Metabolic and transcriptomic response of the wine yeast Saccharomyces cerevisiae strain EC1118 after an oxygen impulse under carbon-sufficient, nitrogen-limited fermentative conditions

FEMS Yeast Research

Volumn 14, Issue 3, 2014, Pages 412-424

  Orellana, Marcelo ^a   Aceituno, Felipe F ^a   Slater, Alex W ^a,b   Almonacid, Leonardo I ^a,b   Melo, Francisco ^a,b   Agosin, Eduardo ^a  

^a PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

^b Pontificia Universidad Católica de Chile   (Chile)

Author keywords

Fermentation; Oxidative stress; Oxygen impulse; Wine yeast

Indexed keywords

CARBON; DISSOLVED OXYGEN; ERGOSTEROL; MANNOPROTEIN; NITROGEN; OXYGEN; TRANSCRIPTOME;

ANAEROBIC CELL CULTURE; ARTICLE; BIOREACTOR; BIOSYNTHESIS; FERMENTATION; FUNGAL STRAIN; GENE EXPRESSION; METABOLISM; MITOCHONDRIAL RESPIRATION; NONHUMAN; OXIDATIVE STRESS; PUMP; SACCHAROMYCES CEREVISIAE; TRANSCRIPTION REGULATION; TRANSCRIPTOMICS; WINE; YEAST CELL; ANAEROBIC GROWTH; DRUG EFFECTS; GENETICS; METABOLOME; MICROBIOLOGY;

SACCHAROMYCES CEREVISIAE;

ANAEROBIOSIS; CARBON; FERMENTATION; METABOLIC NETWORKS AND PATHWAYS; METABOLOME; NITROGEN; OXIDATIVE STRESS; OXYGEN; SACCHAROMYCES CEREVISIAE; TRANSCRIPTOME; WINE;

EID: 84899968949     PISSN: 15671356     EISSN: 15671364     Source Type: Journal    
DOI: 10.1111/1567-1364.12135     Document Type: Article

References (76)

1. Aceituno FF, Orellana M, Torres J, Mendoza S, Slater AW, Melo F & Agosin E (2012) Oxygen response of the wine yeast Saccharomyces cerevisiae EC1118 strain grown under carbon-sufficient, nitrogen-limited oenological conditions. Appl Environ Microbiol 78: 8340-8352.
2. Alexandre H, Rousseaux I & Charpentier C (1994) Relationship between ethanol tolerance, lipid composition and plasma membrane fluidity in Saccharomyces cerevisiae and Kloeckera apiculata. FEMS Microbiol Lett 124: 17-22.
3. Alexandre H, Ansanay-Galeote V, Dequin S & Blondin B (2001) Global gene expression during short-term ethanol stress in Saccharomyces cerevisiae. FEBS Lett 498: 98-103.
4. Bauer FF & Pretorius IS (2000) Yeast stress response and fermentation efficiency: how to survive the making of wine: a review. S Afr J Enol Vitic 21: 27-51.
5. Bell W, Sun W, Hohmann S et al. (1998) Composition and functional analysis of the Saccharomyces cerevisiae trehalose synthase complex. J Biol Chem 273: 33311-33319.
6. Blateyron L & Sablayrolles JM (2001) Stuck and slow fermentations in enology: statistical study of causes and effectiveness of combined additions of oxygen and diammonium phosphate. J Biosci Bioeng 91: 184-189.
7. Boulton RB, Sinlgleton VL, Bisson LF & Kunkee RE (1998) Principles and Practices of Winemaking. Aspen Publishers, Inc., Gaithersburg, MD.
8. Breitling R, Armengaud P, Amtmann A & Herzyk P (2004) Rank products: a simple, yet powerful, new method to detect differentially regulated genes in replicated microarray experiments. FEBS Lett 573: 83-92.
9. Caridi A (2006) Enological functions of parietal yeast mannoproteins. Antonie Van Leeuwenhoek 89: 417-422.
10. Caridi A (2007) New perspectives in safety and quality enhancement of wine through selection of yeasts based on the parietal adsorption activity. Int J Food Microbiol 120: 167-172.
11. Causton HC, Ren B, Koh SS et al. (2001) Remodeling of yeast genome expression in response to environmental changes. Mol Biol Cell 12: 323-337.
12. Chalier P, Angot B, Delteil D, Doco T & Gunata Z (2007) Interactions between aroma compounds and whole mannoprotein isolated from Saccharomyces cerevisiae strains. Food Chem 100: 22-30.
13. Chen T, Li F & Chen BS (2009) Cross-talks of sensory transcription networks in response to various environmental stresses. Interdiscip Sci 1: 46-54.
14. Christie KR, Weng S, Balakrishnan R et al. (2004) Saccharomyces Genome Database (SGD) provides tools to identify and analyze sequences from Saccharomyces cerevisiae and related sequences from other organisms. Nucleic Acids Res 32: D311-D314.
15. Davies BSJ & Rine J (2006) A role for sterol levels in oxygen sensing in Saccharomyces cerevisiae. Genetics 174: 191-201.
16. Decottignies A, Evain A & Ghislain M (2004) Binding of Cdc48p to a ubiquitin-related UBX domain from novel yeast proteins involved in intracellular proteolysis and sporulation. Yeast 21: 127-139.
17. Dikicioglu D, Karabekmez E, Rash B, Pir P, Kirdar B & Oliver SG (2011) How yeast re-programmes its transcriptional profile in response to different nutrient impulses. BMC Syst Biol 5: 148.
18. Dupin IVS, Stockdale VJ, Williams PJ, Jones GP, Markides AJ & Waters EJ (2000) Saccharomyces cerevisiae mannoproteins that protect wine from protein haze: evaluation of extraction methods and immunolocalization. J Agric Food Chem 48: 1086-1095.
19. Erasmus DJ, van der Merwe GK & van Vuuren HJ (2003) Genome-wide expression analyses: metabolic adaptation of Saccharomyces cerevisiae to high sugar stress. FEMS Yeast Res 3: 375-399.
20. Escot S, Feuillat M, Dulau L & Charpentier C (2001) Release of polysaccharides by yeasts and the influence of released polysaccharides on colour stability and wine astringency. Aust J Grape Wine Res 7: 153-159.
21. Estruch F (2000) Stress-controlled transcription factors, stress-induced genes and stress tolerance in budding yeast. FEMS Microbiol Rev 24: 469-486.
22. Fornairon-Bonnefond C, Demaretz V, Rosenfeld E & Salmon JM (2002) Oxygen addition and sterol synthesis in Saccharomyces cerevisiae during enological fermentation. J Biosci Bioeng 93: 176-182.
23. Gasch AP, Spellman PT, Kao CM et al. (2000) Genomic expression programs in the response of yeast cells to environmental changes. Mol Biol Cell 11: 4241-4257.
24. Gonzalez-Ramos D, Cebollero E & Gonzalez R (2008) A recombinant Saccharomyces cerevisiae strain overproducing mannoproteins stabilizes wine against protein haze. Appl Environ Microbiol 74: 5533-5540.
25. Green R, Lesage G, Sdicu A-M, Ménard P & Bussey H (2003) A synthetic analysis of the Saccharomyces cerevisiae stress sensor Mid2p, and identification of a Mid2p-interacting protein, Zeo1p, that modulates the PKC1-MPK1 cell integrity pathway. Microbiology 149: 2487-2499.
26. Hickman MJ & Winston F (2007) Heme levels switch the function of Hap1 of Saccharomyces cerevisiae between transcriptional activator and transcriptional repressor. Mol Cell Biol 27: 7414-7424.
27. Ingledew WM, Magnus CA & Sosulski FW (1987) Influence of oxygen on proline utilization during the wine fermentation. Am J Enol Vitic 38: 246-248.
28. Jamieson DJ (1998) Oxidative stress responses of the yeast Saccharomyces cerevisiae. Yeast 14: 1511-1527.
29. Jothi R, Balaji S, Wuster A et al. (2009) Genomic analysis reveals a tight link between transcription factor dynamics and regulatory network architecture. Mol Syst Biol 5: 294.
30. Klis FM, Boorsma A & De Groot PW (2006) Cell wall construction in Saccharomyces cerevisiae. Yeast 23: 185-202.
31. Kobayashi N, McClanahan TK, Simon JR, Treger JM & McEntee K (1996) Structure and functional analysis of the multistress response gene DDR2 from Saccharomyces cerevisiae. Biochem Biophys Res Commun 229: 540-547.
32. Kresnowati MTAP, van Winden WA, Almering MJH et al. (2006) When transcriptome meets metabolome: fast cellular responses of yeast to sudden relief of glucose limitation. Mol Syst Biol 2: 1-16.
33. Kwast KE, Burke PV & Poyton RO (1998) Oxygen sensing and the transcriptional regulation of oxygen-responsive genes in yeast. J Exp Biol 201: 1177-1195.
34. Kwast KE, Lai LC, Menda N, James DT III, Aref S & Burke PV (2002) Genomic analyses of anaerobically induced genes in Saccharomyces cerevisiae: functional roles of Rox1 and other factors in mediating the anoxic response. J Bacteriol 184: 250-265.
35. Lai LC, Kosorukoff AL, Burke PV & Kwast KE (2005) Dynamical remodeling of the transcriptome during short-term anaerobiosis in Saccharomyces cerevisiae: differential response and role of Msn2 and/or Msn4 and other factors in galactose and glucose media. Mol Cell Biol 25: 4075-4091.
36. Lai LC, Kosorukoff AL, Burke PV & Kwast KE (2006) Metabolic-state-dependent remodeling of the transcriptome in response to anoxia and subsequent reoxygenation in Saccharomyces cerevisiae. Eukaryot Cell 5: 1468-1489.
37. Landolfo S, Zara G, Zara S, Budroni M, Ciani M & Mannazzu I (2010) Oleic acid and ergosterol supplementation mitigates oxidative stress in wine strains of Saccharomyces cerevisiae. Int J Food Microbiol 141: 229-235.
38. Levin DE (2011) Regulation of cell wall biogenesis in Saccharomyces cerevisiae: the cell wall integrity signaling pathway. Genetics 189: 1145-1175.
39. Li L, Ye Y, Pan L, Zhu Y, Zheng S & Lin Y (2009) The induction of trehalose and glycerol in Saccharomyces cerevisiae in response to various stresses. Biochem Biophys Res Commun 387: 778-783.
40. 2+-induced growth defect in sphingolipid mannosyltransferase-deficient yeast. J Biol Chem 279: 36390-36396.
41. Lorenz MC & Heitman J (1998) Regulators of pseudohyphal differentiation in Saccharomyces cerevisiae identified through multicopy suppressor analysis in ammonium permease mutant strains. Genetics 150: 1443-1457.
42. Luo Z & van Vuuren HJ (2008) Stress-induced production, processing and stability of a seripauperin protein, Pau5p, in Saccharomyces cerevisiae. FEMS Yeast Res 8: 374-385.
43. Luo Z & van Vuuren HJ (2009) Functional analyses of PAU genes in Saccharomyces cerevisiae. Microbiology 155: 4036-4049.
44. Marks VD, Ho Sui SJ, Erasmus D et al. (2008) Dynamics of the yeast transcriptome during wine fermentation reveals a novel fermentation stress response. FEMS Yeast Res 8: 35-52.
45. Martinez-Pastor M, Marchler G, Schüller C, Marchler-Bauer A, Ruis H & Estruch F (1996) The Saccharomyces cerevisiae zinc finger proteins Msn2p and Msn4p are required for transcriptional induction through the stress response element (STRE). EMBO J 15: 2227.
46. Matys V, Fricke E, Geffers R et al. (2003) TRANSFAC: transcriptional regulation, from patterns to profiles. Nucleic Acids Res 31: 374-378.
47. Morano KA, Grant CM & Moye-Rowley WS (2012) The response to heat shock and oxidative stress in Saccharomyces cerevisiae. Genetics 190: 1157-1195.
48. Morgan BA, Banks GR, Toone WM, Raitt D, Kuge S & Johnston LH (1997) The Skn7 response regulator controls gene expression in the oxidative stress response of the budding yeast Saccharomyces cerevisiae. EMBO J 16: 1035-1044.
49. Ng CH, Tan SX, Perrone GG, Thorpe GW, Higgins VJ & Dawes IW (2008) Adaptation to hydrogen peroxide in Saccharomyces cerevisiae: the role of NADPH-generating systems and the SKN7 transcription factor. Free Radic Biol Med 44: 1131-1145.
50. Pearson RK, Zylkin T, Schwaber JS & Gonye GE (2004) Quantitative evaluation of clustering results using computational negative controls. Proceedings of the Fourth SIAM International Conference on Data Mining (Berry MW, Umeshwar D, Kamath C & Skilliconr D, eds), pp. 188-199. Society for Industrial and Applied Mathematics, Lake Buena Vista, FL.
51. Pizarro FJ, Jewett MC, Nielsen J & Agosin E (2008) Growth temperature exerts differential physiological and transcriptional responses in laboratory and wine strains of Saccharomyces cerevisiae. Appl Environ Microbiol 74: 6358-6368.
52. Plakunov VK & Shelemekh OV (2009) Mechanisms of oxygen regulation in microorganisms. Microbiology 78: 535-546.
53. Rachidi N, Martinez MJ, Barre P & Blondin B (2000) Saccharomyces cerevisiae PAU genes are induced by anaerobiosis. Mol Microbiol 35: 1421-1430.
54. Raitt DC, Johnson AL, Erkine AM, Makino K, Morgan B, Gross DS & Johnston LH (2000) The Skn7 response regulator of Saccharomyces cerevisiae interacts with Hsf1 in vivo and is required for the induction of heat shock genes by oxidative stress. Mol Biol Cell 11: 2335-2347.
55. Rintala E, Toivari M, Pitkanen JP, Wiebe MG, Ruohonen L & Penttila M (2009) Low oxygen levels as a trigger for enhancement of respiratory metabolism in Saccharomyces cerevisiae. BMC Genomics 10: 461.
56. Rosenfeld E & Beauvoit B (2003) Role of the non-respiratory pathways in the utilization of molecular oxygen by Saccharomyces cerevisiae. Yeast 20: 1115-1144.
57. Rosenfeld E, Beauvoit B, Blondin B & Salmon JM (2003) Oxygen consumption by anaerobic Saccharomyces cerevisiae under enological conditions: effect on fermentation kinetics. Appl Environ Microbiol 69: 113-121.
58. Rossignol T, Dulau L, Julien A & Blondin B (2003) Genome-wide monitoring of wine yeast gene expression during alcoholic fermentation. Yeast 20: 1369-1385.
59. Rossignol T, Postaire O, Storai J & Blondin B (2006) Analysis of the genomic response of a wine yeast to rehydration and inoculation. Appl Microbiol Biotechnol 71: 699-712.
60. Rossouw D, Olivares-Hernandes R, Nielsen J & Bauer FF (2009) Comparative transcriptomic approach to investigate differences in wine yeast physiology and metabolism during fermentation. Appl Environ Microbiol 75: 6600-6612.
61. Saa PA, Moenne MI, Perez-Correa JR & Agosin E (2012) Modeling oxygen dissolution and biological uptake during pulse oxygen additions in oenological fermentations. Bioprocess Biosyst Eng 35: 1167-1178.
62. Sanchez OJ & Cardona CA (2008) Trends in biotechnological production of fuel ethanol from different feedstocks. Bioresour Technol 99: 5270-5295.
63. Singh J, Kumar D, Ramakrishnan N et al. (2005) Transcriptional response of Saccharomyces cerevisiae to desiccation and rehydration. Appl Environ Microbiol 71: 8752-8763.
64. Smoot ME, Ono K, Ruscheinski J, Wang PL & Ideker T (2011) Cytoscape 2.8: new features for data integration and network visualization. Bioinformatics 27: 431-432.
65. Sokal RR & Rohlf FJ (1962) The comparison of dendrograms by objective methods. Taxon 11: 33-40.
66. Teixeira MC, Monteiro P, Jain P et al. (2006) The YEASTRACT database: a tool for the analysis of transcription regulatory associations in Saccharomyces cerevisiae. Nucleic Acids Res 34: D446-D451.
67. Ter Linde JJ & Steensma HY (2002) A microarray-assisted screen for potential Hap1 and Rox1 target genes in Saccharomyces cerevisiae. Yeast 19: 825-840.
68. Ter Linde J & Steensma H (2003) Transcriptional regulation of YML083c under aerobic and anaerobic conditions. Yeast 20: 439-454.
69. Valero E, Millan C & Ortega JM (2001) Influence of oxygen addition during growth phase on the biosynthesis of lipids in Saccharomyces cerevisiae (M(3)30-9) in enological fermentations. J Biosci Bioeng 92: 33-38.
70. van den Brink J, Daran-Lapujade P, Pronk JT & de Winde JH (2008) New insights into the Saccharomyces cerevisiae fermentation switch: dynamic transcriptional response to anaerobicity and glucose-excess. BMC Genomics 9: 100.
71. Varela C, Pizarro F & Agosin E (2004) Biomass content governs fermentation rate in nitrogen-deficient wine musts. Appl Environ Microbiol 70: 3392-3400.
72. Varela C, Cardenas J, Melo F & Agosin E (2005) Quantitative analysis of wine yeast gene expression profiles under winemaking conditions. Yeast 22: 369-383.
73. Vargas FA, Aceituno FF & Agosin E (2010) Biochemistry and molecular biology of yeast alcoholic fermentation. Comprehensive Food Fermentation and Biotechnology, Vol. 2 (Pandey A, Soccol CR, Gnansounou E, Larroche C, NeeNigam PS & Dussap CG, eds), pp. 245-299. Asiatech Publishers, New Delhi, India.
74. Wanduragala S, Sanyal N, Liang X & Becker DF (2010) Purification and characterization of Put1p from Saccharomyces cerevisiae. Arch Biochem Biophys 498: 136-142.
75. Yao R, Zhang Z, An X, Bucci B, Perlstein DL, Stubbe J & Huang M (2003) Subcellular localization of yeast ribonucleotide reductase regulated by the DNA replication and damage checkpoint pathways. P Natl Acad Sci USA 100: 6628-6633.
76. Zu T, Verna J & Ballester R (2001) Mutations in WSC genes for putative stress receptors result in sensitivity to multiple stress conditions and impairment of Rlm1-dependent gene expression in Saccharomyces cerevisiae. Mol Genet Genomics 266: 142-155.