Skip to main content
SpringerLink
Log in

Effect of growth temperature on yeast lipid composition and alcoholic fermentation at low temperature

  • Original Paper
  • Published:
European Food Research and Technology Aims and scope Submit manuscript

Abstract

The loss of viability of wine yeast strains due to low-temperature fermentations could be overcome by increasing their stress tolerance and adaptability. Changes in membrane lipid composition are one of the first responses to cold stress. The aim of this study was to analyze the various adaptation mechanisms to low temperatures by comparing the better adapted Saccharomyces species. The viability, vitality, fermentation capacity, and lipid composition of different Saccharomyces species (S. cerevisiae, S. bayanus, S. uvarum, and a hybrid S. cerevisiae/S. uvarum) with different fermentative origins (wine, beer, and baker’s strains together with a laboratory strain) were compared after culturing at low (13 °C) and optimal (25 °C) temperatures. In spite of specific responses of the different strains/species, the results showed that at low temperature, the medium-chain fatty acid and the triacylglyceride content increased, whereas the phosphatidic acid content and the phosphatidylcholine/phosphatidylethanolamine ratio decreased. Only the laboratory strain was not able to ferment the sugars, and after growing at both temperatures, its lipid composition was very different from that of the other strains. The hybrid strain showed the highest sugar consumption at 13 °C and the best vitality whatever the preculture temperature used. The rest of the species needed a preadaptation at low temperature involving a change in their lipid composition to improve their fermentation rate at 13 °C.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Beltran G, Novo M, Guillamón JM, Mas A, Rozès N (2008) Effect of fermentation temperature and culture media on the yeast lipid composition and wine volatile compounds. Int J Food Microbiol 121:169–177

    Article  CAS  Google Scholar 

  2. Llauradó J, Rozès N, Bobet R, Mas A, Constantí M (2002) Low temperature alcoholic fermentation in high sugar concentration grape musts. J Food Sci 67:268–273

    Article  Google Scholar 

  3. Torija MJ, Beltran G, Novo M, Poblet M, Guillamón JM, Mas A, Rozès N (2003) Effects of fermentation temperature and Saccharomyces species on the cell fatty acid composition and presence of volatile compounds in wine. Int J Food Microbiol 85:127–136

    Article  CAS  Google Scholar 

  4. Beltran G, Novo M, Leberre V, Sokol S, Labourdette D, Guillamón JM, Mas A, François J, Rozès N (2006) Integration of transcriptomic and metabolic analyses for understanding the global responses of low-temperature winemaking fermentations. FEMS Yeast Res 6:1167–1183

    Article  CAS  Google Scholar 

  5. Salvadó Z, Chiva R, Rodríguez-Vargas S, Rández-Gil F, Mas A, Guillamón JM (2008) Proteomic evolution of a wine yeast during the first hours of fermentation. FEMS Yeast Res 8:1137–1146

    Article  Google Scholar 

  6. Sakamoto T, Murata N (2002) Regulation of the desaturation of fatty acids and its role in tolerance to cold and salt stress. Curr Opin Microbiol 5:208–210

    Article  Google Scholar 

  7. Redón M, Guillamón JM, Mas A, Rozès N (2009) Effect of lipid supplementation upon Saccharomyces cerevisiae lipid composition and fermentation performance at low temperature. Eur Food Res Technol 228:833–840

    Article  Google Scholar 

  8. Naumov GI, Masneuf I, Naumova ES, Aigle M, Dubourdieu D (2000) Association of Saccharomyces bayanus var. uvarum with some French wines: genetic analysis of yeast populations. Res Microbiol 151:683–691

    Article  CAS  Google Scholar 

  9. Nguyen HV, Gaillardin C (2005) Evolutionary relationships between the former species Saccharomyces uvarum and the hybrids Saccharomyces bayanus and Saccharomyces pastorianus; reinstatement of Saccharomyces uvarum (Beijerinck) as a distinct species. FEMS Yeast Res 5:471–483

    Article  CAS  Google Scholar 

  10. Pulvirenti A, Nguyen H, Caggia C, Giudici P, Rainieri S, Zambonelli C (2000) Saccharomyces uvarum, a proper species within Saccharomyces sensu stricto. FEMS Microbiol Lett 192:191–196

    Article  CAS  Google Scholar 

  11. Naumov GI, Nguyen HV, Naumova ES, Michel A, Aigle M, Gaillardin C (2001) Genetic identification of Saccharomyces bayanus var. uvarum, a cider-fermenting yeast. Int J Food Microbiol 65:163–171

    Article  CAS  Google Scholar 

  12. Naumov GI, Naumova ES, Antunovics Z, Sipiczki M (2002) Saccharomyces bayanus var. uvarum in Tokaj wine-making of Slovakia and Hungary. Appl Microbiol Biotechnol 59:727–730

    Article  CAS  Google Scholar 

  13. Demuyter C, Lollier M, Legras JL, Le Jeune C (2004) Predominance of Saccharomyces uvarum during spontaneous alcoholic fermentation, for three consecutive years, in an Alsatian winery. J Appl Microbiol 97:1140–1148

    Article  CAS  Google Scholar 

  14. Naumov GI (1996) Genetic identification of biological species in the Saccharomyces sensu stricto complex. J Ind Microbiol 17:295–302

    Article  CAS  Google Scholar 

  15. Giudici P, Caggia C, Pulvirenti A, Zambonelli C, Rainieri S (1998) Electrophoretic profile of hybrids between cryotolerant and non-cryotolerant Saccharomyces strains. Lett Appl Microbiol 27:31–34

    Article  CAS  Google Scholar 

  16. Naumov GI, James SA, Naumova ES, Louis EJ, Roberts IN (2000) Three new species in the Saccharomyces sensu stricto complex: Saccharomyces cariocanus, Saccharomyces kudriavzevii and Saccharomyces mikatae. Int J Syst Evol Microbiol 50:1931–1942

    CAS  Google Scholar 

  17. González SS, Barrio E, Gafner J, Querol A (2006) Natural hybrids from Saccharomyces cerevisiae, Saccharomyces bayanus and Saccharomyces kudriavzevii in wine fermentations. FEMS Yeast Res 6:1221–1234

    Article  Google Scholar 

  18. Nilsson-Tillgren T, Gjermansen C, Kielland-Brandt MC, Litske Petersen JG, Holmberg S (1981) Genetic differences between Saccharomyces carlsbergensis and S. cerevisiae. Analysis of chromosome III by single chromosome transfer. Carlberg Res Commun 46:65–76

    Article  CAS  Google Scholar 

  19. Rainieri S, Kodama Y, Kaneko Y, Mikata K, Nakao Y, Ashikari T (2006) Pure and mixed genetic lines of Saccharomyces bayanus and Saccharomyces pastorianus and their contribution to the lager brewing strain genome. Appl Environ Microbiol 72:3968–3974

    Article  CAS  Google Scholar 

  20. Masneuf I, Hansen J, Groth C, Piskur J, Dubourdieu D (1998) New hybrids between Saccharomyces sensu stricto yeast species found among wine and cider production strains. Appl Environ Microbiol 64:3887–3892

    CAS  Google Scholar 

  21. Lopandic K, Gangl H, Wallner E, Tscheik G, Leitner G, Querol A, Borth N, Breitenbach M, Prillinger H, Tiefenbrunner W (2007) Genetically different wine yeasts isolated from Austrian vine-growing regions influence wine aroma differently and contain putative hybrids between Saccharomyces cerevisiae and Saccharomyces kudriavzevii. FEMS Yeast Res 7:953–965

    Article  CAS  Google Scholar 

  22. Gangl H, Batusic M, Tscheik G, Tiefenbrunner W, Hack C, Lopandic K (2009) Exceptional fermentation characteristics of natural hybrids from Saccharomyces cerevisiae and S. kudriavzevii. N Biotechnol 25:244–251

    Article  CAS  Google Scholar 

  23. Naumova ES, Naumov GI, Masneuf-Pomarède I, Aigle M, Dubourdieu D (2005) Molecular genetic study of introgression between Saccharomyces bayanus and S. cerevisiae. Yeast 22:1099–1115

    Article  CAS  Google Scholar 

  24. Masneuf-Pomarède I, Bely M, Marullo P, Lonvaud-Funel A, Dubourdieu D (2010) Reassessment of phenotypic traits for Saccharomyces bayanus var. uvarum wine yeast strains. Int J Food Microbiol 139:79–86

    Article  Google Scholar 

  25. Masneuf I, Murat ML, Dubourdieu D, Naumov GL, Tominaga T (2002) Hybrids Saccharomyces cerevisiae x Saccharomyces bayanus var. uvarum having a high liberating ability of some sulfur varietal aromas of “vitis vinifera” Sauvignon blanc wines. Int J Vine Wine Sci 36:205–212

    CAS  Google Scholar 

  26. Riou C, Nicaud JM, Barre P, Gaillardin C (1997) Stationary-phase gene expression in Saccharomyces cerevisiae during wine fermentation. Yeast 13:903–915

    Article  CAS  Google Scholar 

  27. Rozès N, Garcia Jares C, Larue F, Lonvaud-Funel A (1992) Differentiation between fermenting and spoilage yeasts in wine by total free fatty acid analysis. J Sci Food Agric 59:351–359

    Article  Google Scholar 

  28. Sweeney JY, Kuehne HA, Sniegowski PD (2004) Sympatric natural Saccharomyces cerevisiae and S. paradoxus populations have different thermal growth profiles. FEMS Yeast Res 4:521–525

    Article  CAS  Google Scholar 

  29. Sampaio JP, Gonçalves P (2008) Natural populations of Saccharomyces kudriavzevii in Portugal are associated with oak bark and are sympatric with S. cerevisiae and S. paradoxus. Appl Environ Microb 74:2144–2152

    Article  CAS  Google Scholar 

  30. Goddard MR (2008) Quantifying the complexities of Saccharomyces cerevisiae’s ecosystem engineering via fermentation. Ecology 9:2077–2082

    Article  Google Scholar 

  31. Arroyo-Lopez FN, Orlić S, Querol A, Barrio E (2009) Effects of temperature, pH and sugar concentration on the growth parameters of Saccharomyces cerevisiae, S. kudriavzevii and their interspecific hybrid. Int J Food Microbiol 131:120–127

    Article  CAS  Google Scholar 

  32. Llauradó JM, Rozès N, Constantí M, Mas A (2005) Study of some Saccharomyces cerevisiae strains for wine-making after pre-adaptation at low temperatures. J Agric Food Chem 53:1003–1011

    Article  Google Scholar 

  33. Abe F, Horikoshi K (2000) Tryptophan permease gene TAT2 confers high-pressure growth in Saccharomyces cerevisiae. Mol Cell Biol 20:8093–8102

    Article  CAS  Google Scholar 

  34. Gabardino J, Sturley SL (2005) Homoeostatic systems for sterols and other lipids. Biochem Soc T 33:1182–1185

    Article  Google Scholar 

  35. You KM, Rosenfield CL, Knipple DC (2003) Ethanol tolerance in the yeast Saccharomyces cerevisiae is dependent on cellular oleic acid content. Appl Environ Microbiol 69:1499–1503

    Article  CAS  Google Scholar 

  36. Mannazzu I, Angelozzi D, Belviso S, Budroni M, Farris GA, Goffrini P, Lodi T, Marzona M, Bardi L (2008) Behaviour of Saccharomyces cerevisiae wine strains during adaptation to unfavourable conditions of fermentation on synthetic medium: cell lipid composition, membrane integrity, viability and fermentative activity. Int J Food Microbiol 121:84–91

    Article  CAS  Google Scholar 

  37. Müllner H, Daum G (2004) Dynamics of neutral lipid storage in yeast. Acta Biochim Pol 51:323–347

    Google Scholar 

Download references

Acknowledgments

This work was financially supported by a grant from the Spanish government (AGL2007-65498-C02/ALI). Saccharomyces uvarum PJP3 and the hybrid S. cerevisiae/S. uvarum 14a were kindly supplied by Prof. Isabelle Masneuf-Pomarède, ENITA of Bordeaux (France). The commercial baker’s strain Plus Vital was also kindly supplied by Dr. Francisca Rández from the IATA (CSIC). The authors would also like to thank the Language Service of the Rovira i Virgili University for checking the manuscript.

Author information

Authors and Affiliations

  1. Biotecnologia Enològica, Department of Bioquímica i Biotecnología, Facultat d’Enologia, Universitat Rovira i Virgili, Campus Sescelades, C/Marcel lí Domingo, s/n, 43007, Tarragona, Spain

    Marian Redón, Albert Mas & Nicolas Rozès

  2. Departamento de Biotecnología de los alimentos, Instituto de Agroquímica y Tecnología de Alimentos (CSIC), P.O. Box 73, 46100, Burjassot, Valencia, Spain

    José Manuel Guillamón

Authors
  1. Marian Redón
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. José Manuel Guillamón
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Albert Mas
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Nicolas Rozès
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to José Manuel Guillamón.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Redón, M., Guillamón, J.M., Mas, A. et al. Effect of growth temperature on yeast lipid composition and alcoholic fermentation at low temperature. Eur Food Res Technol 232, 517–527 (2011). https://doi.org/10.1007/s00217-010-1415-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00217-010-1415-3

Keywords

Search

Navigation