Evolutionary engineering of a wine yeast strain revealed a key role of inositol and mannoprotein metabolism during low-temperature fermentation

BMC Genomics

Volumn 16, Issue 1, 2015, Pages

  López Malo, María ^a   García Rios, Estéfani ^a   Melgar, Bruno ^a   Sanchez, Monica R ^b   Dunham, Maitreya J ^b   Guillamón, José Manuel ^a  

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

^b UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Cold; Experimental evolution; Fermentation; Inositol; Wine; Yeast

Indexed keywords

INOSITOL; MANNOPROTEIN; MANNOPROTEINS; MEMBRANE PROTEIN;

ARTICLE; DAN1 GENE; DOWN REGULATION; FERMENTATION; FUNGAL CELL CULTURE; FUNGAL STRAIN; FUNGUS GROWTH; GENE; LIPID COMPOSITION; LOW TEMPERATURE; MUTAGENESIS; MUTATION RATE; NONHUMAN; PHENOTYPE; PROTEIN CONTENT; PROTEIN METABOLISM; PROTEIN SYNTHESIS; SINGLE NUCLEOTIDE POLYMORPHISM; TIR1 GENE; TIR3 GENE; TIR4 GENE; UPREGULATION; WINE; YEAST; GENETICS; METABOLIC ENGINEERING; METABOLISM; MOLECULAR EVOLUTION; TEMPERATURE;

SACCHAROMYCES CEREVISIAE;

EVOLUTION, MOLECULAR; FERMENTATION; INOSITOL; MEMBRANE GLYCOPROTEINS; METABOLIC ENGINEERING; TEMPERATURE; WINE; YEASTS;

EID: 84937231943     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/s12864-015-1755-2     Document Type: Article

References (67)

1. Beltran G, Novo M, Leberre V, Sokol S, Labourdette D, Guillamón JM, et al. Integration of transcriptomic and metabolic analyses for understanding the global responses of low-temperature winemaking fermentations. FEMS Yeast Res. 2006;6:1167-83.
2. Torija MJ, Beltran G, Novo M, Poblet M, Guillamón JM, Mas A, et al. Effects of fermentation temperature and Saccharomyces species on the cell fatty acid composition and presence of volatile compounds. Int J Food Microbiol. 2003;85:127-36.
3. Bisson L. Stuck and sluggish fermentation. Am J Enol Vitic. 1999;50:107-19.
4. Llauradó JM, Rozès N, Constanti M, Mas A. Study of some Saccharomyces cerevisiae strains for winemaking after preadaptation at low temperatures. J Agric Food Chem. 2005;53:1003-11.
5. Castellari L, Ferruzzi M, Magrini A, Giudici P. Unbalanced wine fermentation cryotolerant vs non-cryotolerant Saccharamyces strains. Vitis. 1994;33:49-52.
6. Giudici P, Caggia C, Pulvirenti A, Ranieri S. Karyotyping of Saccharomyces strains with different temperature profiles. J Appl Microbiol. 1998;84:811-9.
7. Massoutier C, Alexandre H, Feuillat M, Charpentier C. Isolation and characterization of cryotolerant Saccharomyces strains. Vitis. 1998;37:55-9.
8. Salvadó Z, Arroyo-López FN, Guillamón JM, Salazar G, Querol A, Barrio E. Temperature adaptation markedly determines the growth and evolution within the genus Saccharomyces. Appl Environ Microbiol. 2011;77:2292-302.
9. Dequin S. The potential of genetic engineering for improving brewing, wine-making and baking yeasts. Appl Microbiol Biotechnol. 2001;56:577-88.
10. Donalies UE, Nguyen HT, Stahl U, Nevoigt E. Improvements of Saccharomyces yeast strains used in brewing, wine making and baking. Adv Biochem Eng Biotechnol. 2008;111:67-98.
11. Husnik JI, Volschenk H, Bauer J, Colavizza D, Luo Z, van Vuuren HJ. Metabolic engineering of malolactic wine yeast. Metab Eng. 2006;8:315-23.
12. Çakar ZP, Turanli-Yildiz B, Alkim C, Yilmaz U. Evolutionary engineering of Saccharomyces cerevisiae for improved industrially important properties. FEMS Yeast Res. 2012;12:171-82.
13. Sonderegger M, Sauer U. Evolutionary engineering of Saccharomyces cerevisiae for anaerobic growth on xylose. Appl Environ Microbiol. 2003;69:1990-8.
14. Guimarães PMR, François J, Parrou JL, Teixeira JA, Domingues L. Adaptive evolution of a lactose-consuming Saccharomyces cerevisiae recombinant. Appl Environ Microbiol. 2008;74:1748-56.
15. Teunissen A, Dumortier F, Gorwa MF, Bauer J, Tanghe A, Loïez A, et al. Isolation and characterization of a freeze-tolerant diploid derivative of an industrial baker's yeast strain and its use in frozen doughs. Appl Environ Microbiol. 2002;68:4780-7.
16. Cadière A, Ortiz-Julien A, Camarasa C, Dequin S. Evolutionary engineering Saccharomyces cerevisiae wine yeast strains with increased in vivo flux through the pentose phosphate pathway. Metab Eng. 2011;13:263-71.
17. Cadière A, Aguera E, Caillé S, Ortiz-Julien A, Dequin S. Pilot-scale evaluation the enological traits of a novel, aromatic wine yeast strain obtained by adaptive evolution. Food Microbiol. 2012;32:332-7.
18. McBryde C, Gardner JM, de Barros Lopes M, Jiranek V. Generation of novel yeast strains by adaptive evolution. Am J Enol Vitic. 2006;57:423-30.
19. Paquin C, Adams J. Frequency of fixation of adaptive mutations is higher in evolving diploid than haploid yeast populations. Nature. 1983;302:495-500.
20. Çakar ZP, Seker UOS, Tamerler C, Sonderegger M, Sauer U. Evolutionary engineering of multiple-stress resistant Saccharomyces cerevisiae. FEMS Yeast Res. 2005;5:569-78.
21. Araya CL, Payen C, Dunham MJ, Fields S. Whole-genome sequencing of a laboratory-evolved yeast strain. BMC Genomics. 2010;11:88.
22. Dunham MJ, Badrane H, Ferea T, Adams J, Brown PO, Rosenzweig F, et al. Characteristic genome rearrangements in experimental evolution of Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 2002;99:16144-9.
23. Abramova N, Sertil O, Mehta S, Lowry CV. Reciprocal regulation of anaerobic and aerobic cell wall mannoprotein gene expression in Saccharomyces cerevisiae. J Bacteriol. 2001;183:2881-7.
24. Brown SL, Stockdale VJ, Pettolino F, Pocock KF, de Barros Lopes M, Williams PJ, et al. Reducing haziness in white wine by overexpression of Saccharomyces cerevisiae genes YOL155c and YDR055w. Appl Microbiol Biotechnol. 2007;73:1363-76.
25. Carman GM, Han GS. Regulation of phospholipid synthesis in the yeast Saccharomyces cerevisiae. Annu Rev Biochem. 2011;80:859-83.
26. López-Malo M, García-Ríos E, Chiva R, Guillamón JM. Functional analysis of lipid metabolism genes in wine yeasts during alcoholic fermentation at low temperature. Microb Cell. 2014;1:365-75.
27. Steensels J, Snoek T, Meersman E, Nicolino MP, Voordeckers K, Verstrepen KJ. Improving industrial yeast strains: exploiting natural and artificial diversity. FEMS Microbiol Rev. 2014;38:947-95.
28. Walker ME, Nguyen TD, Liccioli T, Schmid F, Kalatzis N, Sundstrom JF, et al. Genome-wide identification of the fermentome; genes required for successful and timely completion of fermentation by Saccharomyces cerevisiae. BMC Genomics. 2014;15:552.
29. Wenger JW, Piotrowski J, Nagarajan S, Chiotti K, Sherlock G, Rosenzweig F. Hunger artists: Yeast adapted to carbon limitation show trade-offs under carbon sufficiency. PLoS Genet. 2011;7, e1002202.
30. Russell N. Cold adaptation of microorganisms. Phil Trans R Soc Lond. 1990;326:595-611.
31. Fisher E, Almaguer C, Holic R, Griac P, Patton-Vogt J. Glycerophosphocholine-dependent growth requires Gde1p (YPL110c) and Git1p in Saccharomyces cerevisiae. J Biol Chem. 2005;280:36110-7.
32. Patton-Vogt JL, Henry SA. GIT1, a gene encoding a novel transporter for glycerophosphoinositol in Saccharomyces cerevisiae. Genetics. 1998;149:1707-15.
33. de Kroon AI, Rijken PJ, De Smet CH. Checks and balances in membrane phospholipid class and acyl chain homeostasis, the yeast perspective. Progr Lipid Res. 2013;52:374-94.
34. Kapteyn JC, Van Egmond P, Sievi E, Van Den Ende H, Makarow M, Klis FM. The contribution of the O-glycosylated protein Pir2p/Hsp150 to the construction of the yeast cell wall in wild-type cells and beta 1,6-glucan-deficient mutants. Mol Microbiol. 1999;31:1835-44.
35. Leidich SD, Kostova Z, Latek RR, Costello LC, Drapp DA, Gray W, et al. Temperature-sensitive yeast GPI anchoring mutants gpi2 and gpi3 are defective in the synthesis of N-acetylglucosaminyl phosphatidylinositol. Cloning of the GPI2 gene. J Biol Chem. 1995;270:13029-35.
36. Fraering P, Imhof I, Meyer U, Strub JM, van Dorsselaer A, Vionnet C, et al. The GPI transamidase complex of Saccharomyces cerevisiae contains Gaa1p, Gpi8p, and Gpi16p. Mol Biol Cell. 2001;12:3295-306.
37. Abe F. Induction of DAN/TIR yeast cell wall mannoprotein genes in response to high hydrostatic pressure and low temperature. FEBS Lett. 2007;581:4993-8.
38. Rossignol T, Dulau L, Julien A, Blondin B. Genome-wide monitoring of wine yeast gene expression during alcoholic fermentation. Yeast. 2003;20:1369-85.
39. Chiva R, López-Malo M, Salvadó Z, Mas A, Guillamón JM. Analysis of low temperature-induced genes (LTIG) in wine yeast during alcoholic fermentation. FEMS Yeast Res. 2012;12:831-43.
40. Hibbs MA, Hess DC, Myers CL, Huttenhower C, Li K, Troyanskaya OG. Exploring the functional landscape of gene expression: directed search of large microarray compendia. Bioinformatics. 2007;23:2692-9.
41. Pitkänen JP, Törmä A, Alff S, Huopaniemi L, Mattila P, Renkonen R. Excess mannose limits the growth of phosphomannose isomerase PMI40 deletion strain of Saccharomyces cerevisiae. J Biol Chem. 2004;79:5737-43.
42. Worley J, Luo X, Capaldi AP. Inositol pyrophosphates regulate cell growth and the environmental stress response by activating the HDAC Rpd3L. Cell Rep. 2013;3:1476-82.
43. Legras JL, Karst F. Optimisation of interdelta analysis for Saccharomyces cerevisiae strain characterisation. FEMS Microbiol Lett. 2003;221:249-55.
44. Winston F. EMS and UV mutagenesis in yeast. Curr Protoc Mol Biol. 2008;82:13.3B.1-5.
45. Quirós M, Martínez-Moreno R, Albiol J, Morales P, Vázquez-Lima F, Barreiro-Vázquez A, et al. Metabolic flux analysis during the exponential growth phase of Saccharomyces cerevisiae in wine fermentations. PLoS One. 2013;8, e71909.
46. Güldener U, Heck S, Fiedler T, Beinhauer J, Hegemann JH. A new efficient gene disruption cassette for repeated use in budding yeast. Nucleic Acids Res. 1996;24:2519-24.
47. Goldstein AL, McCusker JH. Three new dominant drug resistence cassettes for gene disruption in Saccharomyces cerevisiae. Yeast. 1999;15:1541-53.
48. Huxley C, Green ED, Dunham I. Rapid assessment of S. cerevisiae mating type by PCR. Trends Genet. 1990;6:236.
49. Jansen G, Wu C, Schade B, Thomas DY, Whiteway M. Drag and Drop cloning in yeast. Gene. 2005;344:43-51.
50. Riou C, Nicaud J, Barre P, Gaillardin C. Stationary-phase gene expression in Saccharomyces cerevisiae during wine fermentation. Yeast. 1997;13:903-15.
51. Speers RA, Rogers P, Smith B. Non-linear modelling of industrial brewing fermentations. J Inst Brew. 2003;109:229-35.
52. García-Ríos E, López-Malo M, Guillamón JM. Global phenotypic and genomic comparison of two Saccharomyces cerevisiae wine strains reveals a novel role of the sulfur assimilation pathway in adaptation at low temperature fermentations. BMC Genomics. 2014;15:1059.
53. Gutiérrez A, Chiva R, Sancho M, Beltran G, Arroyo-López FN, Guillamón JM. Nitrogen requirements of commercial wine yeast strains during fermentation of a synthetic grape must. Food Microbiol. 2012;31:25-32.
54. Sierkstra LN, Verbakel JM, Verrips CT. Analysis of transcription and translation of glycolytic enzymes in glucose-limited continuous cultures of Saccharomyces cerevisiae. J Gen Microbiol. 1992;138:2559-66.
55. Sambrook J, Fritsch EF, Maniatis T. Methods in yeast genetics: a laboratory manual. Cold Spring Harbor, NY. NY: Cold Spring Harbor Laboratory Press; 1989.
56. Gonzalez-Roca E, Garcia-Albéniz X, Rodriguez-Mulero S, Gomis RR, Kornacker K, Auer H. Accurate expresión profiling of very small cell populations. PLoS One. 2010;5, e14418.
57. Irizarry RA, Bolstad BM, Collin F, Cope LM, Hobbs B, Speed TP. Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res. 2003;31, e15.
58. Benjamini Y, Hochberg Y. Controlling the False Discovery Rate: A practical and powerful approach to multiple testing. J R Stat Soci. 1995;57:289-300.
59. Adey A, Morrison H, Asan X, Xun X, Kitzman J, Turner E, et al. Rapid, low-input, low-bias construction of shotgun fragment libraries by high-density in vitro transposition. Genome Biol. 2010;14:R119.
60. Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler Transform. Bioinformatics. 2009;25:1754-60.
61. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, et al. The Sequence alignment/map (SAM) format and SAMtools. Bioinformatics. 2009;25:2078-9.
62. Pashkova N, Gakhar L, Winistorfer S, Sunshine AB, Rich M, Dunham MJ, et al. The yeast Alix homolog, Bro1, functions as an ubiquitin receptor for protein sorting into multi vesicular endosomes. Dev Cell. 2013;5:520-33.
63. Robinson JT, Thorvaldsdóttir H, Winckler W, Guttman M, Lander ES, Getz G, et al. Integrative Genomics Viewer. Nature Biotechnol. 2011;29:24-6.
64. Quirós M, Morales P, Pérez-Través L, Barcenilla JM, González R. A new methodology to determine cell wall mannoprotein content and release in wine yeasts. Food Chem. 2011;125:760-6.
65. Redón M, Guillamón JM, Mas A, Rozès N. Effect of lipids supplementation upon Saccharomyces cerevisiae lipid composition and fermentation performance at low temperature. Eur Food Res Tech. 2009;228:833-40.
66. Friederichs JM, Ghosh S, Smoyer CJ, McCroskey S, Miller BD, Weaver KJ, et al. The SUN protein Mps3 is required for spindle pole body insertion into the nuclear membrane and nuclear envelope homeostasis. PLoS Genet. 2011;7, e1002365.
67. Welti R, Shah J, Li W, Li M, Chen J, Burke JJ, et al. Plant lipidomics: Discerning biological function by profiling plant complex lipids using mass spectrometry. Front Biosci. 2002;12:2494-506.