Mechanisms of yeast stress tolerance and its manipulation for efficient fuel ethanol production

Journal of Biotechnology

Volumn 144, Issue 1, 2009, Pages 23-30

  Zhao, X Q ^a   Bai, F W ^a  

^a DALIAN UNIVERSITY OF TECHNOLOGY   (China)

Author keywords

Ethanol fermentation; Saccharomyces cerevisiae; Stress tolerance

Indexed keywords

DEFENSE MECHANISM; ETHANOL FERMENTATION; ETHANOL INHIBITION; ETHANOL PRODUCTION; FUEL ETHANOL; GENOME SHUFFLING; HIGH GRAVITY; HIGH TEMPERATURE; IN-DEPTH UNDERSTANDING; LATEST DEVELOPMENT; LIGNOCELLULOSIC BIOMASS; OSMOTIC PRESSURE; PRE-TREATMENT; SACCHAROMYCES CEREVISIAE; STRESS RESPONSE; STRESS TOLERANCE; YEAST CELL; YEAST STRAIN;

BIOMASS; CELLULOSIC ETHANOL; ELASTICITY; ETHANOL; FERMENTATION; MACHINERY; SUGAR (SUCROSE); SUGARS;

YEAST;

ALCOHOL; AMINO ACID DERIVATIVE; BIOFUEL; LIGNOCELLULOSE; SUGAR; ZINC;

AERATION; ALCOHOL PRODUCTION; AMINO ACID SYNTHESIS; AMINO ACID TRANSPORT; BIOCHEMISTRY; BIOENGINEERING; BIOSYNTHESIS; CELL MEMBRANE; CELL MEMBRANE PERMEABILITY; CELL STRESS; CELL VIABILITY; CELL WALL; CHEMICAL COMPOSITION; CULTURE MEDIUM; ENERGY METABOLISM; ENERGY RESOURCE; ENZYME ACTIVITY; FERMENTATION; FUNGAL BIOMASS; FUNGAL CELL; FUNGAL GENE; FUNGAL GENOME; FUNGAL METABOLISM; FUNGAL STRAIN; GENE FUNCTION; GENE OVEREXPRESSION; GENETIC ENGINEERING; GENETIC RECOMBINATION; GENETIC TRANSCRIPTION; HIGH TEMPERATURE PROCEDURES; MITOCHONDRIAL RESPIRATION; MOLECULAR EVOLUTION; NONHUMAN; OSMOTIC PRESSURE; PRIORITY JOURNAL; PROCESS OPTIMIZATION; PROMOTER REGION; PROTEOMICS; REVIEW; SACCHAROMYCES CEREVISIAE; STRESS; YEAST;

ADAPTATION, PHYSIOLOGICAL; BIOFUELS; ETHANOL; GENETIC ENGINEERING; SACCHAROMYCES CEREVISIAE; STRESS, PHYSIOLOGICAL;

SACCHAROMYCES CEREVISIAE;

EID: 70349775063     PISSN: 01681656     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jbiotec.2009.05.001     Document Type: Review

References (92)

1. +-ATPase activity and the lipid composition of the plasma membrane in different wine yeast strains. Int. J. Food Microbiol. 110 (2006) 34-42
2. Alexandre H., Ansanay-Galeote V., Dequin S., and Blondin B. Global gene expression during short-term ethanol stress in Saccharomyces cerevisiae. FEBS Lett. 498 (2001) 98-103
3. Alfenore S., Molina-Jouve C., Guillouet S.E., Uribelarrea J.L., Goma G., and Benbadis L. Improving ethanol production and viability of Saccharomyces cerevisiae by a vitamin feeding strategy during fed-batch process. Appl. Microbiol. Biotechnol. 60 (2002) 67-72
4. Alfenore S., Cameleyre X., Benbadis L., Bideaux C., Uribelarrea J.L., Goma G., Molina-Jouve C., and Guillouet S.E. Aeration strategy: a need for very high ethanol performance in Saccharomyces cerevisiae fed-batch process. Appl. Microbiol. Biotechnol. 63 (2004) 537-542
5. Almeida J.R.M., Modig T., Petersson A., Hahn-Hagerdal B., Liden G., and Gorwa-Grauslund M.F. Increased tolerance and conversion of inhibitors in lignocellulosic hydrolysates by Saccharomyces cerevisiae. J. Chem. Technol. Biotechnol. 82 (2007) 340-349
6. Alper H., Moxley J., Nevoigt E., Fink G.R., and Stephanopoulos G. Engineering yeast transcription machinery for improved ethanol tolerance and production. Science 314 (2006) 1565-1568
7. Attfield P.V. Stress tolerance: the key to effective strains of industrial baker's yeast. Nat. Biotechnol. 15 (1997) 1351-1357
8. Bai F.W., Chen L.J., Zhang Z., Anderson W.A., and Moo-Young M. Continuous ethanol production and evaluation of yeast cell lysis and viability loss under very high gravity medium conditions. J. Biotechnol. 110 (2004) 287-293
9. Bai F.W., Anderson W.A., and Moo-Young M. Ethanol fermentation technologies from sugar and starch feedstocks. Biotechnol. Adv. 26 (2008) 89-105
10. Berry D.B., and Gasch A.P. Stress-activated genomic expression changes serve a preparative role for impending stress in yeast. Mol. Biol. Cell 19 (2008) 4580-4587
11. Birch R.M., and Walker G.M. Influence of magnesium ions on heat shock and ethanol stress responses of Saccharomyces cerevisiae. Enzyme Microb. Technol. 26 (2000) 678-687
12. Cakar Z.P., Seker U.O., Tamerler C., Sonderegger M., and Sauer U. Evolutionary engineering of multiple-stress resistant Saccharomyces cerevisiae. FEMS Yeast Res. 5 (2005) 569-578
13. Causton H.C., Ren B., Koh S.S., Harbison C.T., Kanin E., Jennings E.G., Lee T.I., True H.L., Lander E.S., and Young R.A. Remodeling of yeast genome expression in response to environmental changes. Mol. Biol. Cell 12 (2001) 323-337
14. Chandrasena G., and Walker G.M. Use of response surface to investigate metal ion interaction in yeast fermentations. J. Am. Soc. Brew. Chem. 55 (1997) 24-29
15. Chatterjee M.T., Khalawan S.A., and Curran B.P.G. Cellular lipid composition influences stress activation of the yeast general stress response element (STRE). Microbiology 146 (2000) 844-877
16. Chen H., and Fink G.R. Feedback control of morphogenesis in fungi by aromatic alcohols. Genes Dev. 20 (2006) 1150-1161
17. Chi Z., Kohlwein S.D., and Paltauf F. Role of phosphatidylinositol (PI) in ethanol production and ethanol tolerance by a high ethanol producing yeast. J. Ind. Microbiol. Biotechnol. 22 (1999) 58-63
18. Costa V., Reis E., Quintanilha A., and Moradas-Ferreira P. Acquisition of ethanol tolerance in Saccharomyces cerevisiae: the key role of the mitochondrial superoxide dismutase. Arch. Biochem. Biophys. 300 (1993) 608-614
19. Cot M., Loret M.O., Francois J., and Benbadis L. Physiological behaviour of Saccharomyces cerevisiae in aerated fed-batch fermentation for high level production of bioethanol. FEMS Yeast Res. 7 (2007) 22-32
20. De Nicola R., Hazelwood L.A., De Hulster E.A., Walsh M.C., Knijnenburg T.A., Reinders M.J., Walker G.M., Pronk J.T., Daran J.M., and Daran-Lapujade P. Physiological and transcriptional responses of Saccharomyces cerevisiae to zinc limitation in chemostat cultures. Appl. Environ. Microbiol. 73 (2007) 7680-7692
21. Dombek K.M., and Ingram L.O. Magnesium limitation and its role in apparent toxicity of ethanol during yeast fermentation. Appl. Environ. Microbiol. 52 (1986) 975-981
22. Domingues L., Vicente A.A., Lima N., and Teixeira J.A. Applications of yeast flocculation in biotechnological processes. Biotechnol. Bioproc. Eng. 5 (2000) 288-305
23. Du X., and Takagi H. N-Acetyltransferase Mpr1 confers ethanol tolerance on Saccharomyces cerevisiae by reducing reactive oxygen species. Appl. Microbiol. Biotechnol. 75 (2007) 1343-1351
24. Espinazo-Romeu M., Cantoral J.M., Matallana E., and Aranda A. Btn2p is involved in ethanol tolerance and biofilm formation in flor yeast. FEMS Yeast Res. 8 (2008) 1127-1136
25. Fischer C.R., Klein-Marcuschamer D., and Stephanopoulos G. Selection and optimization of microbial hosts for biofuels production. Metab. Eng. 10 (2008) 295-304
26. Fujita K., Matsuyama A., Kobayashi Y., and Iwahashi H. The genome-wide screening of yeast deletion mutants to identify the genes required for tolerance to ethanol and other alcohols. FEMS Yeast Res. 6 (2006) 744-750
27. Galhardo R.S., Hastings P.J., and Rosenberg S.M. Mutation as a stress response and the regulation of evolvability. Crit. Rev. Biochem. Mol. Biol. 42 (2007) 399-435
28. Gasch A.P., Spellman P.T., Kao C.M., Carmel-Harel O., Eisen M.B., Storz G., Botstein D., and Brown P.O. Genomic expression programs in the response of yeast cells to environmental changes. Mol. Biol. Cell 11 (2000) 4241-4257
29. Gibson B.R., Lawrence S.J., Leclaire J.P., Powell C.D., and Smart K.A. Yeast responses to stresses associated with industrial brewery handling. FEMS Microbiol. Rev. 31 (2007) 535-569
30. Ge X.M., Zhao X.Q., and Bai F.W. On-line monitoring and characterization of flocculating yeast cell flocs during continuous ethanol fermentation. Biotechnol. Bioeng. 90 (2005) 523-531
31. Gorsich S.E., Dien B.S., Nichols N.N., Slininger P.J., Liu Z.L., and Skory C.D. Tolerance to furfural-induced stress is associated with pentose phosphate pathway genes ZWF1, GND1, RPE1 and TKL1 in Saccharomyces cerevisiae. Appl. Microbiol. Biotechnol. 71 (2006) 339-349
32. Guimaraes P.M., and Londesborough J. The adenylate energy charge and specific fermentation rate of brewer's yeasts fermenting high- and very high-gravity worts. Yeast 25 (2008) 47-58
33. Guimarães P.M., François J., Parrou J.L., Teixeira J.A., and Domingues L. Adaptive evolution of a lactose-consuming Saccharomyces cerevisiae recombinant. Appl. Environ. Microbiol. 74 (2008) 1748-1756
34. Hirasawa T., Yoshikawa K., Nakakura Y., Nagahisa K., Furusawa C., Katakura Y., Shimizu H., and Shioya S. Identification of target genes conferring ethanol stress tolerance to Saccharomyces cerevisiae based on DNA microarray data analysis. J. Biotechnol. 131 (2007) 34-44
35. Hu C.K., Bai F.W., and An L.J. Protein amino acid composition of plasma membranes affects membrane fluidity and thereby ethanol tolerance in a self-flocculating fusant of Schizosaccharomyces pombe and Saccharomyces cerevisiae. Chin. J. Biotechnol. 21 (2005) 809-813
36. Hu C.K., Bai F.W., and An L.J. Effect of flocculence of a self-flocculating yeast on its tolerance to ethanol and the mechanism. Chin. J. Biotechnol. 21 (2005) 123-128
37. 2+ via reduction in plasma membrane permeability. Biotechnol. Lett. 25 (2003) 1191-1194
38. Hu C.K., Bai F.W., and An L.J. Enhancements in ethanol tolerance of a self-flocculating yeast by calcium ion through decrease in plasmalemma permeability. Chin. J. Biotechnol. 19 (2003) 715-719
39. Hu X.H., Wang M.H., Tan T., Li J.R., Yang H., Leach L., Zhang R.M., and Luo Z.W. Genetic dissection of ethanol tolerance in the budding yeast Saccharomyces cerevisiae. Genetics 175 (2007) 1479-1487
40. Ingram L.O., and Buttke T.M. Effects of alcohols on microorganisms. Adv. Microb. Physiol. 25 (1984) 253-300
41. Jung Y.J., and Park H.D. Antisense-mediated inhibition of acid trehalase (ATH1) gene expression promotes ethanol fermentation and tolerance in Saccharomyces cerevisiae. Biotechnol. Lett. 27 (2005) 1855-1859
42. Kaino T., and Takagi H. Gene expression profiles and intracellular contents of stress protectants in Saccharomyces cerevisiae under ethanol and sorbitol stresses. Appl. Microbiol. Biotechnol. 79 (2008) 273-283
43. Klinke H.B., Thomsen A.B., and Ahring B.K. Inhibition of ethnol-producing yeast and bacteria by degradation products produced during pre-treatment of biomass. Appl. Microbiol. Biotechnol. 66 (2004) 10-26
44. Larsson S., Cassland P., and Jönsson L.J. Development of a Saccharomyces cerevisiae strain with enhanced resistance to phenolic fermentation inhibitors in lignocellulose hydrolysates by heterologous expression of laccase. Appl. Environ. Microbiol. 67 (2001) 1163-1170
45. Lei J.J., Zhao X.Q., Ge X.M., and Bai F.W. Ethanol tolerance and the variation of plasma membrane composition of yeast floc populations with different size distribution. J. Biotechnol. 131 (2007) 270-275
46. Liu Z.L. Genomic adaptation of ethanologenic yeast to biomass conversion inhibitors. Appl. Microbiol. Biotechnol. 73 (2006) 27-36
47. Maddox I.S., and Hough J.S. Effect of zinc and cobalt on yeast growth and fermentation. J. Inst. Brew. 76 (1970) 262-264
48. Marks V.D., Ho Sui S.J., Erasmus D., van der Merwe G.K., Brumm J., Wasserman W.W., Bryan J., and van Vuuren H.J. Dynamics of the yeast transcriptome during wine fermentation reveals a novel fermentation stress response. FEMS Yeast Res. 8 (2008) 35-52
49. Martin C., Marcet M., Almazan O., and Jonsson L.J. Adaptation of a recombinant xylose-utilizing Saccharomyces cerevisiae strain to a sugar-cane bagasse hydrolysate with high content of fermentation inhibitors. Bioresour. Technol. 98 (2007) 1767-1773
50. Morita Y., Nakamori S., and Takagi H. L-proline accumulation and freeze tolerance of Saccharomyces cerevisiae are caused by a mutation in the PRO1 gene encoding gamma-glutamyl kinase. Appl. Environ. Microbiol. 69 (2003) 212-219
51. Nabais R.C., Sa-Correia I., Viegas C.A., and Novais J.M. Influence of calcium ion on ethanol tolerance of Saccharomyces bayanus and alcoholic fermentation by yeasts. Appl. Environ. Microbiol. 54 (1988) 2439-2446
52. Nevoigt E. Progress in metabolic engineering of Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 72 (2008) 379-412
53. Nilsson A., Taherzadeh M.J., and Lidén G. Use of dynamic step response for control of fed-batch conversion of lignocellulosic hydrolyzates to ethanol. Biotechnology 89 (2001) 41-53
54. Palmqvist E., and Hahn-Hagerdal B. Fermentation of lignocellulosic hydrolysates. II. Inhibitors and mechanisms of inhibition. Bioresour. Technol. 74 (2000) 25-33
55. Patnaik R., Louie S., Gavrilovic V., Perry K., Stemmer W.P., Ryan C.M., and del Cardayré S. Genome shuffling of Lactobacillus for improved acid tolerance. Nat. Biotechnol. 20 (2002) 707-712
56. Pereira M.D., Eleutherio E.C., and Panek A.D. Acquisition of tolerance against oxidative stress damage in Saccharomyces cerevisiae. BMC Microbiol. 1 (2001) 11-21
57. Petersson A.J., Almeida J.R., Modig T., Karhumaa K., Hahn-Hagerdal B., Gorwa-Grauslund M.F., and Liden G. A 5-hydroxymethyl furfural reducing enzyme encoded by Saccharomyces cerevisiae ADH6 gene conveys HMF tolerance. Yeast 23 (2006) 455-464
58. Pham T.K., Chong P.K., Gan C.S., and Wright P.C. Proteomic analysis of Saccharomyces cerevisiae under high gravity fermentation conditions. J. Proteome Res. 5 (2006) 3411-3419
59. Pham T.K., and Wright P.C. The proteomic response of Saccharomyces cerevisiae in very high glucose conditions with amino acid supplementation. J. Proteome Res. 7 (2008) 4766-4774
60. Pizarro F.J., Felipe M.C., Nielsen J., and Agosin E. Growth temperature exerts differential physiological and transcriptional responses in laboratory and wine strains of Saccharomyces cerevisiae. Appl. Environ. Microbiol. 74 (2008) 6358-6368
61. Pizarro F.J., Vargas F.A., and Agosin E. A systems biology perspective of wine fermentations. Yeast 24 (2007) 977-991
62. Querol A., Fernández-Espinar M.T., del Olmo M., and Barrio E. Adaptive evolution of wine yeast. Int. J. Food Microbiol. 86 (2003) 3-10
63. Rossignol T., Dulau L., Julien A., and Blondin B. Genome-wide monitoring of wine yeast gene expression during alcoholic fermentation. Yeast 20 (2003) 1369-1385
64. Salmon J.M. Effect of sugar transport inactivation in Saccharomyces cerevisiae on sluggish and stuck enological fermentations. Appl. Environ. Microbiol. 55 (1989) 953-958
65. Santos J., Sousa M.J., Cardoso H., Inácio J., Silva S., Spencer-Martins I., and Leão C. Ethanol tolerance of sugar transport, and the rectification of stuck wine fermentations. Microbiology 154 (2008) 422-430
66. Sekine T., Kawaguchi A., Hamano Y., and Takagi H. Desensitization of feedback inhibition of the Saccharomyces cerevisiae gamma-glutamyl kinase enhances proline accumulation and freezing tolerance. Appl. Environ. Microbiol. 73 (2007) 4011-4019
67. Shi D.J., Wang C.L., and Wang K.M. Genome shuffling to improve thermotolerance, ethanol tolerance and ethanol productivity of Saccharomyces cerevisiae. J. Ind. Microbiol. Biotechnol. 36 (2009) 139-147
68. Takagi H. Proline as a stress protectant in yeast: physiological functions, metabolic regulations, and biotechnological applications. Appl. Microbiol. Biotechnol. 81 (2008) 211-223
69. Takagi H., Matsui F., Kawaguchi A., Wu H., Shimoi H., and Kubo Y. Construction and analysis of self-cloning sake yeasts that accumulate proline. J. Biosci. Bioeng. 103 (2007) 377-380
70. Takahashi T., Shimoi H., and Ito K. Identification of genes required for growth under ethanol stress using transposon mutagenesis in Saccharomyces cerevisiae. Mol. Genet. Genomics 265 (2001) 1112-1119
71. Thomas K.C., and Ingledew W.M. Fuel ethanol production: effects of free amino nitrogen on fermentation of very-high-gravity wheat mashes. Appl. Environ. Microbiol. 56 (1990) 2046-2050
72. Thomas K.C., and Ingledew W.M. Production of 21% (v/v) ethanol by fermentation of very high gravity (VHG) wheat mashes. J. Ind. Microbiol. 10 (1992) 61-68
73. Tosun A., and Ergun M. Use of experimental design method to investigate metal ion effects in yeast fermentations. J. Chem. Biotechnol. 82 (2007) 11-15
74. Trabalzini L., Paffetti A., Scaloni A., Talamo F., Ferro E., Coratza G., Bovalini L., Lusini P., Martelli P., and Santucci A. Proteomic response to physiological fermentation stresses in a wild-type wine strain of Saccharomyces cerevisiae. Biochem. J. 370 (2003) 35-46
75. Van Laere A. Trehalose, reserve and/or stress metabolite. FEMS Microbiol. Rev. 63 (1989) 201-210
76. Van Voorst F., Houghton L.J., Jonson L., Kiellan M.C., and Brant A. Genome-wide identification of genes required for growth of Saccharomyces cerevisiae under ethanol stress. Yeast 23 (2006) 351-359
77. Varela C.J., Cárdenas J., Melo F., and Agosin E. Quantitative analysis of wine yeast gene expression profiles under winemaking conditions. Yeast 22 (2005) 369-383
78. Varela J.C., Praekelt U.M., Meacock P.A., Planta R.J., and Mager W.H. The accharomyces cerevisiae HSP12 gene is activated by the high-osmolarity glycerol pathway and negatively regulated by protein kinase A. Mol. Cell. Biol. 15 (1995) 6232-6245
79. Verstrepen K.J., Derdelinckx G., Verachtert H., and Delvaux F.R. Yeast flocculation: what brewers should know. Appl. Microbiol. Biotechnol. 61 (2003) 197-205
80. Wang S., Thomas K.C., Sosulski K., and Ingledew W.M. Grain pearling and very high gravity (VHG) fermentation technologies for fuel alcohol production from rye and triticale. Process Biochem. 34 (1999) 421-428
81. Wang Y., Li Y., Pei X., Yu L., and Feng Y. Genome-shuffling improved acid tolerance and l-lactic acid volumetric productivity in Lactobacillus rhamnosus. J. Biotechnol. 129 (2007) 510-515
82. Wisselink H.W., Toirkens M.J., del Rosario Franco Berriel M., Winkler A.A., van Dijken J.P., Pronk J.T., and van Maris A.J. Engineering of Saccharomyces cerevisiae for efficient anaerobic alcoholic fermentation of l-arabinose. Appl. Environ. Microbiol. 73 (2007) 4881-4891
83. Wu H., Zheng X., Araki Y., Sahara H., Takagi H., and Shimoi H. Global gene expression analysis of yeast cells during sake brewing. Appl. Environ. Microbiol. 72 (2006) 7353-7358
84. Xu T.J., Zhao X.Q., and Bai F.W. Continuous ethanol production using self flocculating yeast in a cascade of fermentors. Enzyme Microb. Technol. 37 (2005) 634-640
85. Xue C., Zhao X.Q., Yuan W.J., and Bai F.W. Improving ethanol tolerance of a self-flocculating yeast by optimization of medium composition. World J. Microbiol. Biotechnol. 24 (2008) 2257-2261
86. Yazawa H., Iwahashi H., and Uemura H. Disruption of URA7 and GAL6 improves the ethanol tolerance and fermentation capacity of Saccharomyces cerevisiae. Yeast 24 (2007) 551-560
87. You K.M., Rosenfield C.L., and Knipple D.C. Ethanol tolerance in the yeast Saccharomyces cerevisiae is dependent on cellular oleic acid content. Appl. Environ. Microbiol. 69 (2003) 1499-1503
88. Yoshikawa K., Tanaka T., Furusawa C., Nagahisa K., Hirasawa T., and Shimizu H. Comprehensive phenotypic analysis for identification of genes affecting growth under ethanol stress in Saccharomyces cerevisiae. FEMS Yeast Res. 9 (2009) 32-44
89. Zhang Y.X., Perry K., Vinci V.A., Powell K., Stemmer W.P., and del Cardayré S.B. Genome shuffling leads to rapid phenotypic improvement in bacteria. Nature 415 (2002) 644-646
90. Zhao X.Q., Xue C., Ge X.M., Wang J.Y., Yuan W.J., and Bai F.W. Impact of zinc supplementation on the improvement of ethanol tolerance of self-flocculating yeast in continuous ethanol fermentation. J. Biotechnol. 139 (2009) 55-60
91. Zuzuarregui A., and del Olmo M. Expression of stress response genes in wine strains with different fermentative behavior. FEMS Yeast Res. 4 (2004) 699-710
92. Zuzuarregui A., Monteoliva L., Gil C., and del Olmo M. Transcriptomic and proteomic approach for understanding the molecular basis of adaptation of Saccharomyces cerevisiae to wine fermentation. Appl. Environ. Microbiol. 72 (2006) 836-847