Surviving in the presence of sulphur dioxide: Strategies developed by wine yeasts

Applied Microbiology and Biotechnology

Volumn 95, Issue 3, 2012, Pages 601-613

  Divol, Benoit ^a   Du Toit, Maret ^a   Duckitt, Edward ^a  

^a STELLENBOSCH UNIVERSITY   (South Africa)

Author keywords

Cellular and molecular response; Sulphur dioxide; VBNC state; Wine; Yeast

Indexed keywords

CULTURABLE; DEFENCE MECHANISMS; MOLECULAR MECHANISM; MOLECULAR RESPONSE; ON CURRENTS; VBNC STATE; WINE YEAST; YEAST CELL;

ALDEHYDES; SULFUR DETERMINATION; SULFUR DIOXIDE; WINE;

YEAST;

ACETALDEHYDE; BISULFITE; SULFITE; SULFUR DIOXIDE;

ANTIOXIDANT; MOLECULAR ANALYSIS; NINETEENTH CENTURY; PH; SULFUR DIOXIDE; YEAST;

DEFENSE MECHANISM; MOLECULAR MECHANICS; NONHUMAN; OXIDATION; PH; REVIEW; SACCHAROMYCES CEREVISIAE; WINE; WINE YEAST; YEAST; YEAST CELL;

FOOD PRESERVATIVES; METABOLIC NETWORKS AND PATHWAYS; MICROBIAL VIABILITY; SULFUR DIOXIDE; WINE; YEASTS;

SACCHAROMYCES CEREVISIAE;

EID: 84864586837     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-012-4186-x     Document Type: Review

References (114)

1. Aa E, Townsend JP, Adams RI, Nielsen KM, Taylor JW (2006) Population structure and gene evolution in Saccharomyces cerevisiae. FEMS Yeast Res 6:702-715
2. Agnolucci M, Rea F, Sbrana C, Cristani C, Fracassetti D, Tirelli A, Nuti M (2010) Sulphur dioxide affects culturability and volatile phenol production by Brettanomyces/Dekkera bruxellensis. Int J Food Microbiol 143:76-80
3. Anacleto J, van Uden N (1982) Kinetics and activation energetics of death in Saccharomyces cerevisiae induced by sulfur dioxide. Biotechnol Bioeng 24:2477-2486
4. Aranda A, del Olmo M (2004) Exposure to acetaldehyde in yeast determines an induction of sulfur amino acid metabolism and polyamine transporter genes, which depends on Met4p and Haa1p transcription factors, respectively. Appl Environ Microbiol 70:1913-1922
5. Aranda A, Jimenez-Marti E, Orozco H, Matallana E, Del Olmo M (2006) Sulfur and adenine metabolisms are linked, and both modulate sulfite resistance in wine yeast. J Agric Food Chem 54:5839-5846
6. Avram D, Bakalinsky AT (1996) FZF1 (SUL1) suppresses sulfite sensitivity but not the glucose derepression or aberrant cell morphology of a grr1 mutant of Saccharomyces cerevisiae. Genetics 144:511-521
7. Avram D, Bakalinsky AT (1997) SSU1 encodes a plasma membrane protein with a central role in a network of proteins conferring sulfite tolerance in Saccharomyces cerevisiae. J Bacteriol 179:5971-5974
8. Avram D, Leid M, Bakalinsky AT (1999) Fzf1p of Saccharomyces cerevisiae is a positive regulator of SSU1 transcription and its first zinc finger region is required for DNA binding. Yeast 15:473-480
9. Bailey RB, Woodword A (1984) Isoaltion and characterization of a pleiotropic glucose repression resistance mutant of Saccharomyces cerevisiae. Mol Gen Genet 193:507-512
10. Bakker J, Bridle P, Bellworthy SJ, Garcia-Viguera C, Reade HP, Watkins SJ (1998) Effect of sulphur dioxide and must extraction on colour, phenolic composition and sensory quality of red table wine. J Sci Food Agric 78:297-307
11. Baldwin GN (1951) Basic effect of sulphur dioxide on yeast growth. Am J Enol Vitic 2:43-53
12. Barata A, Caldeira J, Botelheiro R, Pagliara D, Malfeito-Ferreira M, Loureiro V (2008) Survival patterns of Dekkera bruxellensis in wines and inhibitory effect of sulphur dioxide. Int J Food Microbiol 121:201-207
13. Barral Y, Jentsch S, Mann C (1995) G1 cyclin turnover and nutrient uptake are controlled by a common pathway in yeast. Genes Dev 9:399-409
14. Bartowsky EJ, Pretorius IS (2009) Microbial formation and modification of flavor and off-flavor compounds in wine. In: König H, Unden G, Fröhlich J (eds) Biology of microorganisms on grapes, in must and in wine. Springer, Berlin, pp 209-232
15. Beck-Speier I, Hinze H, Holzer H (1985) Effect of sulfite on the energy metabolism of mammalian tissues in correlation to sulfite oxidase activity. Biochim Biophys Act Gen Subj 841:81-89
16. Beech FW, Thomas S (1985) Action antimicrobienne de l'anhydride sulfureux. Bull OIV 652-653:564-581
17. Bleve G, Rizzotti L, Dellaglio F, Torriani S (2003) Development of reverse-transcription (RT)-PCR and real-time RT-PCR assays for rapid detection and quantification of viable yeasts and molds contaminating yogurts and pasteurized food products. Appl Environ Microbiol 69:4116-4122
18. Booth IR (2002) Stress and the single cell: intrapopulation diversity is a mechanism to ensure survival upon exposure to stress. Int J Food Microbiol 16:365-375
19. Burroughs LF (1975) Determining free sulfur dioxide in red wine. Am J Enol Vitic 26:25-29
20. Carmack M, Moore MB, Balis ME (1950) The structure of the antihemorrhagic sodium bisulfite addition product of 2-methyl-1,4-naphthoquinone (menadione). J Am Chem Soc 72:844-847
21. Casalone E, Colella CM, Ricci F, Polsinelli M (1989) Isolation and characterization of Saccharomyces cerevisiae mutants resistant to sulphite. Yeast 5 Spec No:S287-291
22. Casalone E, Colella CM, Daly S, Gallori E, Moriani L, Polsinelli M (1992) Mechanism of resistance to sulfite in Saccharomyces cerevisiae. Curr Genet 22:435-440
23. Casalone E, Colella CM, Daly S, Fontana S, Torricelli I, Polsinelli M (1994) Cloning and characterization of a sulfite resistant gene of Saccharomyces cerevisiae. Yeast 10:1101-1110
24. Charles A, Suzuki I (1966) Purification and properties of sulfite: cytochrome c oxidoreductase from Thiobacillus novellus. Biochim Biophys Acta 128:522-534
25. Conklin DS, Kung C, Culbertson MR (1993) The COT2 gene is required for glucose-dependent divalent cation transport in Saccharomyces cerevisiae. Mol Cell Biol 13:2041-2049
26. Del Mar LM, Pierobon S, Tafi MC, Signoretto C, Canepari P (2000) mRNA detection by reverse-transcription-PCR for monitoring viability over time in an Enterococcus faecalis viable but nonculturable population maintained in a laboratory microcosm. Appl Environ Microbiol 66:4564-4567
27. Divol B, Lonvaud-Funel A (2005) Evidence for viable but nonculturable yeasts in botrytis affected wine. J Appl Microbiol 99:85-93
28. Divol B, Miot-Sertier C, Lonvaud-Funel A (2006) Genetic characterization of strains of Saccharomyces cerevisiae responsible for 'refermentation' in Botrytis-affected wines. J Appl Microbiol 100:516-526
29. Donalies UEB, Stahl U (2002) Increasing sulphite formation in Saccharomyces cerevisiae by overexpression of MET14 and SSU1. Yeast 19:475-484
30. du Toit WJ, Pretorius IS, Lonvaud-Funel A (2005) The effect of sulphur dioxide and oxygen on the viability and culturability of a strain of Acetobacter pasteurianus and a strain of Brettanomyces bruxellensis isolated from wine. J Appl Microbiol 98:862-871
31. Erickson JR, Johnston M (1994) Suppressors reveal two classes of glucose repression genes in the yeast Saccharomyces cerevisiae. Genetics 136:1271-1278
32. Feng C, Tollin G, Enemark JH (2007) Sulfite oxidizing enzymes. Biochi Biophys Acta Prot Proteome 1774:527-539
33. Flick JS, Johnston M (1991) GRR1 of Saccharomyces cerevisiae is required for glucose repression and encodes a protein with leucine-rich repeats. Mol Cell Biol 11:5101-5115
34. Freese E, Sheu CW, Galliers E (1973) Function of lipophilic acids as antimicrobial food additives. Nature 241:321-325
35. Friedrich CG, Bardischewsky F, Rother D, Quentmeier A, Fischer J (2005) Prokaryotic sulfur oxidation. Curr OpinMicrobiol 8:253-259
36. Frivik SK, Ebeler SE (2003) Influence of sulfur dioxide on the formation of aldehydes in white wine. Am J Enol Vitic 54:31-38
37. Giraffa G (2004) Studying the dynamics of microbial populations during food fermentation. FEMS Microbiol Rev 28:251-260
38. Goto-Yamamoto N, Kitano K, Shiki K, Yoshida Y, Suzuki T, Iwata T, Yamane Y, Hara S (1998) SSU1-R, a sulfite resistance gene of wine yeast, is an allele of SSU1 with a different upstream sequence. J Ferment Bioeng 86:427-433
39. Hänsch R, Lang C, Rennenberg H, Mendel RR (2007) Significance of plant sulfite oxidase. Plant Biol (Stutt) 9:589-595
40. Heimberg M, Fridovich I, Handler P (1953) The enzymatic oxidation of sulfite. J Biol Chem 204:913-926
41. Hellborg L, Piskur J (2009) Complex nature of the genome in a wine spoilage yeast, Dekkera bruxellensis. Eukaryot Cell 8:1739-1749
42. Henick-Kling T, Edinger W, Daniel P, Monk P (1998) Selective effects of sulfur dioxide and yeast starter culture addition on indigenous yeast populations and sensory characteristics of wine. J Appl Microbiol 84:865-876
43. Herrero M, Garcia LA, DiazM(2003) The effect of SO2 on the production of ethanol, acetaldehyde, organic acids and flavor volatiles during industrial cider fermentation. J Agric Food Chem 51:3455-3459
44. Hinze H, Holzer H (1986) Analysis of the energy metabolism after incubation of Saccharomyces cerevisiae with sulfite or nitrite. Arch Microbiol 145:27-31
45. Hohmann S, Mager PWH (2003) Yeast stress responses. Springer
46. Berlin Imai T, Ohno T (1995) The relationship between viability and intracellular pH in the yeast Saccharomyces cerevisiae. Appl Environ Microbiol 61:3604-3608
47. Ingram M (1948) The germicidal effect of free and combined sulphur dioxide. J Soc Chem Ind (London) 67:18-21
48. Kappler U, Dahl C (2001) Enzymology and molecular biology of prokaryotic sulfite oxidation. FEMS Microbiol Lett 203:1-9
49. Kåtgedal B, K llberg M, Sörbo B (1986) A possible involvement of glutathione in the detoxification of sulfite. Biochem Biophys Res Comm 136:1036-1041
50. Kell DB, Kaprelysants AS, Weichart DH, Harwood CR, Barer MR (1998) Viability and activity in readily culturable bacteria: a review and discussion of the practical issues. Antonie Leeuwenhoek 73:169-187
51. Kim YJ, Francisco L, Chen GC, Marcotte E, Chan CS (1994) Control of cellular morphogenesis by the Ip12/Bem2 GTPase-activating protein: possible role of protein phosphorylation. J Cell Biol 127:1381-1394
52. Kobayashi K, Yoshimoto A (1982) Studies on yeast sulfite reductase. IV. Structure and steady-state kinetics. Biochim Biophys Act Bioenerg 705:348-356
53. Kurek EJ (1985) Properties of an enzymatic complex active in sulfite and thiosulfate oxidation by Rhodotorula sp. Arch Microbiol 143:277-282
54. Ladrey C (1871) L'art de faire le vin. Imprimerie J.E. Rabutot, Dijon, France
55. Liti G, Carter DM, Moses AM, Warringer J, Parts L, James SA, Davey RP, Roberts IN, Burt A, Koufopanou V, Tsai IJ, Bergman CM, Bensasson D, O'Kelly MJT, van Oudenaarden A, Barton DBH, Bailes E, Nguyen Ba AN, Jones M, Quail MA, Goodhead I, Sims S, Smith F, Blomberg A, Durbin R, Louis EJ (2009) Population genomics of domestic and wild yeasts. Nature 458:337-341
56. Liu S-Q, Pilone GJ (2000) An overview of formation and roles of acetaldehyde in winemaking with emphasis on microbiological implications. Int J Food Sci Technol 35:49-61
57. Macris BJ, Markakis P (1974) Transport and toxicity of sulphur dioxide in Saccharomyces cerevisiae var. ellipsoideus. J Sci Food Agric 25:21-29
58. Maier K, Hinze H, Leuschel L (1986) Mechanism of sulfite action on the energy metabolism of Saccharomyces cerevisiae. Biochim Biophys Act Bioenerg 848:120-130
59. Mannervik B, Persson G, Eriksson S (1974) Enzymatic catalysis of the reversible sulfitolysis of glutathione disulfide and the biological reduction of thiosulfate esters. Arch Biochem Biophys 163:283-289
60. Meng Z, Zhang L (1992) Cytogenetic damage induced in human lymphocytes by sodium bisulfite. Mutat Res Genet Toxic 298:63-69
61. Millet V, Lonvaud-Funel A (2000) The viable but non-culturable state of wine micro-organisms during storage. Lett Appl Microbiol 30:136-141
62. Mills DA, Johannsen EA, Cocolin L (2002) Yeast diversity and persistence in Botrytis-affected wine fermentations. Appl Environ Microbiol 68:4884-4893
63. Mukai F, Hawryluk I, Shapiro R (1970) The mutagenic specificity of sodium bisulfite. Biochem Biophys Res Comm 39:983-988
64. Nardi T, Corich V, Giacomini A, Blondin B (2010) A sulphiteinducible form of the sulphite efflux gene SSU1 in a Saccharomyces cerevisiae wine yeast. Microbiology 156:1686-1696
65. Oliver JD (1993) Formation of viable but nonculturable cells. In: Kjelleberg S (ed) Starvation in bacteria. Plenum Press, New York, pp 239-272
66. Oliver JD (2005) The viable but nonculturable state in bacteria. J Microbiol 43:93-100
67. Oliver JD (2010) Recent findings on the viable but nonculturable state in pathogenic bacteria. FEMS Microbiol Rev 34:415-425
68. Pagano DA, Zeiger E (1987) Conditions affecting the mutagenicity of sodium bisulfite in Salmonella typhimurium. Mutat Res Fundam Mol Mech Mutag 179:159-166
69. PaganoDA, Zeiger E, StarkAA(1990)Autoxidation and mutagenicity of sodium bisulfite. Mutat Res Fundam Mol Mech Mutag 228:89-96
70. Park H, Bakalinsky AT (2000) SSU1 mediates sulphite efflux in Saccharomyces cerevisiae. Yeast 16:881-888
71. Park H, Bakalinsky AT (2004) Evidence for sulfite proton symport in Saccharomyces cerevisiae. J Microbiol Biotechnol 14:967-971
72. Park H, Hwang YS (2008) Genome-wide transcriptional responses to sulfite in Saccharomyces cerevisiae. J Microbiol 46:542-548
73. Pasteur L (1866) Etudes sur le vin. Imprimerie Impériale, Paris
74. Peneau S, Chassaing D, Carpentier B (2007) First evidence of division and accumulation of viable but nonculturable Pseudomonas fluorescens cells on surfaces subjected to conditions encountered atmeat processing premises. Appl Environ Microbiol 73:2839-2846
75. Perez-Ortin JE, Querol A, Puig S, Barrio E (2002) Molecular characterization of a chromosomal rearrangement involved in the adaptive evolution of yeast strains. Genome Res 12:1533-1539
76. Peynaud E, Lafourcade S (1952) Les conditions d'emploi de l'anhydride sulfureux dans les vins liquoreux. Bull OIV 252:110-120
77. Pilkington BJ, Rose AH (1988) Reaction of Saccharomyces cerevisiae and Zygosaccharomyces bailii to sulfite. J GenMicrobiol 134:2823-2830
78. Postgate JR (1969) Viable counts and viability. Meth Microbiol 1:611-628
79. Prakash D, Hinze H, Holzer H (1986) Synergistic effect of m-chloroperoxybenzoic acid, sulfite and nitrite on the energy metabolism of Saccharomyces cerevisiae. FEMS Microbiol Lett 34:305-308
80. Rahn O, Conn JE (1944) Effect of increase in acidity on antiseptic efficiency. Ind Eng Chem 36:185-187
81. Rankine BC, Pocock KF (1969) Influence of yeast strain on binding of sulphur dioxide in wines, and on its formation during fermentation. J Sci Food Agric 20:104-109
82. Rehm JH, Wittmann H (1962) Beitrag zur Kenntnis der antimikrobiellen Wirkung der schwefligen Säure. I. Übersicht uber einflussnehmende Faktoren auf die antimikrobiellen Wirkung der schwefligen Säure. Z Lebensmittelunters u-Forsch 118:413-429
83. Rehm JH, Wittmann H (1963) Beitrag zur Kenntnis der antimikrobiellen Wirkung der schwefligen Säure. II. Die Wirkung der dissoziierten und undissoziierten Säure auf verschiedene Mikroorganismen. Z Lebensmittelunters u-Forsch 120:465-478
84. Ribéreau-Gayon J, Peynaud E (1960) Traité d'oenologie Tome 1. Paris et Liege Librarie Polytechnique Ch. Béranger, Paris
85. Ripper M (1892) Die schweflige Säure im Weine und deren Bestimmung. J Prakt Chem 46:428-473
86. Romano P, Tini V (1975) Intensita e stabilita della resistenza alla SO2 in ceppi selvaggi di Saccharomyces ellipsoideus Riv Sci Tecnol Alimenti Nutr Um 5 245-246
87. Sardessai YN (2005) Viable but non-culturable bacteria: their impact on public health. Curr Sci 89:1650
88. Sarver A, DeRisi J (2005) Fzf1p regulates an inducible response to nitrosative stress in Saccharomyces cerevisiae. Mol Biol Cell 16:4781-4791
89. Schimz K-L (1980) The effect of sulfite on the yeast Saccharomyces cerevisiae. Arch Microbiol 125:89-95
90. Schimz K-L, Holzer H (1979) Rapid decrease of ATP content in intact cells of Saccharomyces cerevisiae after incubation with low concentrations of sulfite. Arch Microbiol 121:225-229
91. Serpaggi V, Remize F, Sequeira-Le Grand A, Alexandre H (2010a) Specific identification and quantification of the spoilage microorganism Brettanomyces in wine by flow cytometry: a useful tool for winemakers. Cytometry 77A:497-499
92. Serpaggi V, Remize F, Sequeira-Le Grand A, Alexandre H (2010b) The "viable but non culturable" state in spoilage yeast Brettanomyces: a risk for winemakers? 14th Australian Wine Industry Technical Conference, Adelaide
93. Serpaggi V, Remize F, Recorbet G, Gaudot-Dumas E, Sequeira-Le Grand A, Alexandre H (2012) Characterization of the "viable but nonculturable" (VBNC) state in the wine spoilage yeast Brettanomyces. Food Microbiol 30:438-447
94. Silver M, Lundgren D (1968) The thiosulfate-oxidizing enzyme of Ferrobacillus ferrooxidans (Thiobacillus ferrooxidans). Can J Biochem 46:1215-1220
95. Steels H, James SA, Roberts IM, Stratford M (2000) Sorbic acid resistance: the inoculum effect. Yeast 16:1173-1183
96. Stratford M, Rose IM (1986) Transport of sulphur dioxide by Saccharomyces cerevisiae. J Gen Microbiol 132:1-6
97. Stratford M, Morgan P, Rose AH (1987) Sulphur dioxide resistance in Saccharomyces cerevisiae and Saccharomycodes ludwigii. J Gen Microbiol 133:2173-2179
98. Suzuki I, SilverM(1966) The initial product and properties of the sulfuroxidizing enzyme of Thiobacilli. Biochim Biophys Act 122:22-23
99. Thomas S, Davenport R (1985) Zygosaccharomyces bailii-a profile of characteristics and spoilage activities. Food Microbiol 2:157-169
100. Thomas D, Surdin-Kerjan Y (1997) Metabolism of sulfur amino acids in Saccharomyces cerevisiae. Microbiol Mol Biol Rev 61:503-532
101. Thomas D, Barbey R, Henry D, Surdin-Kerjan Y (1992) Physiological analysis of mutants of Saccharomyces cerevisiae impaired in sulphate assimilation. J Gen Microbiol 138:2021-2028
102. Thornton RJ (1982) Selective hybridisation of pure culture wine yeasts. II. Improvement of fermentation efficiency and inheritance of SO2 tolerance. Eur J Appl Microbiol Biotechnol 14:159-164
103. Uzuka Y, Tanaka R, Nomura T, Tanaka K (1985) Method for the determination of sulfite resistance in wine yeasts. J Ferment Technol 63:107-114
104. Vallier LG, Coons D, Binson LF, Carison M (1994) Altered regulatory responses to glucose are associated with a glucose transport defect in grr1 mutant of Saccharomyces cerevisiae. Genetics 136:1279-1285
105. Ventre J (1934) Les levures en vinification: étude du ferment et du milieu -conditions d'emploi. Revue de Viticulture, Paris
106. Wang M, McIntee EJ, Cheng G, Shi Y, Villalta PW, Hecht SS (2000) Identification of DNA adducts of acetaldehyde. Chem Res Toxicol 13:1149-1157
107. Warth AD (1977) Mechanism of resistance of Saccharomyces bailii to benzoic, sorbic and other weak acids used as food preservatives. J Appl Bacteriol 43:215-230
108. Warth AD (1985) Resistance of yeast species to benzoic and sorbic acids and to sulfur dioxide. J Food Protect 48:564-569
109. Weeks C (1969) Production of sulfur dioxide-binding compounds and of sulfur dioxide by two Saccharomyces yeasts. Am J Enol Vitic 20:32-39
110. Xu HS, Roberts NC, Singleton FL, Atwell RW, Grimes DJ, Colwell RR (1982) Survival and viability of nonculturable Escherichia coli and Vibrio cholerae in the estuarine and marine environment. Microb Evol 8:313-323
111. Xu X, Wightman JD, Geller BL, Avram D, Bakalinsky AT (1994) Isolation and characterization of sulfite mutants of Saccharomyces cerevisiae. Curr Genet 25:488-496
112. Yoshimoto A, Sato R (1968) Studies on yeast sulfite reductase I. Purification and characterization. Biochim Biophys Acta Bioenerg 153:555-575
113. Yuasa N, Nakagawa Y, Hayakawa M, Iimura Y (2004) Distribution of the sulfite resistance gene SSU1-R and the variation in its promoter region in wine yeasts. J Biosci Bioeng 98:394-397
114. Yuasa N, Nakagawa Y, Hayakawa M, Iimura Y (2005) Two alleles of the sulfite resistance genes are differentially regulated in Saccharomyces cerevisiae. Biosci Biotechnol Biochem 69:1584-1588