Adaptive evolution of baker's yeast in a dough-like environment enhances freeze and salinity tolerance

Microbial Biotechnology

Volumn 3, Issue 2, 2010, Pages 210-221

  Aguilera, Jaime ^a,b   Andreu, Pasqual ^a   Randez Gil, Francisca ^a   Prieto, Jose Antonio ^a  

^a INSTITUTO DE AGROQUÍMICA Y TECNOLOGÍA DE ALIMENTOS CSIC   (Spain)

^b EUROPEAN FOOD SAFETY AUTHORITY   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON; CARBON DIOXIDE; GLUCOSE; SODIUM CHLORIDE; SORBITOL;

ARTICLE; CARBON SOURCE; CONTROLLED STUDY; DOUGH; ENVIRONMENT; EVOLUTIONARY ADAPTATION; EXPERIMENTAL DESIGN; FLOUR; FREEZING TOLERANCE; GLUCONEOGENESIS; GROWTH RATE; HYPOTHESIS; LIQUID; LOW TEMPERATURE; NONHUMAN; PHENOTYPE; PLOIDY; POPULATION; SACCHAROMYCES CEREVISIAE; SALT TOLERANCE; YEAST; YEAST CELL;

ADAPTATION, BIOLOGICAL; COLD TEMPERATURE; FOOD MICROBIOLOGY; SACCHAROMYCES CEREVISIAE; SALINITY; SERIAL PASSAGE; SODIUM CHLORIDE; SORBITOL; STRESS, PHYSIOLOGICAL;

EID: 77953602249     PISSN: 17517907     EISSN: 17517915     Source Type: Journal    
DOI: 10.1111/j.1751-7915.2009.00136.x     Document Type: Article

References (59)

1. Adams, J., and Oeller, P.W. (1986) Structure of evolving populations of saccharomyces cerevisiae: adaptive changes are frequently associated with sequence alterations involving mobile elements belonging to the Ty family. Proc Natl Acad Sci USA 83: 7124-7127.
2. Aguilera, J., Randez-Gil, F., and Prieto, J.A. (2007) Cold response in Saccharomyces cerevisiae: new functions for old mechanisms. FEMS Microbiol Rev 31: 327-341.
3. Attfield, P.V. (1997) Stress tolerance: the key to effective strains of industrial baker's yeast. Nat Biotechnol 15: 1351-1357.
4. Causton, H.C., Ren, B., Koh, S.S., Harbison, C.T., Kanin, E., Jennings, E.G., et al. (2001) Remodeling of yeast genome expression in response to environmental changes. Mol Biol Cell 12: 323-337.
5. Cooper, V.S., and Lenski, R.E. (2000) The population genetics of ecological specialization in evolving Escherichia coli populations. Nature 407: 736-739.
6. Cyert, M.S. (2003) Calcineurin signaling in Saccharomyces cerevisiae: how yeast go crazy in response to stress. Biochem Biophys Res Commun 311: 1143-1150.
7. Dequin, S. (2001) The potential of genetic engineering for improving brewing, wine-making and baking yeasts. Appl Microbiol Biotechnol 56: 577-588.
8. Diniz-Mendez, L., Bernardes, E., de Araujo, P.S., Panek, A.D., and Paschoalin, V.M.F. (1999) Preservation of frozen yeast cells by trehalose. Biotechnol Bioeng 65: 572-578.
9. Dixon, G.H., and Kornberg, H.L. (1959) Assay methods for key enzymes of the glyoxylate cycle. Biochem J 72: 3p.
10. Dykhuizen, D.E. (1990) Mountaineering with microbes. Nature 346: 15-16.
11. Estruch, F., and Prieto, J.A. (2003) Construction of a Trpcommercial baker's yeast strain by using food-safe-grade dominant drug resistance cassettes. FEMS Yeast Res 4: 329-338.
12. Gancedo, J.M. (1998) Yeast carbon catabolite repression. Microbiol Mol Biol Rev 62: 334-361.
13. Gancedo, J.M., and Gancedo, C. (1971) Fructose-1,6-diphosphatase, phosphofructokinase and glucose-6-phosphate dehydrogenase from fermenting and non fermenting yeasts. Arch Microbiol 76: 132-138.
14. 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 11: 3157-3164.
15. Gerstein, A.C., Chun, H.J., Grant, A., and Otto, S.P. (2006) Genomic convergence toward diploidy in Saccharomyces cerevisiae. PLoS Genet 2: e145.
16. Gerstein, A.C., McBride, R.M., and Otto, S.P. (2008) Ploidy reduction in Saccharomyces cerevisiae. Biol Lett 4: 91-94.
17. Guimarães, P.M., François, J., Parrou, J.L., Teixeira, J.A., and Domingues, L. (2008) Adaptive evolution of a lactose-consuming Saccharomyces cerevisiae recombinant. Appl Environ Microbiol 74: 1748-1756.
18. Hansen, R.J., Hinze, H., and Holzer, H. (1976) Assay of phosphoenolpyruvate carboxykinase in crude yeast extracts. Anal Biochem 74: 576-584.
19. Haro, R., Garciadeblas, B., and Rodriguez-Navarro, A. (1991) A novel P-type ATPase from yeast involved in sodium transport. FEBS Lett 291: 189-191.
20. Heer, D., and Sauer, U. (2008) Identification of furfural as a key toxin in lignocellulosic hydrolysates and evolution of a tolerant yeast strain. Microbial Biotechnol 1: 497-506.
21. Heidenreich, E. (2007) Adaptive mutation in Saccharomyces cerevisiae. Crit Rev Biochem Mol Biol 42: 285-311.
22. Hermes-Lima, M., and Storey, K.B. (1993) Antioxidant defences in the tolerance of freezing and anoxia by garter snakes. Am J Physiol 265: R646-R652.
23. Hernandez-Lopez, M.J., Prieto, J.A., and Randez-Gil, F. (2003) Osmotolerance and leavening ability in sweet and frozen sweet dough. Comparative analysis between Torulaspora delbrueckii and Saccharomyces cerevisiae baker's yeast strains. Antonie Van Leeuwenhoek 84: 125-134.
24. Higgins, V.J., Bell, P.J., Dawes, I.W., and Attfield, P.V. (2001) Generation of a novel Saccharomyces cerevisiae strain that exhibits strong maltose utilization and hyperosmotic resistance using nonrecombinant techniques. Appl Environ Microbiol 67: 4346-4348.
25. Hirasawa, R., Yokoigawa, K., Isobe, Y., and Kawai, H. (2001) Improving the freeze tolerance of bakers' yeast by loading with trehalose. Biosci Biotechnol Biochem 65: 522-526.
26. Hutter, K.J., and Eipel, H. (1979) Microbial determinations by flow cytometry. J Gen Microbiol 113: 369-375.
27. Kandror, O., Bretschneider, N., Kreydin, E., Cavalieri, D., and Goldberg, A.L. (2004) Yeast adapt to near-freezing temperatures by STRE/Msn2,4-dependent induction of trehalose synthesis and certain molecular chaperones. Mol Cell 13: 771-781.
28. Kronberg, M.F., Nikel, P.I., Cerrutti, P., and Galvagno, M.A. (2007) Modelling the freezing response of baker's yeast prestressed cells: a statistical approach. J Appl Microbiol 104: 716-727.
29. Kuyper, M., Winkler, A.A., van Dijken, J.P., and Pronk, J.T. (2004) Minimal metabolic engineering of Saccharomyces cerevisiae for efficient anaerobic xylose fermentation: a proof of principle. FEMS Yeast Res 4: 655-664.
30. McEwen, J.E., Cameron, V.L., and Poyton, R.O. (1985) Rapid method for isolation and screening of cytochrome c oxidase-deficient mutants of Saccharomyces cerevisiae. J Bacteriol 161: 831-835.
31. van Maris, A.J., Geertman, J.M., Vermeulen, A., Groothuizen, M.K., Winkler, A.A., Piper, M.D., et al. (2004) Directed evolution of pyruvate decarboxylase-negative Saccharomyces cerevisiae, yielding a C2-independent, glucose-tolerant, and pyruvate-hyperproducing yeast. Appl Environ Microbiol 70: 159-166.
32. Marquez, J.A., Pascual-Ahuir, A., Proft, M., and Serrano, R. (1998) The Ssn6-Tup1 repressor complex of Saccharomyces cerevisiae is involved in the osmotic induction of HOG-dependent and -independent genes. EMBO J 17: 2543-2553.
33. Morris, G.J., Coulson, G.E., and Clarke, K.J. (1988) Freezing injury in Saccharomyces cerevisiae. The effects of growth conditions. Cryobiology 25: 471-472.
34. Murga, M.L., Cabrera, G.M., de Valdez, G.F., Disalvo, A., and Seldes, A.M. (2000) Influence of growth temperature on cryotolerance and lipid composition of Lactobacillus acidophilus. J Appl Microbiol 88: 342-348.
35. Myers, D.K., and Attfield, P.V. (1999) Intracellular concentration of exogenous glycerol in Saccharomyces cerevisiae provides for improved leavening of frozen sweet doughs. Food Microbiol 16: 45-51.
36. Niederacher, D., and Entian, K.-D. (1987) Isolation and caracterization of the regulatory HEX2 gene necessary for glucose repression in yeast. Mol Gen Genet 206: 505-509.
37. Okada, H., and Halvorson, H.O. (1964) Uptake of alphathioethyl- glucopyranoside by Saccharomyces cerevisiae. 1. The genetic control of facilitated diffusion and active transport. Biochim Biophys Acta 82: 538-542.
38. Panadero, J., Randez-Gil, F., and Prieto, J.A. (2005a) Validation of a flour-free model dough system for throughput studies of baker's yeast. Appl Environ Microbiol 71: 1142-1147.
39. Panadero, J., Randez-Gil, F., and Prieto, J.A. (2005b) Heterologous expression of type I antifreeze peptide GS-5 in baker's yeast increases freeze tolerance and provides enhanced gas production in frozen dough. J Agric Food Chem 53: 9966-9970.
40. Panadero, J., Pallotti, C., Rodríguez-Vargas, S., Randez-Gil, F., and Prieto, J.A. (2006) A downshift in temperature activates the high osmolarity glycerol (HOG) pathway, which determines freeze tolerance in Saccharomyces cerevisiae. J Biol Chem 281: 4638-4645.
41. Panadero, J., Hernández-López, M.J., Prieto, J.A., and 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.
42. Paquin, C., and Adams, J. (1983) Frequency of fixation of adaptive mutations is higher in evolving diploid than haploid yeast populations. Nature 302: 495-500.
43. Park, J.I., Grant, C.M., Attfield, P.V., and Dawes, I.W. (1997) The freeze-thaw stress response of the yeast Saccharomyces cerevisiae is growth phase specific and is controlled by nutritional state via the RAS-cyclic AMP signal transduction pathway. Appl Environ Microbiol 63: 3818-3824.
44. Patnaik, R. (2008) Engineering complex phenotypes in industrial strains. Biotechnol Prog 24: 38-47.
45. Querol, A., Fernández-Espinar, M.T., del Olmo, M., and Barrio, E. (2003) Adaptive evolution of wine yeast. Int J Food Microbiol 86: 3-10.
46. Randez-Gil, F., Sanz, P., and Prieto, J.A. (1999) Engineering baker's yeast: room for improvement. Trends Biotechnol 17: 237-244.
47. Randez-Gil, F., Aguilera, J., Codón, A., Rincón, A.M., Estruch, F., and Prieto, J.A. (2003) Baker's yeast: challenges and future prospects. In Functional Genetics of Industrial Yeasts. de Winde, J.H. (ed.). Heidelberg, Germany: Springer-Verlag, pp. 57-97.
48. Rodriguez-Vargas, S., Estruch, F., and Randez-Gil, F. (2002) Gene expression analysis of cold and freeze stress in baker's yeast. Appl Environ Microbiol 68: 3024-3030.
49. Rodriguez-Vargas, S., Sánchez-García, A., Martínez-Rivas, J.M., Prieto, J.A., and Randez-Gil, F. (2007) Fluidization of membrane lipids enhances the tolerance of Saccharomyces cerevisiae to freezing and salt stress. Appl Environ Microbiol 73: 110-116.
50. Rusnak, F., and Mertz, P. (2000) Calcineurin: form and function. Physiol Rev 80: 1483-1521.
51. Stathopoulos, A.M., and Cyert, M.S. (1997) Calcineurin acts through the CRZ1/TCN1-encoded transcription factor to regulate gene expression in yeast. Genes Dev 11: 3432-3444.
52. Tai, S.L., Daran-Lapujade, P., Walsh, M.C., Pronk, J.T., and Daran, J.M. (2007) Acclimation of Saccharomyces cerevisiae to low temperature: a chemostat-based transcriptome analysis. Mol Biol Cell 18: 5100-5112.
53. Tanghe, A., van Dijck, P., Dumortier, F., Teunissen, A., Hohmann, S., and Thevelein, J.M. (2002) Aquaporin expression correlates with freeze tolerance in baker's yeast, and overexpression improves freeze tolerance in industrial strains. Appl Environ Microbiol 68: 5981-5989.
54. Tanghe, A., van Dijck, P., and Thevelein, J.M. (2003) Determinants of freeze tolerance in microorganisms, physiological importance, and biotechnological applications. Adv Appl Microbiol 53: 129-176.
55. Thammavongs, B., Panoff, J.M., and Guéguen, M. (2000) Phenotypic adaptation to freeze-thaw stress of the yeastlike fungus Geotrichum candidum. Int J Food Microbiol 60: 99-105.
56. Wolfe, J., and Bryant, G. (1999) Freezing, crying, and/or vitrification of membrane-solute-water systems. Cryobiology 39: 103-129.
57. Wright, B.E. (2004) Stress-directed adaptive mutations and evolution. Mol Microbiol 52: 643-650.
58. Yoshimoto, H., Saltsman, K., Gasch, A.P., Li, H.X., Ogawa, N., Botstein, D., et al. (2002) Genome-wide analysis of gene expression regulated by the calcineurin/Crz1p signaling pathway in Saccharomyces cerevisiae. J Biol Chem 277: 31079-31088.
59. Zeyl, C. (2005) The number of mutations selected during adaptation in a laboratory population of Saccharomyces cerevisiae. Genet 169: 1825-1831.