Skip to main content

Advertisement

Log in

Fermentative capacity of dry active wine yeast requires a specific oxidative stress response during industrial biomass growth

  • Applied Microbial and Cell Physiology
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Induction of the oxidative stress response has been described under many physiological conditions in Saccharomyces cerevisiae, including industrial fermentation for wine yeast biomass production where cells are grown through several batch and fed-batch cultures on molasses. Here, we investigate the influence of aeration on the expression changes of different gene markers for oxidative stress and compare the induction profiles to the accumulation of several intracellular metabolites in order to correlate the molecular response to physiological and metabolic changes. We also demonstrate that this specific oxidative response is relevant for wine yeast performance by construction of a genetically engineered wine yeast strain overexpressing the TRX2 gene that codifies a thioredoxin, one of the most important cellular defenses against oxidative damage. This modified strain displays an improved fermentative capacity and lower levels of oxidative cellular damages than its parental strain after dry biomass production.

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

Access this article

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Aranda A, Querol A, del Olmo M (2002) Correlation between acetaldehyde and ethanol resistance and expression of HSP genes in yeast strains isolated during the biological aging of sherry wines. Arch Microbiol 177:304–312

    Article  CAS  PubMed  Google Scholar 

  • Beudeker RF, van Damm HW, van der Plaat JB, Vellenga K (1990) Developments in baker’s yeast production. In: Verachtert H, deMot R (eds) Yeast: biotechnology and biocatalysis. Marcel Dekker, New York, pp 103–146

    Google Scholar 

  • Buege JA, Aust SD (1978) Microsomal lipid peroxidation. Methods Enzymol 52:302–310

    Article  CAS  PubMed  Google Scholar 

  • Costa V, Moradas-Ferreira P (2001) Oxidative stress and signal transduction in Saccharomyces cerevisiae: insights into ageing, apoptosis and diseases. Mol Aspects Med 22:217–246

    Article  CAS  PubMed  Google Scholar 

  • de Koning W, van Dam K (1992) A method for the determination of changes of glycolytic metabolites in yeast on a subsecond time scale using extraction at neutral pH. Anal Biochem 204:118–123

    Article  PubMed  Google Scholar 

  • Dimster-Denk D, Rine J (1996) Transcriptional regulation of a sterol-biosynthetic enzyme by sterol levels in Saccharomyces cerevisiae. Mol Cell Biol 16:3981–3989

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Espindola AS, Gomes DS, Panek AD, Eleutherio EC (2003) The role of glutathione in yeast dehydration tolerance. Cryobiology 47:236–241

    Article  CAS  Google Scholar 

  • Garrido EO, Grant CM (2002) Role of thioredoxins in the response of Saccharomyces cerevisiae to oxidative stress induced by hydroperoxides. Mol Microbiol 43:993–1003

    Article  CAS  PubMed  Google Scholar 

  • Gasch AP, Spellman PT, Kao CM, Carmel-Harel O, Eisen MB, Storz G, Botstein D, Brown PO (2000) Genomic expression programs in the response of yeast cells to environmental changes. Mol Biol Cell 11:4241–4257

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gibson BR, Lawrence SJ, Boulton CA, Box WG, Graham NS, Linforth RST, Smart KA (2008) The oxidative stress response along a lager brewing yeast strain during industrial propagation and fermentation. FEMS Yeast Res 8:574–584

    Article  CAS  PubMed  Google Scholar 

  • Gietz RD, Schiestl RH, Willems AR, Woods RA (1995) Studies on the transformation of intact yeast cells by the LiAc/SS-DNA/PEG procedure. Yeast 11:355–360

    Article  CAS  PubMed  Google Scholar 

  • Gimeno-Alcañiz JV, Matallana E (2001) Performance of industrial strains of Saccharomyces cerevisae during wine fermentation is affected by manipulation strategies based on sporulation. Syst Appl Microbiol 24:639–644

    Article  Google Scholar 

  • Godon C, Lagniel G, Lee J, Buhler JM, Kieffer S, Perrot M, Boucherie H, Toledano MB, Labarre J (1998) The H2O2 stimulon in Saccharomyces cerevisiae. J Biol Chem 273:22480–22489

    Article  CAS  PubMed  Google Scholar 

  • Grant CM (2001) Role of the glutathione/glutaredoxin and thioredoxin systems in yeast growth and response to stress conditions. Mol Microbiol 39:533–541

    Article  CAS  PubMed  Google Scholar 

  • Gustafsson L (1979) The ATP pool in relation to the production of glycerol and heat during growth of the halotolerant yeast Debaryomyces hansenii. Arch Microbiol 120:15–23

    Article  CAS  Google Scholar 

  • Haarasilta S, Oura E (1975) On the activity and regulation of anaplerotic and gluconeogenetic enzymes during growth process of baker’s yeast. Eur J Biochem 52:1–7

    Article  CAS  PubMed  Google Scholar 

  • Hohmann S, Mager WH (2003) Yeast stress responses. Springer, Heidelberg

    Book  Google Scholar 

  • Holmgren A (1989) Thioredoxin and glutaredoxin systems. J Biol Chem 265:13963–13966

    Article  Google Scholar 

  • Ivorra C, Pérez-Ortín JE, del Olmo M (1999) An inverse correlation between stress resistance and stuck fermentations in wine yeasts. A molecular study. Biotechnol Bioeng 64:698–708

    Article  CAS  PubMed  Google Scholar 

  • Jamieson DJ (1998) Oxidative stress responses of the yeast Saccharomyces cerevisiae. Yeast 14:1511–1527

    Article  CAS  PubMed  Google Scholar 

  • Jorgensen H, Olsson L, Ronnow B, Palmqvist EA (2002) Fed-batch cultivation of baker’s yeast followed by nitrogen or carbon starvation: effects on fermentative capacity and content of trehalose and glycogen. Appl Environ Microbiol 59:310–317

    CAS  Google Scholar 

  • Koerkamp MG, Rep M, Bussemaker HJ, Hardy GPMA, Mul A, Piekarska K, Szigyarto CA, Teixeira de Mattos JM, Tabak HF (2002) Dissection of transient oxidative stress response in Saccharomyces cerevisiae by using DNA microarrays. Mol Biol Cell 13:2783–2794

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Larsson C, Påhlman IL, Ansell R, Rigoulet M, Adler L, Gustafsson L (1998) The importance of the glycerol 3-phosphate shuttle during aerobic growth of Saccharomyces cerevisiae. Yeast 14:347–357

    Article  CAS  PubMed  Google Scholar 

  • Monje-Casas F, Michán C, Pueyo C (2004) Absolute transcript levels of thioredoxin- and glutathione-dependent redox systems in Saccharomyces cerevisiae: response to stress and modulation of growth. Biochem J 383:139–147

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moye-Rowley WS (2003) Regulation of the transcriptional response to oxidative stress in fungi: similarities and differences. Eukaryot Cell 2:381–389

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Muller EGD (1996) A glutathione reductase mutants of yeast accumulates high levels of oxidized glutathione and requires thioredoxin for growth. Mol Biol Cell 7:1805–1813

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nagodawithana TW, Trivedi NB (1990) Yeast selection for baking. In: Panchal CJ (ed) Yeast strain selection. Marcel Dekker, New York, pp 139–184

    Google Scholar 

  • Parks LW, Casey WM (1995) Physiological implications of sterol biosynthesis in yeast. Annu Rev Microbiol 49:95–116

    Article  CAS  PubMed  Google Scholar 

  • Panadero J, Hernández-López MJ, Prieto JA, Randez-Gil F (2007) Overexpression of the calcineurin target CRZ1 provides freeze tolerance and enhances the fermentative capacity of baker’s yeast. Appl Environ Microbiol 73:4824–4831

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pereira MD, Eleutherio ECA, Panek AD (2001) Acquisition of tolerance against oxidative damage in Saccharomyces cerevisiae. BMC Microbiol 1:11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pérez-Torrado R, Gimeno-Alcañiz JV, Matallana E (2002a) Wine yeast strains engineered for glycogen overproduction display enhanced viability under glucose deprivation conditions. Appl EnvironMicrobiol 68:3339–3344

    Google Scholar 

  • Pérez-Torrado R, Carrasco P, Aranda A, Gimeno-Alcañiz JV, Pérez-Ortín JE, Matallana E, del Olmo M (2002b) Study of the first hours of microvinification by the use of osmotic stress-response genes as probes. Syst Appl Microbiol 25:153–161

    Article  PubMed  Google Scholar 

  • Pérez-Torrado R, Bruno-Barcena JM, Matallana E (2005) Monitoring stress-related genes during the process of biomass propagation of Saccharomyces cerevisiae strains used for wine making. Appl Environ Microbiol 71:6831–6837

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Puig S, Perez-Ortín JE (2000) Expression levels and patterns of glycolytic yeast genes during wine fermentation. Syst Appl Microbiol 23:300–303

    Article  CAS  PubMed  Google Scholar 

  • Querol A, Barrio E, Ramón D (1992) A comparative-study of different methods of yeast-strain characterization. Syst Appl Microbiol 15:439–446

    Article  Google Scholar 

  • Rizzi M, Baltes M, Theobald U, Reuss M (1997) In vivo analysis of metabolic dynamics in Saccharomyces cerevisiae: II. Mathematical model. Biotechnol Bioeng 55:592–608

    Article  CAS  PubMed  Google Scholar 

  • Rodrigues-Pousada CA, Nevitt T, Menezes R, Azevedo D, Pereira J, Amaral C (2004) Yeast activator proteins and stress response: an overview. FEBS Lett 567:80–85

    Article  CAS  PubMed  Google Scholar 

  • Rose AH, Vijaylakshimi G (1993) Baker’s yeasts. In: Rose AH, Harrison JS (eds) The yeasts, vol 5. 2nd edn. Academic Press, London, pp 357–397

    Chapter  Google Scholar 

  • Rosen K (1989) Preparation of yeast for industrial use in the production of beverages. In: Cantarelli C, Lanzarini G (eds) Biotechnology applications in beverage production. Elsevier Applied Science, London, pp 169–187

    Chapter  Google Scholar 

  • Servouse M, Karst F (1986) Regulation of early enzymes of ergosterol biosynthesis in Saccharomyces cerevisiae. Biochem J 240:541–547

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Theobald U, Mailinger W, Baltes M, Rizzi M, Reuss M (1997) In vivo analysis of metabolic dynamics in Saccharomyces cerevisiae: I. Experimental observation. Biotechnol Bioeng 55:305–316

    Article  CAS  PubMed  Google Scholar 

  • Toledano MB, Delaunay A, Biteau B, Spector D, Azevedo D (2003) Oxidative stress responses in yeasts. In: Hohmann S, Mager WH (eds) Yeast stress responses. Springer, Berlin, pp 241–287

    Chapter  Google Scholar 

  • Toledano MB, Kumar C, Le MN, Spector D, Tacnet F (2007) The systems biology of thiol redox system in Escherichia coli and yeast: differential functions in oxidative stress, iron metabolism and DNA synthesis. FEBS Lett 581:3598–3607

    Article  CAS  PubMed  Google Scholar 

  • Walker GM (1998) Yeast physiology and biotechnology. Wiley, Chichester

    Google Scholar 

  • Wu AL, Moye-Rowley WS (1994) GSH1, which encodes γ-glutamylcysteine synthetase, is a target gene for yAP-1 transcriptional regulation. Mol Cell Biol 14:5832–5839

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zuzuarregui A, del Olmo M (2004a) Expression of stress response genes in wine strains with different fermentative behaviour. FEMS Yeast Res 4:699–710

    Article  CAS  PubMed  Google Scholar 

  • Zuzuarregui A, del Olmo M (2004b) Analyses of stress resistance under laboratory conditions constitute a suitable criterion for wine yeast selection. Antonie Van Leeuwenhoek 85:271–280

    Article  CAS  PubMed  Google Scholar 

  • Zuzuarregui A, Carrasco P, Palacios A, Julien A, del Olmo M (2005) Analysis of the expression of some stress induced genes in several commercial wine yeast strains at the beginning of vinification. J Appl Microbiol 98:299–307

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by grants AGL2002-01109, AGL 2005-00508 from the “Ministerio de Educación y Ciencia” (MEC), and GRUPOS03/012 and GVACOMP2007-157 from the “Generalitat Valenciana”. R.P.-T. was supported by a predoctoral fellowship from “Generalitat Valenciana” and R.G.-P. is a predoctoral fellow of the I3P program of “Consejo Superior de Investigaciones Científicas” (Spain). We thank Dr. E. Garre for critical reading of the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Emilia Matallana.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Pérez-Torrado, R., Gómez-Pastor, R., Larsson, C. et al. Fermentative capacity of dry active wine yeast requires a specific oxidative stress response during industrial biomass growth. Appl Microbiol Biotechnol 81, 951–960 (2009). https://doi.org/10.1007/s00253-008-1722-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-008-1722-9

Keyword

Navigation