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Mixed culture fermentation using Torulaspora delbrueckii and Saccharomyces cerevisiae with direct and indirect contact: impact of anaerobic growth factors

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Abstract

The role of the initial concentration of anaerobic growth factors (AGF) on interactions between Torulaspora delbrueckii and Saccharomyces cerevisiae was investigated in strict anaerobiosis. Experiments were performed in a synthetic grape must medium in a membrane bioreactor, a special tool designed for studying direct and indirect interactions between microorganisms. In pure culture fermentations, increased AGF concentration had no impact on S. cerevisiae behaviour, whereas it induced an extension of T. delbrueckii latency. Surprisingly, T. delbrueckii used only 75 to 80% of the consumed sugar to produce biomass, glycerol and ethanol. Physical separation influenced the population dynamics of co-fermentations. S.cerevisiae dominated the co-cultures having a single dose of AGF as its presence indirectly induced a decrease in numbers of living T. delbrueckii cells and physical contact with T. delbrueckii stimulated S.cerevisiae growth. Increasing the AGF initial concentration completely upset this domination: S. cerevisiae growth was not stimulated and T. delbrueckii living cells did not decrease. Yeasts incorporate exogenous AGFs, which probably impact their response to competing yeasts. The increase in AGF might have induced changes in the lipid composition of the T. delbrueckii membrane, which would hinder its interaction with S. cerevisiae antimicrobial peptides. The initial concentration of anaerobic growth factors influenced co-culture fermentation population dynamics tremendously, thus highlighting a new way to monitor population evolution and eventually wine organoleptic properties.

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References

  1. Pretorius IS (2000) Tailoring wine yeast for the new millennium: novel approaches to the ancient art of winemaking. Yeast 16:675–729

    Article  CAS  PubMed  Google Scholar 

  2. Ciani M, Comitini F, Mannazzu I, Domizio P (2010) Controlled mixed culture fermentation: a new perspective on the use of non-Saccharomyces yeasts in winemaking. FEMS Yeast Res 10:123–133

    Article  CAS  PubMed  Google Scholar 

  3. 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

    Article  CAS  PubMed  Google Scholar 

  4. Taillandier P, Lai QP, Julien-Ortiz A, Brandam C (2014) Interactions between Torulaspora delbrueckii and Saccharomyces cerevisiae in wine fermentation: influence of inoculation and nitrogen content. World J Microbiol Biotechnol 30:1959–1967

    Article  CAS  PubMed  Google Scholar 

  5. Contreras A, Curtin C, Varela C (2015) Yeast population dynamics reveal a potential ‘collaboration’ between Metschnikowia pulcherrima and Saccharomyces uvarum for the production of reduced alcohol wines during Shiraz fermentation. Appl Microbiol Biotechnol 99:1885–1895

    Article  CAS  PubMed  Google Scholar 

  6. Ciani M, Maccarelli F (1997) Oenological properties of non-Saccharomyces yeasts associated with wine-making. World J Microbiol Biotechnol 14:199–203

    Article  Google Scholar 

  7. Ciani M, Picciotti G (1995) The growth kinetics and fermentation behaviour of some non-Saccharomyces yeasts associated with wine-making. Biotechnol Lett 17:1247–1250

    Article  CAS  Google Scholar 

  8. Renault P, Miot-Sertier C, Marullo P, Hernández-Orte P, Lagarrigue L, Lonvaud-Funel A, Bely M (2009) Genetic characterization and phenotypic variability in Torulaspora delbrueckii species: potential applications in the wine industry. Int J Food Microbiol 134:201–210

    Article  CAS  PubMed  Google Scholar 

  9. Brandam C, Lai QP, Julien-Ortiz A, Taillandier P (2013) Influence of oxygen on alcoholic fermentation by a wine strain of Torulaspora delbrueckii: kinetics and carbon mass balance. Biosci Biotechnol Biochem 77:1848–1853

    Article  CAS  PubMed  Google Scholar 

  10. Renault P, Coulon J, de Revel G, Barbe JC, Bely M (2015) Increase of fruity aroma during mixed T. delbrueckii/S. cerevisiae wine fermentation is linked to specific esters enhancement. Int J Food Microbiol 207:40–48

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  12. Nissen P, Arneborg N (2003) Characterization of early deaths of non-Saccharomyces yeasts in mixed cultures with Saccharomyces cerevisiae. Arch Microbiol 180:257–263

    Article  CAS  PubMed  Google Scholar 

  13. Velázquez R, Zamora E, Álvarez ML, Hernández LM, Ramírez M (2015) Effects of new Torulaspora delbrueckii killer yeasts on the must fermentation kinetics and aroma compounds of white table wine. Front Microbiol 6:1222

    Article  PubMed  PubMed Central  Google Scholar 

  14. Ramírez M, Velázquez R, Maqueda M, López-Piñeiro A, Ribas JC (2015) A new wine Torulaspora delbrueckii killer strain with broad antifungal activity and its toxin-encoding double-stranded RNA virus. Front Microbiol 6:983

    Article  PubMed  PubMed Central  Google Scholar 

  15. Rodriguez-Cousino N, Maqueda M, Ambrona J, Zamora E, Esteban R, Ramírez M (2011) A New Wine Saccharomyces cerevisiae Killer Toxin (Klus), encoded by a double-stranded RNA virus, with broad antifungal activity is evolutionarily related to a chromosomal host gene. Appl Environ Microbiol 77:1822–1832

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Albergaria H, Francisco D, Gori K, Arneborg N, Gírio F (2010) Saccharomyces cerevisiae CCMI 885 secretes peptides that inhibit the growth of some non-Saccharomyces wine-related strains. Appl Microbiol Biotechnol 86:965–972

    Article  CAS  PubMed  Google Scholar 

  17. Branco P, Francisco D, Monteiro M, Almeida MG, Caldeira J, Arneborg N, Prista C, Albergaria H (2017) Antimicrobial properties and death-inducing mechanisms of saccharomycin, a biocide secreted by Saccharomyces cerevisiae. Appl Microbiol Biotechnol 101:159–171

    Article  CAS  PubMed  Google Scholar 

  18. Albergaria H, Arneborg N (2016) Dominance of Saccharomyces cerevisiae in alcoholic fermentation processes: role of physiological fitness and microbial interactions. Appl Microbiol Biotechnol 100:2035–2046

    Article  CAS  PubMed  Google Scholar 

  19. Holm Hansen E, Nissen P, Sommer P, Nielsen JC, Arneborg N (2001) The effect of oxygen on the survival of non-Saccharomyces yeasts during mixed culture fermentations of grape juice with Saccharomyces cerevisiae. J Appl Microbiol 91:541–547

    Article  CAS  PubMed  Google Scholar 

  20. Daum G, Lees ND, Bard M, Dickson R (1998) Biochemistry, cell biology and molecular biology of lipids of Saccharomyces cerevisiae. Yeast 14:1471–1510

    Article  CAS  PubMed  Google Scholar 

  21. Alexandre H, Rousseaux I, Charpentier C (1994) Relationship between ethanol tolerance, lipid composition and plasma membrane fluidity in Saccharomyces cerevisiae and Kloeckera apiculata. FEMS Microbiol Lett 124:17–22

    Article  CAS  PubMed  Google Scholar 

  22. Pina C, Santos C, Couto JA, Hogg T (2004) Ethanol tolerance of five non-Saccharomyces wine yeasts in comparison with a strain of Saccharomyces cerevisiae, influence of different culture conditions. Food Microbiol 21:439–447

    Article  CAS  Google Scholar 

  23. Deytieux C, Mussard L, Biron MJ, Salmon JM (2005) Fine measurement of ergosterol requirements for growth of Saccharomyces cerevisiae during alcoholic fermentation. Appl Microbiol Biotechnol 68:266–271

    Article  CAS  PubMed  Google Scholar 

  24. Delfini C, Costa A (1993) Effects of the Grape must lees and insoluble materials on the alcoholic fermentation rate and the production of acetic acid, pyruvic acid, and acetaldehyde. Am J Enol Vitic 44:86–92

    CAS  Google Scholar 

  25. Rosi I, Bertuccioli M (1992) Influence of lipid addition on fatty acid composition of Saccharomyces cerevisiae and aroma characteristics of experimental wines. J Inst Brew 98:305–314

    Article  CAS  Google Scholar 

  26. Lee AG (2004) How lipids affect the activities of integral membrane proteins. Biochim Biophys Acta BBA Biomembr 1666:62–87

    Article  CAS  Google Scholar 

  27. Lees ND, Bard M, Kirsch DR (1997) In: Parish EJ, Nes WD (eds) Biochemistry and function of sterols, 1st edn. CRC Press, Boca Raton

    Google Scholar 

  28. Kleinhans FW, Lees ND, Bard M, Haak RA, Woods RA (1979) ESR determinations of membrane permeability in a yeast sterol mutant. Chem Phys Lipids 23:143–154

    Article  PubMed  Google Scholar 

  29. Loira I, Vejarano R, Bañuelos MA, Morata A, Tesfaye W, Uthurry C, Villa A, Cintora I, Suárez-Lepe JA (2014) Influence of sequential fermentation with Torulaspora delbrueckii and Saccharomyces cerevisiae on wine quality. LWT Food Sci Technol 59:915–922

    Article  CAS  Google Scholar 

  30. Canonico L, Comitini F, Ciani M (2017) Torulaspora delbrueckii contribution in mixed brewing fermentations with different Saccharomyces cerevisiae strains. Int J Food Microbiol 259:7–13

    Article  CAS  PubMed  Google Scholar 

  31. Azzolini M, Fedrizzi B, Tosi E, Finato F, Vagnoli P, Scrinzi C, Zapparoli G (2012) Effects of Torulaspora delbrueckii and Saccharomyces cerevisiae mixed cultures on fermentation and aroma of Amarone wine. Eur Food Res Technol 235:303–313

    Article  CAS  Google Scholar 

  32. Nissen P, Nielsen D, Arneborg N (2003) Viable Saccharomyces cerevisiae cells at high concentrations cause early growth arrest of non-Saccharomyces yeasts in mixed cultures by a cell-cell contact-mediated mechanism. Yeast 20:331–341

    Article  CAS  PubMed  Google Scholar 

  33. 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

    Article  CAS  Google Scholar 

  34. Lopez CLF, Beaufort S, Brandam C, Taillandier P (2014) Interactions between Kluyveromyces marxianus and Saccharomyces cerevisiae in tequila must type medium fermentation. World J Microbiol Biotechnol 30:2223–2229

    Article  CAS  PubMed  Google Scholar 

  35. Salgado ME, Albasi C, Riba JP (2000) A two-reservoir, hollow-fiber bioreactor for the study of mixed-population dynamics: design aspects and validation of the approach. Biotechnol Bioeng 69:401–408

    Article  Google Scholar 

  36. Salmon JM, Barre P (1998) Improvement of nitrogen assimilation and fermentation kinetics under enological conditions by derepression of alternative nitrogen-assimilatory pathways in an industrial Saccharomyces cerevisiae strain. Appl Environ Microbiol 64:3831–3837

    CAS  PubMed  PubMed Central  Google Scholar 

  37. Albasi C, Tataridis P, Salgado Manjarrez E, Taillandier P (2001) A new tool for the quantification of microorganism interaction dynamics. Ind Eng Chem Res 40:5222–5227

    Article  CAS  Google Scholar 

  38. Jimenez RR, Ladha JK (1993) Automated elemental analysis: a rapid and reliable but expensive measurement of total carbon and nitrogen in plant and soil samples. Commun Soil Sci Plant Anal 24:1897–1924

    Article  CAS  Google Scholar 

  39. Racine JS (2012) RStudio: a platform-independent IDE for R and Sweave. J Appl Econom 27:167–172

    Article  Google Scholar 

  40. Rodriguez RJ, Low C, Bottema CD, Parks LW (1985) Multiple functions for sterols in Saccharomyces cerevisiae. Biochim Biophys Acta BBA-Lipids Lipid Metab 837:336–343

    Article  CAS  Google Scholar 

  41. Lucero HA, Robbins PW (2004) Lipid rafts–protein association and the regulation of protein activity. Arch Biochem Biophys 426:208–224

    Article  CAS  PubMed  Google Scholar 

  42. Souza CM, Pichler H (2007) Lipid requirements for endocytosis in yeast. Biochim Biophys Acta BBA Mol Cell Biol Lipids 1771:442–454

    CAS  Google Scholar 

  43. Valdez-Taubas J, Pelham HRB (2003) Slow diffusion of proteins in the yeast plasma membrane allows polarity to Be maintained by endocytic cycling. Curr Biol 13:1636–1640

    Article  CAS  PubMed  Google Scholar 

  44. Viegas CA, Rosa MF, Sá-Correia I, Novais JM (1989) Inhibition of yeast growth by octanoic and decanoic acids produced during ethanolic fermentation. Appl Environ Microbiol 55:21–28

    CAS  PubMed  PubMed Central  Google Scholar 

  45. Renault PE, Albertin W, Bely M (2013) An innovative tool reveals interaction mechanisms among yeast populations under oenological conditions. Appl Microbiol Biotechnol 97:4105–4119

    Article  CAS  PubMed  Google Scholar 

  46. Mauricio JC, Millán C, Ortega JM (1998) Influence of oxygen on the biosynthesis of cellular fatty acids, sterols and phospholipids during alcoholic fermentation by Saccharomyces cerevisiae and Torulaspora delbrueckii. World J Microbiol Biotechnol 14:405–410

    Article  CAS  Google Scholar 

  47. Tronchoni J, Curiel JA, Morales P, Torres-Pérez R, Gonzalez R (2017) Early transcriptional response to biotic stress in mixed starter fermentations involving Saccharomyces cerevisiae and Torulaspora delbrueckii. Int J Food Microbiol 241:60–68

    Article  CAS  PubMed  Google Scholar 

  48. Rivero D, Berná L, Stefanini I, Baruffini E, Bergerat A, Csikász-Nagy A, De Filippo C, Cavalieri D (2015) Hsp12p and PAU genes are involved in ecological interactions between natural yeast strains: Natural yeast interactions. Environ Microbiol 17:3069–3081

    Article  CAS  PubMed  Google Scholar 

  49. Barbosa C, Mendes-Faia A, Lage P, Mira NP, Mendes-Ferreira A (2015) Genomic expression program of Saccharomyces cerevisiae along a mixed-culture wine fermentation with Hanseniaspora guilliermondii. Microb Cell Factories 14:124

    Article  CAS  Google Scholar 

  50. Hernández-López MJ, Pallotti C, Andreu P, Aguilera J, Prieto JA, Randez-Gil F (2007) Characterization of a Torulaspora delbrueckii diploid strain with optimized performance in sweet and frozen sweet dough. Int J Food Microbiol 116:103–110

    Article  CAS  PubMed  Google Scholar 

  51. Branco P, Viana T, Albergaria H, Arneborg N (2015) Antimicrobial peptides (AMPs) produced by Saccharomyces cerevisiae induce alterations in the intracellular pH, membrane permeability and culturability of Hanseniaspora guilliermondii cells. Int J Food Microbiol 205:112–118

    Article  CAS  PubMed  Google Scholar 

  52. Lichtenstein A, Ganz T, Selsted ME, Lehrer RI (1986) In vitro tumor cell cytolysis mediated by peptide defensins of human and rabbit granulocytes. Blood 68:1407–1410

    CAS  PubMed  Google Scholar 

  53. Pandey BK, Srivastava S, Singh M, Ghosh JK (2011) Inducing toxicity by introducing a leucine-zipper-like motif in frog antimicrobial peptide, magainin 2. Biochem J 436:609–620

    Article  CAS  PubMed  Google Scholar 

  54. Brogden KA (2005) Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria? Nat Rev Microbiol 3:238

    Article  CAS  PubMed  Google Scholar 

  55. Harris F, Dennison S, Phoenix D (2009) Anionic Antimicrobial Peptides from Eukaryotic Organisms. Curr Protein Pept Sci 10:585–606

    Article  CAS  PubMed  Google Scholar 

  56. Kagan BL, Ganz T, Lehrer RI (1994) Defensins: a family of antimicrobial and cytotoxic peptides. Toxicology 87:131–149

    Article  CAS  PubMed  Google Scholar 

  57. Gallo M, Katz E (1972) Regulation of secondary metabolite biosynthesis: catabolite repression of phenoxazinone synthase and actinomycin formation by glucose. J Bacteriol 109:659–667

    CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This work was financially supported by the French Ministry of Higher Education and Research. The authors thank Agathe Juppeau for providing excellent technical assistance.

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  1. Laboratoire de Génie Chimique, Université de Toulouse, CNRS, INPT, UPS, Toulouse, France

    Paul Brou, Patricia Taillandier, Sandra Beaufort & Cédric Brandam

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  1. Paul Brou
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  2. Patricia Taillandier
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Correspondence to Paul Brou.

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Brou, P., Taillandier, P., Beaufort, S. et al. Mixed culture fermentation using Torulaspora delbrueckii and Saccharomyces cerevisiae with direct and indirect contact: impact of anaerobic growth factors. Eur Food Res Technol 244, 1699–1710 (2018). https://doi.org/10.1007/s00217-018-3095-3

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