Non-conventional yeast strains increase the aroma complexity of bread

PLoS ONE

Volumn 11, Issue 10, 2016, Pages

  Aslankoohi, Elham ^a,b   Herrera Malaver, Beatriz ^a,b   Rezaei, Mohammad Naser ^c   Steensels, Jan ^a,b   Courtin, Christophe M ^c   Verstrepen, Kevin J ^a,b  

^a DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^b UNIVERSITY OF LEUVEN   (Belgium)

^c LEUVEN FOOD SCIENCE AND NUTRITION RESEARCH CENTRE LFORCE   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

AROMA; CLINICAL ARTICLE; DOUGH; FLAVOR; HUMAN; NONHUMAN; SACCHAROMYCES BAYANUS; SENSORY ANALYSIS; SPECIES; TORULASPORA DELBRUECKII; YEAST; BREAD; CLASSIFICATION; FERMENTATION; MASS FRAGMENTOGRAPHY; PHYSIOLOGY; SOLID PHASE MICROEXTRACTION; SPECIES DIFFERENCE;

FRAGRANCE;

BREAD; FERMENTATION; GAS CHROMATOGRAPHY-MASS SPECTROMETRY; ODORANTS; SOLID PHASE MICROEXTRACTION; SPECIES SPECIFICITY; YEASTS;

EID: 84992371960     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0165126     Document Type: Article

References (61)

1. Sicard D, Legras JL. Bread, beer and wine: yeast domestication in the Saccharomyces sensu stricto complex. Comptes rendus biologies. 2011;334(3):229-36. Epub 2011/03/08. doi: 10.1016/j.crvi.2010. 12.016 PMID: 21377618.
2. Steensels J, Verstrepen KJ. Taming wild yeast: potential of conventional and nonconventional yeasts in industrial fermentations. Annual review of microbiology. 2014;68:61-80. Epub 2014/04/30. doi: 10. 1146/annurev-micro-091213-113025 PMID: 24773331.
3. Legras J-L, Merdinoglu D, Cornuet J-M, Karst F. Bread, beer and wine: Saccharomyces cerevisiae diversity reflects human history. Molecular Ecology. 2007;16(10):2091-102. doi: 10.1111/j.1365-294X.2007.03266.x PMID: WOS:000246366800009.
4. Piskur J, Rozpedowska E, Polakova S, Merico A, Compagno C. How did Saccharomyces evolve to become a good brewer? Trends in Genetics. 2006;22(4):183-6. doi: 10.1016/j.tig.2006.02.002 PMID: WOS:000237145200001.
5. Gallone B, Steensels J, Prahl T, Soriaga L, Saels V, Herrera-Malaver B, et al. Domestication and divergence of Saccharomyces cerevisiae beer yeasts. Cell. 2016; In Press.
6. Randez-Gil F, Corcoles-Saez I, Prieto JA. Genetic and Phenotypic Characteristics of Baker's Yeast: Relevance to Baking. Annu Rev Food Sci Technol. 2013;4:191-214. doi: 10.1146/annurev-food-030212-182609 PMID: WOS:000321737800010.
7. Domizio P, Lencioni L, Ciani M, Di Blasi S, Pontremolesi C, Sabatelli MP. Spontaneous and inoculated yeast populations dynamics and their effect on organoleptic characters of Vinsanto wine under different process conditions. International Journal of Food Microbiology. 2007;115(3):281-9. doi: 10.1016/j. ijfoodmicro.2006.10.052 PMID: WOS:000245772700003.
8. Daenen L, Sterckx F, Delvaux FR, Verachtert H, Derdelinckx G. Evaluation of the glycoside hydrolase activity of a Brettanomyces strain on glycosides from sour cherry (Prunus cerasus L.) used in the production of special fruit beers. Fems Yeast Research. 2008;8(7):1103-14. doi: 10.1111/j.1567-1364. 2008.00421.x PMID: WOS:000260114400013.
9. De Vuyst L, Van Kerrebroeck S, Harth H, Huys G, Daniel HM, Weckx S. Microbial ecology of sourdough fermentations: diverse or uniform? Food Microbiology. 2014;37:11-29. Epub 2013/11/16. doi: 10.1016/j.fm.2013.06.002 PMID: 24230469.
10. Rainieri S, Pretorius IS. Selection and improvement of wine yeasts. Annals of Microbiology. 2000;50(1):15-31. PMID: WOS:000089017100003.
11. Schuller D, Casal M. The use of genetically modified Saccharomyces cerevisiae strains in the wine industry. Applied Microbiology and Biotechnology. 2005;68(3):292-304. PMID: 10.1007/s00253-005-1994-2. doi: 10.1007/s00253-005-1994-2
12. Wedral D, Shewfelt R, Frank J. The challenge of Brettanomyces in wine. LWT-Food Science and Technology. 2010;43(10):1474-9. doi: 10.1016/j.lwt.2010.06.010 PMID: WOS:000282412300002.
13. Domizio P, Romani C, Lencioni L, Comitini F, Gobbi M, Mannazzu I, et al. Outlining a future for non-Saccharomyces yeasts: Selection of putative spoilage wine strains to be used in association with Saccharomyces cerevisiae for grape juice fermentation. International Journal of Food Microbiology. 2011;147(3):170-80. doi: 10.1016/j.ijfoodmicro.2011.03.020 PMID: WOS:000292360400003.
14. Rojas V, Gil JV, Pinaga F, Manzanares P. Studies on acetate ester production by non-Saccharomyces wine yeasts. International Journal of Food Microbiology. 2001;70(3):283-9. doi: 10.1016/s0168-1605 (01) 00552-9 PMID: WOS:000172495400007.
15. Clemente-Jimenez JM, Mingorance-Cazorla L, Martinez-Rodriguez S, Heras-Vazquez FJL, Rodriguez-Vico F. Influence of sequential yeast mixtures on wine fermentation. International Journal of Food Microbiology. 2005;98(3):301-8. doi: 10.1016/j.ijfoodchem.2004.06.007 PMID: WOS:000227202100009.
16. Moreira N, Mendes F, de Pinho RG, Hogg T, Vasconcelos I. Heavy sulphur compounds, higher alcohols and esters production profile of Hanseniaspora uvarum and Hanseniaspora guilliermondii grown as pure and mixed cultures in grape must. International Journal of Food Microbiology. 2008;124(3):231-8. doi: 10.1016/ijfoodmicro.2008.03.025 PMID: WOS:000256843800003.
17. Crafack M, Mikkelsen MB, Saerens S, Knudsen M, Blennow A, Lowor S, et al. Influencing cocoa flavour using Pichia kluyveri and Kluyveromyces marxianus in a defined mixed starter culture for cocoa fermentation. International Journal of Food Microbiology. 2013;167(1):103-16. doi: 10.1016/j. ijfoodmicro.2013.06.024 PMID: WOS:000326559700013.
18. Saerens S, Swiegers JH, inventors; Google Patents., assignee. Enhancement of beer flavor by a combination of Pichia yeast and different hop varieties patent WO2013030398 A1. 2013 March.
19. Pacheco A, Leão C, Almeida J, Santos J, Sousa MJ, Chaves S. The emerging role of the yeast Torulaspora delbrueckii in bread and wine production: using genetic manipulation to study molecular basis of physiological responses: INTECH Open Access Publisher; 2012. Available from: http://www.intechopen. com/books/export/citation/EndNote/structure-and-function-of-food-engineering/theemergingrole-of-the-yeast-torulaspora-delbrueckii-in-bread-and-wine-production-using-genetic-ma.
20. Ohshima Y, Sugaura T, Horita M, Sasaki T. Industrial application of artificially induced diploid strains of Torulaspora delbrueckii. Applied and Environmental Microbiology. 1987;53(7):1512-4. PMID: WOS: A1987J039200019.
21. Birch AN, Petersen MA, Arneborg N, Hansen ÅS. Influence of commercial baker's yeasts on bread aroma profiles. Food Research International. 2013;52(1):160-6. http://dx.doi.org/10.1016/j.foodres. 2013.03.011.
22. Birch AN, Petersen MA, Hansen ÅS. The aroma profile of wheat bread crumb influenced by yeast concentration and fermentation temperature. LWT-Food Science and Technology. 2013;50(2):480-8. http://dx.doi.org/10.1016/j.lwt.2012.08.019.
23. Almeida MJ, Pais C. Leavening ability and freeze tolerance of yeasts isolated from traditional corn and rye bread doughs. Applied and Environmental Microbiology. 1996;62(12):4401-4. PMID: WOS: A1996VW21600016.
24. Alves-Araujo C, Almeida MJ, Sousa MJ, Leao C. Freeze tolerance of the yeast Torulaspora delbrueckii: cellular and biochemical basis. Fems Microbiology Letters. 2004;240(1):7-14. doi: 10.1016/j. femsle.2004.09.008 PMID: WOS:000224848800002.
25. Spano G, Russo P, Lonvaud-Funel A, Lucas P, Alexandre H, Grandvalet C, et al. Biogenic amines in fermented foods. European Journal of Clinical Nutrition. 2010;64:S95-S100. doi: 10.1038/ejcn. 2010. 218 PMID: WOS:000283752600018.
26. Abelson JN, Simon MI, Guthrie C, Fink GR. Guide to Yeast Genetics and Molecular Biology: Elsevier Science; 2004. 933 p.
27. Burke D, Dawson D, Stearns T. Methods in yeast genetics: a Cold Spring Harbor Laboratory course manual. 2nd ed. New York: CSHL Press; 2000.
28. Joosten H, Northolt MD. Detection, growth, and amine-producing capacity of lactobacilli in cheese. Applied and Environmental Microbiology. 1989;55(9):2356-9. PMID: WOS:A1989AN87500040.
29. Nikolaou E, Soufleros EH, Bouloumpasi E, Tzanetakis N. Selection of indigenous Saccharomyces cerevisiae strains according to their oenological characteristics and vinification results. Food Microbiology. 2006;23(2):205-11. doi: 10.1016/j.fm.2005.03.004 PMID: WOS:000232319900014.
30. AACC. Approved Methods of Analysis. 11th Ed. Method 10-10.03. Optimized Straight-Dough Bread-Making Method. St. Paul, MN, USA: American Association of Cereal Chemists 2000.
31. Meilgaard MC, Civille GV, Carr BT. Sensory evaluation techniques. 3th ed. Florida, USA: CRC press; 1999.
32. Plessas S, Fisher A, Koureta K, Psarianos C, Nigam P, Koutinas AA. Application of Kluyveromyces marxianus, Lactobacillus delbrueckii ssp. bulgaricus and L. helveticus for sourdough bread making. Food Chemistry. 2008;106(3):985-90. http://dx.doi.org/10.1016/j.foodchem.2007.07.012.
33. Halang WA, Langlais R, Kugler E. Cubic spline interpolation for the calculation of retention indices in temperature-programmed gas-liquid chromatography. Analytical Chemistry. 1978;50(13):1829-32. doi: 10.1021/ac50035a026
34. Adams RP. Identification of essential oil compounds by gas chromatography and mass spectrometry. Illinois, USA: Allured Publishing Corporation; 2009.
35. Mondello L. Wiley FFNSC Library-Mass Spectra of Flavors and Fragrances of Natural and Synthetic Compounds. Shimadzu Corporation; 2011.
36. Standard Reference Database [Internet]. 2011 [cited September 11, 2014]. Available from: http://www.nist.gov/srd/onlinelist.cfm.
37. Rezaei MN, Dornez E, Jacobs P, Parsi A, Verstrepen KJ, Courtin CM. Harvesting yeast (Saccharomyces cerevisiae) at different physiological phases significantly affects its functionality in bread dough fermentation. Food Microbiology. 2014;39:108-15. doi: 10.1016/j.fm.2013.11.013 PMID: WOS:000331682600016.
38. Flavornet and human odor space [Internet]. 2004. Available from: http://www.flavornet.org/.
39. Pozo-Bayoán MA, Guichard E, Cayot N. Flavor Control in Baked Cereal Products. Food Reviews International. 2006;22(4):335-79. doi: 10.1080/87559120600864829
40. Frauendorfer F, Schieberle P. Identification of the key aroma compounds in cocoa powder based on molecular sensory correlations. Journal of agricultural and food chemistry. 2006;54(15):5521-9. Epub 2006/07/20. doi: 10.1021/jf060728k PMID: 16848541.
41. Lee S-J, Noble AC. Characterization of Odor-Active Compounds in Californian Chardonnay Wines Using GC-Olfactometry and GC-Mass Spectrometry. Journal of agricultural and food chemistry. 2003;51(27):8036-44. doi: 10.1021/jf034747v PMID: 14690393
42. Rychlik M, Grosch W. Identification and Quantification of Potent Odorants Formed by Toasting of Wheat Bread. LWT-Food Science and Technology. 1996;29(5-6):515-25. http://dx.doi.org/10.1006/fstl.1996.0079.
43. Yang DS, Lee KS, Jeong OY, Kim KJ, Kays SJ. Characterization of volatile aroma compounds in cooked black rice. Journal of agricultural and food chemistry. 2008;56(1):235-40. Epub 2007/12/18. doi: 10.1021/jf072360c PMID: 18081248.
44. Schieberle P, Grosch W. Potent odorants of rye bread crust-differences from the crumb and from wheat bread crust. Zeitschrift für Lebensmittel-Untersuchung und Forschung. 1994;198(4):292-6. doi: 10.1007/BF01193177
45. Birch AN, Petersen MA, Hansen ÅS. Aroma of Wheat Bread Crumb. Cereal Chemistry Journal. 2014;91(2):105-14. doi: 10.1094/CCHEM-06-13-0121-RW
46. Schieberle P, Grosch W. Potent odorants of the wheat bread crumb Differences to the crust and effect of a longer dough fermentation. Zeitschrift für Lebensmittel-Untersuchung und Forschung. 1991;192(2):130-5. doi: 10.1007/BF01202626
47. Poinot P, Grua-Priol J, Arvisenet G, Rannou C, Semenou M, Bail AL, et al. Optimisation of HS-SPME to study representativeness of partially baked bread odorant extracts. Food Research International. 2007;40(9):1170-84. http://dx.doi.org/10.1016/j.foodres.2007.06.011.
48. Annan NT, Poll L, Sefa-Dedeh S, Plahar WA, Jakobsen M. Volatile compounds produced by Lactobacillus fermentum, Saccharomyces cerevisiae and Candida krusei in single starter culture fermentations of Ghanaian maize dough. Journal of Applied Microbiology. 2003;94(3):462-74. doi: 10.1046/j.1365-2672.2003.01852.x PMID: 12588555
49. Busko M, Jelen H, Goral T, Chmielewski J, Stuper K, Szwajkowska-Michalek L, et al. Volatile metabolites in various cereal grains. Food additives & contaminants Part A, Chemistry, analysis, control, exposure & risk assessment. 2010;27(11):1574-81. Epub 2010/08/24. doi: 10.1080/19440049.2010. 506600 PMID: 20730644.
50. Frasse P, Lambert S, Richard-Molard D, Chiron H. The Influence of Fermentation on Volatile Compounds in French Bread Dough. LWT-Food Science and Technology. 1993;26(2):126-32. http://dx. doi.org/10.1006/fstl.1993.1027.
51. Verstrepen KJ, Derdelinckx G, Dufour JP, Winderickx J, Thevelein JM, Pretorius IS, et al. Flavor-active esters: adding fruitiness to beer. Journal of bioscience and bioengineering. 2003;96(2):110-8. Epub 2005/10/20. PMID: 16233495.
52. Saerens SM, Delvaux FR, Verstrepen KJ, Thevelein JM. Production and biological function of volatile esters in Saccharomyces cerevisiae. Microbial biotechnology. 2010;3(2):165-77. Epub 2011/01/25. doi: 10.1111/j.1751-7915.2009.00106.x PMID: 21255318; PubMed Central PMCID: PMCPmc3836583.
53. Christiaens Joaquin F, Franco Luis M, Cools Tanne L, De Meester L, Michiels J, Wenseleers T, et al. The Fungal Aroma Gene ATF1 Promotes Dispersal of Yeast Cells through Insect Vectors. Cell Reports. 2014;9(2):425-32. doi: 10.1016/j.celrep. 2014.09.009 PMID: 25310977
54. Lilly M, Lambrechts MG, Pretorius IS. Effect of Increased Yeast Alcohol Acetyltransferase Activity on Flavor Profiles of Wine and Distillates. Applied and Environmental Microbiology. 2000;66(2):744-53. doi: 10.1128/aem.66.2.744-753.2000 PMID: 10653746
55. Birch AN, van den Berg FWJ, Hansen ÅS. Expansion profiles of wheat doughs fermented by seven commercial baker's yeasts. Journal of Cereal Science. 2013;58(2):318-23. http://dx.doi.org/10.1016/j.jcs.2013.05.009.
56. Brinker EM, Schmidt K, inventors; Google Patents, assignee. Proofing tolerant yeast-leavened dough patent US20100143534 A1. 2007 October.
57. Hernandez-Lopez MJ, Prieto JA, Randez-Gil F. Osmotolerance and leavening ability in sweet and frozen sweet dough. Comparative analysis between Torulaspora delbrueckii and Saccharomyces cerevisiae baker's yeast strains. Anton Leeuw Int J G. 2003;84(2):125-34. doi: 10.1023/a:1025413520192 PMID: WOS:000184988500006.
58. Maillard L. Action of amino acids on sugars. Formation of melanoidins in a methodical way. Comptes Rendus. 1912;154:66.
59. McKinnon CM, Gelinas P, Simard RE. Wine yeast preferment for enhancing bread aroma and flavor. Cereal Chemistry. 1996;73(1):45-50. PMID: WOS:A1996TW32900008.
60. Rossouw D, Jolly N, Jacobson D, Bauer FF. The effect of scale on gene expression: commercial versus laboratory wine fermentations. Applied Microbiology and Biotechnology. 2012;93(3):1207-19. Epub 2011/09/21. doi: 10.1007/s00253-011-3564-0 PMID: 21931974.
61. Steensels J, Snoek T, Meersman E, Nicolino MP, Voordeckers K, Verstrepen KJ. Improving industrial yeast strains: exploiting natural and artificial diversity. FEMS Microbiology Reviews. 2014;38(5):947-95. doi: 10.1111/1574-6976.12073 PMID: 24724938