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Stress tolerance: The key to effective strains of industrial baker's yeast

Abstract

Application of yeasts in traditional biotechnologies such as baking, brewing, distiller's fermentations, and wine making, involves them in exposure to numerous environmental stresses. These can be encountered in concert and sequentially. Yeast exhibit a complex array of stress responses when under conditions that are less than physiologically ideal. These responses involve aspects of cell sensing, signal transduction, transcriptional and posttranslational control, protein-targeting to organelles, accumulation of protectants, and activity of repair functions. The efficiency of these processes in a given yeast strain determines its robustness, and to a large extent, whether it is able to perform to necessary commercial standards in industrial processes. This article reviews aspects of stress and stress response in the context of baker's yeast manufacturing and applications, and discusses the potential for improving the general robustness of industrial baker's yeast strains, in relation to physiological and genetic manipulations.

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References

  1. Evans, I.H. 1990. Yeast strains for baking, pp. 13–45 in Yeast technology. Spencer, J.F.T. and Spencer, D.M. (eds.). Springer-Verlag, Berlin, Germany.

    Google Scholar 

  2. Trivedi, N.B. 1986. Bakers' yeast. CRC Crit. Rev. Biotechnol. 4: 75–109.

    Article  Google Scholar 

  3. Chen, S.L. and Chiger, M. 1985. Production of baker's yeast, pp. 429–462 in Comprehensive biotechnology. Blanch, H.W., Drew, S., and Wang, D.I.C. (eds.). Pergamon Press, New York.

    Google Scholar 

  4. Reed, G. and Nagodawithana, T.W. 1991. Yeast technology, 2nd edition. Van Nostrand Reinhold, New York.

    Google Scholar 

  5. Beudeker, R.F., Van Dam, H.W., Van Der Plaat, J.B. and Vellenga, K. 1990. Developments in baker's yeast production, pp. 103–146 in Yeast biotechnology and biocatalysis. Verachtert, H. and De Mot, R. (eds.). Marcel Dekker, Inc., New York.

    Google Scholar 

  6. Yokota, M. and Fagerson, I.S. 1971. The major volatile components of cane molasses. J. Food Sci. 26: 1091–1094.

    Google Scholar 

  7. Chen, S.L. and Gutmanis, F. 1983. Process for the production of osmotolerant yeast. US patent no. 4,420,563.

  8. Stear, C.A. 1990. Handbook of breadmaking technology. Elsevier Applied Sciences, New York.

    Google Scholar 

  9. Pyler, E.J. 1988. Baking science and technology, 3rd edition. Sosland Publishing Co., Kansas City, MO.

    Google Scholar 

  10. Myers, D.K., Lawlor, D.T.M. and Attfield, P.V. 1997. Influence of invertase activity and glycerol synthesis and retention on fermentation of media with high sugar concentration by Saccharomyces cerevisiae. Appl. Environ. Microbiol. 63: 145–150.

    CAS  PubMed  PubMed Central  Google Scholar 

  11. Welch, W.J. 1993. How cells respond to stress. Sci. Amer. 268: 5, 34–41.

    Article  Google Scholar 

  12. Young, R.A. and Elliot, T.J. 1989. Stress proteins, infection and immune surveillance. Cell 59: 5–8.

    Article  CAS  Google Scholar 

  13. Ruis, H. 1997. Yeast stress responses: achievements, goals and a look beyond yeast, pp. 231–247 in Yeast stress responses. Hohmann, S. and Mager, W.H. (eds.). R.G. Landes Co., Austin, TX.

    Google Scholar 

  14. Thevelein, J.M. 1994. Signal transduction in yeast. Yeast 10: 1753–1790.

    Article  CAS  Google Scholar 

  15. de Winde, J.H., Thevelein, J.M., and Winderickx, J. 1997. From feast to famine: adaptation to nutrient depletion in yeast, pp. 7–52 in Yeast stress responses. Hohmann, S. and Mager, W.H. (eds.). R.G. Landes Co., Austin, TX.

    Google Scholar 

  16. Werner-Washburne, M., Braun, E., Johnston, G.C. and Singer, R.A. 1993. Stationary phase in the yeast Saccharomyces cerevisiae. Microbiol. Rev. 57: 383–401.

    CAS  PubMed  PubMed Central  Google Scholar 

  17. Fuge, E.K. and Werner-Washburne, M. 1997. Stationary phase in the yeast Saccharomyces cerevisiae, pp. 53—74 in Yeast stress responses. Hohmann, S. and Mager, W.H. (eds.). R.G. Landes Co., Austin, TX.

    Google Scholar 

  18. Siderius, M. and Mager, W.H. 1997. General stress response: in search of a common denominator, pp. 213–230 in Yeast Stress Responses. Hohmann, S. and Mager, W.H. (eds.). R.G. Landes Co., Austin, TX.

    Google Scholar 

  19. Panaretou, B. and Piper, P.W., 1990. Plasma-membrane ATPase action affects several stress tolerances of Saccharomyces cerevisiae and Schizosaccharomyces pombe as well as the extent of duration of the heat shock response. J. Gen. Microbiol. 136: 1763–1770.

    Article  CAS  Google Scholar 

  20. Coote, P.J., Cole, M.B. and Jones, M.V. 1991. Induction of increased thermotolerance in Saccharomyces cerevisiae may be triggered by a mechanism involving intracellular pH. J. Gen. Microbiol. 137: 1701–1708.

    Article  CAS  Google Scholar 

  21. Piper, P.W. 1993. Molecular events associated with acquisition of heat tolerance by the yeast Saccharomyces cerevisiae. FEMS Microbiol. Revs. 11: 339–356.

    Article  CAS  Google Scholar 

  22. Coote, P.J., Jones, M.V., Seymour, I.J., Rowe, D.L., Ferdinando, D.R., McArthur, A.J. and Cole, M.B. 1994. Activity of the plasma membrane H+−ATPase is a key physiological determinant of thermotolerance in Saccharomyces cerevisiae. Microbiol. 140: 1881–1890.

    Article  CAS  Google Scholar 

  23. Valle, E., Bergillos, L., Gascón, S., Parra, F. and Ramos, S. 1986. Trehalase activation in yeasts is mediated by an internal acidification. Eur. J. Biochem. 154: 247–251.

    Article  CAS  Google Scholar 

  24. Coote, P.J., Jones, M.V., Edgar, K. and Cole, M.B. 1992. TPK gene products mediate cAMP-independent thermotolerance in Saccharomyces cerevisiae. J. Gen. Microbiol. 138: 2551–2557.

    Article  CAS  Google Scholar 

  25. Costa, V., Amorim, M.A., Reis, E., Quintanilha, A. and Moradas-Ferreira, P. 1997. Mitochondrial superoxide dismutase is essential for ethanol tolerance of Saccharomyces cerevisiae in post-diauxic phase. Microbiol. 143: 1649–1656.

    Article  CAS  Google Scholar 

  26. Steels, E.L., Learmonth, R.P. and Watson, K. 1994. Stress tolerance and membrane lipid unsaturation in Saccharomyces cerevisiae grown aerobically or anaerobically. Microbiol. 140: 569–576.

    Article  CAS  Google Scholar 

  27. Krems, B., Charizanis, C. and Entian, K.-D. 1995. Mutants of Saccharomyces cerevisiae sensitive to oxidative and osmotic stress. Curr. Genet. 27: 427–434.

    Article  CAS  Google Scholar 

  28. Davidson, J.F., Whyte, B., Bissinger, P.H. and Schiestl, R.H. 1996. Oxidative stress is involved in heat-induced cell death in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 93: 5116–5121.

    Article  CAS  Google Scholar 

  29. Lewis, J.G., Learmonth, R.P., Attfield, R.V. and Watson, K. 1997. Stress co-tolerance and trehalose content in baking strains of Saccharomyces cerevisiae. J. Ind. Microbiol. Biotechnol. 18: 30–36.

    Article  CAS  Google Scholar 

  30. Moradas-Ferreira, P., Costa, V., Piper, P. and Mager, M. 1996. The molecular defence against reactive oxygen species in yeast. Mol. Microbiol. 19: 651–658.

    Article  CAS  Google Scholar 

  31. Brown, A.D. 1978. Compatible solutes and extreme water stress in eukaryotic microorganisms. Adv. Microb. Physiol. 17: 181–242.

    Article  CAS  Google Scholar 

  32. Blomberg, A. and Adler, L. 1992. Physiology of osmotolerance in fungi. Adv. Microb. Physiol. 33: 143–212.

    Google Scholar 

  33. Hohmann, S. 1997. Shaping up: The response of yeast to osmotic stress, pp. 101–145 in Yeast Stress Responses. Hohmann, S. and Mager, W.H. (eds.). R.G. Landes Co., Austin, TX.

    Google Scholar 

  34. Varela, J.C.S. and Mager, W.H. 1996. Response of Saccharomyces cerevisiaeto changes in external osmolarity. Microbiology. 142: 721–731.

    Article  CAS  Google Scholar 

  35. Beker, M.J. and Rapoport, A.I. 1987. Conservation of yeasts by dehydration. Adv. Biochem. Eng. Biotechnol. 35: 127–171.

    Google Scholar 

  36. Rapoport, A.I., Khrustaleva, G.M., Ya Chamanis, G. and Beker, M.E. 1995. Yeast anhydrobiosis: permeability of the plasma membrane. Mikrobiologiya 64: 275–278.

    CAS  Google Scholar 

  37. Mazur, P. 1970. Cryobiology: the freezing of biological systems. Science 168: 939–949.

    Article  CAS  Google Scholar 

  38. Crowe, J.H., Carpenter, J.F., Crowe, L.M. and Anchordoguy, T.J. 1990. Are freezing and dehydration similar stress vectors? A comparison of modes of interaction of stabilizing solutes with biomolecules. Cryobiology 27: 219–231.

    Article  CAS  Google Scholar 

  39. Grout, B., Morris, J. and McLellan, M. 1990. Cryopreservation and the maintenance of cell lines. Trends Biotechnol. 8: 293–297.

    Article  CAS  Google Scholar 

  40. Hatano, S., Udou, M., Koga, N., Honjoh, K.-I. and Miyamoto, T. 1996. Impairment of the glycolytic system and actin in baker's yeast during frozen storage. Biosci. Biotech. Biochem. 60: 61–64.

    Article  CAS  Google Scholar 

  41. Beker, M.J., Blumbergs, J.E., Ventina, E.J. and Rapoport, A.I. 1984. Characteristics of cellular membranes at rehydration of dehydrated yeast Saccharomyces cerevisiae. Eur. J. Appl. Microbiol. Biotechnol. 19: 347–352.

    Google Scholar 

  42. Mager, W.H. and De Kruijff, A.J.J. 1995. Stress-induced transcriptional activation. Microbiol. Rev. 59: 506–531.

    CAS  PubMed  PubMed Central  Google Scholar 

  43. Ruis, H. and Schüller, C. 1995. Stress signalling in yeast. Bioessays 17: 959–965.

    Article  CAS  Google Scholar 

  44. Sorger, P.K. and Pelham, H.R.B. 1988. Yeast heat shock factor is an essential DNA-binding protein that exhibits temperature dependent phosphorylation. Cell 54: 855–864.

    Article  CAS  Google Scholar 

  45. Martinez-Pastor, M.T., Marchler, G., Schüller, C., Marchler-Bauer, A., Ruis, H. and Estruch, F., 1996. Saccharomyces cerevisiae zinc finger proteins Msn2p and Msn4p are required for transcriptional induction through the stress response element (STRE). EMBO J. 15: 2227–2235.

    Article  CAS  Google Scholar 

  46. Schmitt, A.P. and McEntee, K., 1996. MSN2p, a zinc finger DNA-binding protein, is the transcriptional activator of the multistress response in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 93: 5777–5782.

    Article  CAS  Google Scholar 

  47. Bossier, P., Fernandes, L., Rocha, D. and Rodrigues-Pousada, C. 1993. Overexpression of YAP2, coding for a new yAP protein, and YAP1 in Saccharomyces cerevisiae alleviates growth inhibition caused by 1,10-phenanthroline. J. Biol. Chem. 268: 23640–23645.

    CAS  PubMed  Google Scholar 

  48. Gounalaki, N. and Thireos, G., 1994. Yap1p, a yeast transcriptional activator that mediates multidrug resistance, regulates metabolic stress response. EMBO J. 13: 4036–4041.

    Article  CAS  Google Scholar 

  49. Lindquist, S. and Craig, E. 1988. The heat shock proteins. Annu. Rev. Genet. 22: 631–677.

    Article  CAS  Google Scholar 

  50. Parsell, D.A. and Lindquist, S. 1993. The function of heat shock proteins in stress tolerance: degradation and reactivation of damaged proteins. Annu. Rev. Genet. 27: 437–496.

    Article  CAS  Google Scholar 

  51. Piper, P. 1997. The yeast heat shock response, pp. 75–99 in Yeast stress responses. Hohmann, S. and Mager, W.H. (eds.). R.G. Landes Co., Austin, TX.

    Google Scholar 

  52. Sanchez, Y. and Lindquist, S. 1990. HSP104 is required for induced thermotolerance. Science 248: 1112–1115.

    Article  CAS  Google Scholar 

  53. Santoro, N. and Thiele, D. 1997. Oxidative stress responses in the yeast Saccharomyces cerevisiae, pp. 171–211 in Yeast stress responses.Hohmann, S. and Mager, W.H. (eds.). R.G. Landes Co., Austin, TX.

    Google Scholar 

  54. Serrano, R., M´rquez, J.A. and Rios, G. 1997. Crucial factors in salt stress tolerance, pp. 147–169 in Yeast stress responses, Hohmann, S. and Mager, W.H. (eds.). R.G. Landes Co., Austin, TX.

    Google Scholar 

  55. Mendoza, I., Quintero, F.J., Bressan, R.A., Hasegawa, P.M. and Pardo, J.M. 1996. Activated calcineurin confers high tolerance to ion stress and alters budding pattern and cell morphology of yeast cells. J. Biol. Chem. 38: 23061–23067.

    Article  Google Scholar 

  56. Bogulslawski, G. 1992. PBS2, a yeast gene encoding a putative protein kinase, interacts with the RAS2pathway and affects osmotic sensitivity in Saccharomyces cerevisiae. J. Gen. Microbiol. 138: 2425–2432.

    Article  Google Scholar 

  57. Brewster, J.L., de Valoir, T., Dwyer, N.D., Winter, E., and Gustin, M.C. 1993. An osmosensing signal transduction pathway in yeast. Science 259: 1760–1763.

    Article  CAS  Google Scholar 

  58. Schüller, C., Brewster, J.L., Alexander, M.R., Gustin, M.C. and Ruis, H. 1994. The HOG pathway controls osmotic regulation of transcription via the stress response element (STRE) of the Saccharomyces cerevisiae CTT1gene. EMBO J. 13: 4382–4389.

    Article  Google Scholar 

  59. Gaxiola, R., de Larrinoa, I.F., Villalba, J.M., and Serrano, R. 1992. A novel and conserved salt-induced protein is an important determinant of salt tolerance in yeast. EMBO J. 9: 3157–3164.

    Article  Google Scholar 

  60. Brown, A.D. and Edgley, M. 1980. Osmoregulation in yeast, pp. 75–90 in Genetic Engineering of Osmoregulation, Rains, D.W., Valentine, R.C. and Hollaender, A. (eds.). Plenum Press, New York.

    Chapter  Google Scholar 

  61. Albertyn, J., Hohmann, S., Thevelein, J.M. and Prior, B.A. 1994. GPD1, which encodes glycerol-3-phosphate dehydrogenase, is essential for growth under osmotic stress in Saccharomyces cerevisiae, and its expression is regulated by the high-osmolarity glycerol response pathway. Mol. Cell. Biol. 14: 4135–4144.

    Article  CAS  Google Scholar 

  62. Luyten, K., Albertyn, J., Skibbe, W.F., Prior, B.A., Ramos, J., Thevelein, J.M. and Hohmann, S., 1995. Fps1, a yeast member of the MIP family of cannel proteins, is a facilitator for glycerol uptake and efflux and is inactive under osmotic stress. EMBO J. 14: 1360–1371.

    Article  CAS  Google Scholar 

  63. Hohmann, S. and Thevelein, J.M. 1994. Souches de levures transformées de manière à posséder une résistance au stress et/ou un pouvoir fermentatif améloiré. European patent no. EP0577915A1.

  64. Attfield, P.V., Kletsas, S. and Hazell, B.W. 1994. Concomitant appearance of intrinsic thermotolerance and storage of trehalose in Saccharomyces cerevisiae during early respiratory phase of bacth culture is CIF1-dependent. Microbiology 140: 2625–2632.

    Article  Google Scholar 

  65. De Virgilio, C., Hottiger, T., Dominguez, J., Boller, T. and Wiemken, A. 1994. The role of trehalose synthesis for acquisition of thermotolerance I Genetic evidence that trehalose is a thermoprotectant. Eur. J. Biochem. 219: 179–186.

    Article  CAS  Google Scholar 

  66. Van Dijck, P., Colavizza, D., Smet, P. and Thevelein, J.M. 1995. Differential importance of trehalose in stress resistance in fermenting and nonfermenting Saccharomyces cerevisiae cells. Appl. Environ. Microbiol. 61: 109–115.

    CAS  PubMed  PubMed Central  Google Scholar 

  67. Osinga, K.A., Renniers, A.C.H.M., Welbergen, J.W., Roobol, R.H. and van der Wilden, W. 1989. Maltose fermentation in Saccharomyces cerevisiae. Yeast 5: S207–S212.

    CAS  Google Scholar 

  68. Londesborough, J. and Vuorio, O. 1995. Method to increase the trehalose content of organisms by transforming them with the structural genes for the short and long chains of yeast trehalose synthase. US patent no. 5,422,254.

  69. Klionsky, D., Holzer, H. and Struelle, M. 1997. Stress tolerant yeast mutants. International patent no. WO97/01626.

  70. Dujon, B. 1996. The yeast genome project: What did we learn? Trends Genet. 12: 263–270.

    Article  CAS  Google Scholar 

  71. Myers, D.K., Joseph, V.M., Pehm, S., Galvagno, M. and Attfield, P.V. 1997. Loading of Saccharomyces cerevisiae with glycerol leads to enhanced fermentation in sweet bread doughs. Food Microbiol. In press.

  72. Evans, R.J. and Attfield, P.V. 1989. Genetic engineering of yeasts: principles and applications, pp. 33–60 in Biotechnology and the food industry, Rogers, P.L. and Fleet, G.H. (eds.). Gordon and Breach Science Publishers, New York.

    Google Scholar 

  73. Oliver, S.G. 1991. “Classical” yeast biotechnology, pp. 213–248 in Saccharomyces, Biotechnology handbooks, vol. 4 Tuite, M.F. and Oliver, S.G. (eds.). Plenum Press, New York.

    Chapter  Google Scholar 

  74. Oliver, S.G. 1997. Yeast as a navigational aid in genome analysis. Microbiol 143: 1483–1487.

    Article  CAS  Google Scholar 

  75. Oliver, S.G. 1996. From DNA sequence to biological function. Nature 379: 597–600.

    Article  CAS  Google Scholar 

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Attfield, P. Stress tolerance: The key to effective strains of industrial baker's yeast. Nat Biotechnol 15, 1351–1357 (1997). https://doi.org/10.1038/nbt1297-1351

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