vazquez F, de Figueroa LIC (2008) Screening of β-glucosidase activity in wine yeasts isolated from Cuyo viticulture region of Argentina. 12th international congress on yeasts (ICY-2008), Kiev, Ukraine

  • Maturano YP, Nally MC, Toro ME, Castellanos de Figueroa L, Vazquez F (2009a) Estudio cualitativo de actividades enzimáticas y fenómeno killer en levaduras vínicas. Revista de Enología 1:1–11

    Google Scholar 

  • Maturano YP, Toro ME, Castellanos de Figueroa L, Vazquez F (2009b) Determinación de actividades celulolítica y xilanolítica en levaduras no–Saccharomyces de origen enológico. Revista de Enología 2:1–9

    Google Scholar 

  • Maturano YP, Rodríguez Assaf LA, Toro ME, Nally MC, Vallejo M, Castellanos de Figueroa L, Combina M, Vazquez F (2012) Multi-enzyme production by pure and mixed cultures of Saccharomyces and non-Saccharomyces yeasts during wine fermentation. Int J Food Microbiol 155:43–50

    CAS  Article  PubMed  Google Scholar 

  • Mendes-Pinto MM (2009) Carotenoid breakdown products the norisoprenoids in wine aroma. Arch Biochem Biophys 48:236–245

    Article  Google Scholar 

  • Miller GL (1959) Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal Chem 31:426–428

    CAS  Article  Google Scholar 

  • Moreira N, Mendes F, Guedes de Pinho P, Hogg T, Vascancelos I (2008) Heavy sulphur compounds, higher alcohols and esters production profile of Hanseniaspora uvarum and Hanseniaspora guilliermondii grown as pure and mixed cultures in grape must. Int J Food Microbiol 124:231–238

    CAS  Article  PubMed  Google Scholar 

  • Moreno JJ, Millán C, Ortega JM, Medina M (1991) Analytical differentiation of wine fermentations using pure and mixed yeast cultures. J Ind Microbiol 7:181–189

    CAS  Article  Google Scholar 

  • Oliveira KF, Malavolta L, Souza CS, Vicente EJ, Laluce C (2006) Pectinolytic activity secreted by yeasts isolated from fermented citrus molasses. J Appl Microbiol 100:633–640

    CAS  Article  PubMed  Google Scholar 

  • Oliveira JM, Oliveira P, Baumes RL, Maia MO (2008) Volatile and glycosidically bound composition of Loureiro and Alvarinho wines. Food Sci Technol Int 14:341–353

    CAS  Article  Google Scholar 

  • Penci C, Martinez M, Fabani MP, Tapia A, Feresin GE, Wunderlin DA (2012) Matching changes in sensory evaluation with physical and chemical parameters. A case study: Argentinean pistachio nuts (Pistachia vera L. cv Kerman). Food Bioprocess Technol. doi:10.1007/s11947-012-0993-4

    Google Scholar 

  • Perestrelo R, Fernandes A, Albuquerque FF, Marques JC, Câmara JS (2006) Analytical characterization of the aroma of Tinta Negra Mole red wine: identification of the main odorants compounds. Anal Chem Acta 563(1):154–164

    CAS  Article  Google Scholar 

  • Povhe Jemec K, Raspor P (2005) Initial Saccharomyces cerevisiae concentration in single or composite cultures dictates bioprocess kinetics. Food Microbiol 22:293–300

    CAS  Article  Google Scholar 

  • Sadoudi M, Tourdot-Maréchal R, Rousseaux S, Steyer D, Gallardo-Chacón JJ, Ballester J, Vichi S, Guérin-Schneider R, Caixach J, Alexandre H (2012) Yeast-yeast interactions revealed by aromatic profile analysis of Sauvignon Blanc wine fermented by single or co-culture of non-Saccharomyces and Saccharomyces yeasts. Food Microbiol 32:243–253

    CAS  Article  PubMed  Google Scholar 

  • Sánchez Palomo E, Díaz-Maroto MC, González Viñas MA, Soriano-Pérez A, Pérez-Coello MS (2007) Aroma profile of wines from Albillo and Muscat grape varieties at different stages of ripening. Food Control 18:398–403

    Article  Google Scholar 

  • Strauss M, Jolly N, Lambrechts M, van Rensburg P (2001) Screening for the production of extracellular hydrolytic enzymes by non-Saccharomyces wine yeasts. J Appl Microbiol 91:182–190

    CAS  Article  PubMed  Google Scholar 

  • Sun SY, Gong HS, Jiang XM, Zhao YP (2014) Selected non- Saccharomyces wine yeasts in controlled multistarter fermentations with Saccharomyces cerevisiae on alcoholic fermentation behaviour and wine aroma of cherry wines. Food Microbiol 44:15–23

    CAS  Article  PubMed  Google Scholar 

  • Toro ME, Vazquez F (2002) Fermentation behaviour of controlled mixed and sequential cultures of Candida cantarellii and Saccharomyces cerevisiae wine yeasts. World J Microbiol Biotechnol 18:347–354

    CAS  Google Scholar 

  • Zamuz S, Sestelo ABF, Poza M, Villa TG (2004) Enzymes as potential markers of wine aging. J Inst Brew 110:220–226

    CAS  Article  Google Scholar 

  • Zohre DE, Erten H (2002) The influence of Kloeckera apiculata and Candida pulcherrima yeasts on wine fermentation. Process Biochem 38:319–324

    CAS  Article  Google Scholar 

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Acknowledgments

The authors wish to thank CICITCA-UNSJ and PAE-PICT-2007-02359 for financial support of this work.

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Correspondence to Yolanda Paola Maturano.

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Maturano, Y.P., Assof, M., Fabani, M.P. et al. Enzymatic activities produced by mixed Saccharomyces and non-Saccharomyces cultures: relationship with wine volatile composition. Antonie van Leeuwenhoek 108, 1239–1256 (2015). https://doi.org/10.1007/s10482-015-0578-0

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  • DOI: https://doi.org/10.1007/s10482-015-0578-0

Keywords

  • Mixed cultures
  • Enzymatic activities
  • Non-Saccharomyces yeasts
  • Aromatic profile of wines