Yeast interactions in inoculated wine fermentation

Frontiers in Microbiology

Volumn 7, Issue APR, 2016, Pages

  Ciani, Maurizio ^a   Capece, Angela ^b   Comitini, Francesca ^a   Canonico, Laura ^a   Siesto, Gabriella ^b   Romano, Patrizia ^b  

^a UNIVERSITÀ POLITECNICA DELLE MARCHE   (Italy)

^b UNIVERSITY OF BASILICATA   (Italy)

Author keywords

Inoculated wine fermentation; Non Saccharomyces; Saccharomyces cerevisiae; Starter dominance; Yeast yeast interactions

Indexed keywords

ALCOHOL; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; NITROGEN; POLYPEPTIDE ANTIBIOTIC AGENT; SULFUR DIOXIDE; YEAST KILLER FACTOR;

APOPTOSIS; FERMENTATION; FOOD QUALITY; FUNGAL CELL CULTURE; FUNGAL STRAIN; INOCULATION; MICROFLORA; NONHUMAN; OSMOTIC PRESSURE; PH; SACCHAROMYCES CEREVISIAE; SHORT SURVEY; TEMPERATURE; WINE; YEAST;

EID: 84966262741     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2016.00555     Document Type: Short Survey

References (62)

1. Albergaria, H., Francisco, D., Gori, K., Arneborg, N., and Girio, F. (2010). Saccharomyces cerevisiae CCMI 885 secretes peptides that inhibit the growth of some non-Saccharomyces wine-related strains. Appl. Microbiol. Biotechnol. 86, 965-972. doi: 10.1007/s00253-009-2409-6
2. Andorrà, I., Berradre, M., Mas, A., Esteve-Zarzoso, B., and Guillamón, J. M. (2012). Effect of mixed culture fermentations on yeast populations and aroma profile. LWT Food Sci. Technol. 49, 8-13. doi: 10.1016/j.lwt.2012.04.008
3. Arroyo-López, F. N., Peréz-Través, L., Querol, A., and Barrio, E. (2011). Exclusion of Saccharomyces kudriavzevii from a wine model system mediated by Saccharomyces cerevisiae. Yeast 28, 423-435. doi: 10.1002/yea.1848
4. Azzolini, M., Fedrizzi, B., Tosi, E., Finato, F., Vagnoli, P., Scrinzi, C., et al. (2012). Effects of Torulaspora delbrueckii and Saccharomyces cerevisiae mixed cultures on fermentation and aroma of Amarone. Eur. Food Res. Technol. 235, 303-313. doi: 10.1007/s00217-012-1762-3
5. Barrajón, N., Arévalo-Villena, M., Rodríguez-Aragón, L. J., and Briones, A. (2009). Ecological study of wine yeast in inoculated vats from La Mancha region. Food Control 20, 778-783. doi: 10.1016/j.foodcont.2008.10.002
6. Barrajón, N., Arévalo-Villena, M., Úbeda, J., and Briones, A. (2010). "Competition between spontaneous and commercial yeasts in winemaking: study of possible factors involved, " in Communicating Current Research and Education Topics and Trends in Applied Microbiology and Microbiology Book Series Vol. 2, ed. A. Mendez-Vilas (Badajoz: Formatex Research Center), 1035-1041
7. Barrajón, N., Arévalo-Villena, M., Úbeda, J., and Briones, A. (2011). Enological properties in wild and commercial Saccharomyces cerevisiae yeasts: relationship with competition during alcoholic fermentation. World J. Microbiol. Biotechnol. 27, 2703-2710. doi: 10.1007/s11274-011-0744-0
8. Bauer, F. F., and Pretorius, I. S. (2000). Yeast stress response and fermentation efficiency: how to survive the making of wine. South Afr. J. Enol. Vitic. 21, 27-51
9. Bisson, L. F. (1999). Stuck and sluggish fermentations. Am J. Enol Vitic. 50, 107-119
10. Branco, P., Francisco, D., Chambon, C., Hébraud, M., Arneborg, N., and Almeida, M. G. (2014). Identification of novel GAPDH-derived antimicrobial peptides secreted by Saccharomyces cerevisiae and involved in wine microbial interactions. Appl. Microbiol. Biotechnol. 98, 843-853. doi: 10.1007/s00253-013-5411-y
11. Branco, P., Viana, T., Albergaria, H., and Arneborg, N. (2015). Antimicrobial peptides (AMPs) produced by Saccharomyces cerevisiae induce alterations in the intracellular pH, membrane permeability and culturability of Hanseniaspora guilliermondii cells. Int. J. Food Microbiol. 16, 205-212. doi: 10.1016/j.ijfoodmicro.2015.04.015
12. Brandam, C., Lai, Q. P., Julien-Ortiz, A., and Taillandier, P. (2013). Influence oxygen of alcoholic fermentation by a wine strain of Torulaspora delbrueckii: kinetics and carbon mass balance. Biosci. Biotechnol. Biochem. 77, 1848-1853. doi: 10.1271/bbb.130228
13. Canonico, L., Comitini, F., and Ciani, M. (2015). Influence of vintage and selected starter on Torulaspora delbrueckii/Saccharomyces cerevisiae sequential fermentation. Eur. Food Res. Technol. 241, 827-833. doi: 10.1007/s00217-015-2507-x
14. Capece, A., Romaniello, R., Poeta, C., Siesto, G., Massari, C., Pietrafesa, R., et al. (2011). Control of inoculated fermentations in wine cellars by mitochondrial DNA analysis of starter yeast. Ann. Microbiol. 61, 49-56. doi: 10.1007/s13213-010-0087-3
15. Capece, A., Romaniello, R., Siesto, G., Pietrafesa, R., Massari, C., Poeta, C., et al. (2010). Selection of indigenous Saccharomyces cerevisiae strains for Nero d'Avola wine and evaluation of selected starter implantation in pilot fermentation. Int. J. Food Microbiol. 144, 187-192. doi: 10.1016/j.ijfoodmicro.2010.09.009
16. Capece, A., Siesto, G., Romaniello, R., Lagreca, V. M., Pietrafesa, R., Calabretti, A., et al. (2013). Assessment of competition in wine fermentation among wild Saccharomyces cerevisiae strains isolated from Sangiovese grapes in Tuscany region. LWT- Food Sci. Technol. 54, 485-492. doi: 10.1016/j.lwt.2013.07.001
17. Casey, G. P., Magnus, C. A., and Ingledew, W. M. (1984). High gravity brewing: effects of nutrition on yeast composition, fermentative ability and alcohol production. Appl. Environ. Microbiol. 48, 639-646
18. Cheraiti, N., Guezenec, S., and Salmon, J.-M. (2005). Redox interactions between Saccharomyces cerevisiae and Saccharomyces uvarum in mixed culture under enological conditions. Appl. Environ. Microbiol. 71, 255-260. doi: 10.1128/AEM.71.1.255-260.2005
19. Ciani, M., and Comitini, F. (2006). Influence of temperature and oxygen concentration on the fermentation behavior of Candida stellata in mixed fermentation with Saccharomyces cerevisiae. World J. Microbiol. Biotechnol. 22, 619-623. doi: 10.1007/s11274-005-9080-6
20. Ciani, M., and Comitini, F. (2015). Yeast interactions in multi-starter wine fermentation. Curr. Opin. Food Sci. 1, 1-6. doi: 10.1016/j.cofs.2014.07.001
21. Ciani, M., Comitini, F., Mannazzu, I., and Domizio, P. (2010). Controlled mixed culture fermentation: a new perspective on the use of non-Saccharomyces yeasts in winemaking. FEMS Yeast Res. 10, 123-133. doi: 10.1111/j.1567-1364.2009.00579.x
22. Comitini, F., and Ciani, M. (2010). The zymocidial activity of Tetrapisispora phaffii in the control of Hanseniaspora uvarum during the early stages of winemaking. Lett. Appl. Microbiol. 50, 50-56. doi: 10.1111/j.1472-765X.2009.02754.x
23. Comitini, F., De Ingeniis, J., Pepe, L., Mannazzu, I., and Ciani, M. (2004). Pichia anomala and Kluyveromyces wickerhamii killer toxins as new tools against Dekkera/Brettanomyces spoilage yeasts. FEMS Microbiol. Lett. 238, 235-240. doi: 10.1111/j.1574-6968.2004.tb09761.x
24. Comitini, F., Gobbi, M., Domizio, P., Romani, C., Lencioni, L., Mannazzu, I., et al. (2011). Selected non-Saccharomyces wine yeasts in controlled multi starter fermentations with Saccharomyces cerevisiae. Food Microbiol. 28, 873-882. doi: 10.1016/j.fm.2010.12.001
25. Dizzy, M., and Bisson, L. F. (2000). Proteolytic activity of yeast strains during grape juice fermentation. Am. J. Enol. Vitic. 51, 155-167. doi: 10.1007/s10482-015-0578-0
26. Domizio, P., Romani, C., Lencioni, L., Comitini, F., Gobbi, M., Mannazzu, I., et al. (2011). 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. Int. J. Food Microbiol. 147, 170-180. doi: 10.1016/j.ijfoodmicro.2011.03.020
27. Duarte, F. L., Claudia Alves, A., Alemão, M. F., and Baleiras-Couto, M. M. (2013). Influence of red wine fermentation oenological additives on inoculated strain implantation. World J. Microbiol. Biotechnol. 29, 1139-1144. doi: 10.1007/s11274-013-1272-x
28. Fleet, G. H. (2003). Yeast interactions and wine flavor. Int. J. Food Microbiol. 86, 11-22. doi: 10.1016/S0168-1605(03)00245-9
29. Gao, C., and Fleet, G. H. (1988). The effects of temperature and pH on the ethanol tolerance of the wine yeasts, Saccharomyces cerevisiae, Candida stellata and Kloeckera apiculata. J. Appl. Bacteriol. 65, 405-410. doi: 10.1111/j.1365-2672.1988.tb01909.x
30. García-Ríos, E., Gutiérrez, A., Salvadó, Z., Arroyo-López, F. N., and Guillamon, M. (2014). The fitness advantage of commercial wine yeasts in relation to the nitrogen concentration, temperature, and ethanol content under microvinification conditions. Appl. Environ. Microbiol. 80, 704-713. doi: 10.1128/AEM.03405-13
31. Gobbi, M., Comitini, F., Domizio, P., Romani, C., Lencioni, L., Mannazzu, I., et al. (2013). Lachancea thermotolerans and Saccharomyces cerevisiae in simultaneous and sequential co-fermentation: a strategy to enhance acidity and improve the overall quality of wine. Food Microbiol. 33, 271-281. doi: 10.1016/j.fm.2012.10.004
32. Hansen, E. H., Nissen, P., Sommer, P., Nielsen, J. C., and Arneborg, N. (2001). The effect of oxygen on the survival of non-Saccharomyces yeasts during mixed culture fermentations of grape juice with Saccharomyces cerevisiae. J. Appl. Microbiol. 91, 541-547. doi: 10.1046/j.1365-2672.2001.01426.x
33. Howell, K. S., Cozzolino, D., Bartowsky, E. J., Fleet, G. H., and Henschke, P. A. (2006). Metabolic profiling as a tool for revealing Saccharomyces interactions during wine fermentation. FEMS Yeast Res. 6, 91-101. doi: 10.1111/j.1567-1364.2005.00010.x
34. Ivey, M., Massel, M., and Phister, T. G. (2013). Microbial interactions in food fermentations. Annu. Rev. Food Sci. Technol. 4, 141-162. doi: 10.1146/annurev-food-022811-101219
35. Jolly, N. P., Varela, C., and Pretorius, I. S. (2014). Not your ordinary yeast: non-Saccharomyces yeast in wine production uncovered. FEMS Yeast Res. 14, 215-237. doi: 10.1111/1567-1364.12111
36. Kemsawasd, V., Viana, T., Ardo, Y., and Arneborg, N. (2015). Influence of nitrogen sources on growth and fermentation performance of different wine yeast species during alcoholic fermentation. Appl. Microbiol. Biotechnol. 99, 10191-10207. doi: 10.1007/s00253-015-6835-3
37. King, E. S., Swiegers, J. H., Travis, B., Francis, I. L., Bastian, S. E. P., and Pretorius, I. S. (2008). Coinoculated fermentations using Saccharomyces yeasts affect the volatile composition and sensory properties of Vitis vinifera L. cv. Sauvignon Blanc wines. J. Agric. Food Chem. 56, 10829-10837. doi: 10.1021/jf801695h
38. Liu, Y., Rousseaux, S., Tourdot-Mareìchal, R., Sadoudi, M., Gougeon, R., Schmitt-Kopplin, P., et al. (2015). Wine microbiome, a dynamic world of microbial interactions. Crit. Rev. Food Sci. Nutr. doi: 10.1080/10408398.2014.983591 [Epub ahead of print]
39. Lucero, P., Peñalver, E., Moreno, E., and Lagunas, R. (2000). Internal trehalose protects endocytosis from inhibition by ethanol in Saccharomyces cerevisiae. Appl. Environ. Microbiol. 66, 4456-4461. doi: 10.1128/AEM.66.10.4456-4461.2000
40. Madeo, F., Frohlich, E., and Frohlich, K. U. (1997). A yeast mutant showing diagnostic markers of early and late apoptosis. J. Cell Biol. 139, 729-734. doi: 10.1083/jcb.139.3.729
41. Medina, K., Boido, E., Dellacassa, E., and Carrau, F. (2012). Growth of non-Saccharomyces yeasts effects nutrient availability for Saccharomyces cerevisiae during wine fermentation. Int. J. Food Microbiol. 157, 245-250. doi: 10.1016/j.ijfoodmicro.2012.05.012
42. Nissen, P., Nielsen, D., and Arneborg, N. (2003). Viable Saccharomyces cerevisiae cells at high concentrations cause early growth arrest of non- Saccharomyces yeasts in mixed cultures by a cell-cell contact-mediated mechanism. Yeast 20, 331-341. doi: 10.1002/yea.965
43. Nissen, P., Nielsen, D., and Arneborg, N. (2004). The relative glucose uptake abilities of non-Saccharomyces yeasts play a role in their coexistence with Saccharomyces cerevisiae in mixed cultures. Appl. Microbiol. Biotechnol. 64, 543-550. doi: 10.1007/s00253-003-1487-0
44. Oro, L., Ciani, M., and Comitini, F. (2014). Antimicrobial activity of Metschnikowia pulcherrima on wine yeasts. J. Appl. Microbiol. 116, 1209-1217. doi: 10.1111/jam.12446
45. Pérez, F., Ramírez, M., and Regodón, J. A. (2001). Influence of killer strains of Saccharomyces cerevisiae on wine fermentation. Antonie Van Leeuwenhoek 79, 393-399. doi: 10.1023/A:1012034608908
46. Perez-Nevado, F., Albergaria, H., Hogg, T., and Girio, F. (2006). Cellular death of two non-Saccharomyces wine-related yeasts during mixed fermentation with Saccharomyces cerevisiae. Int. J. Food Microbiol. 108, 336-345. doi: 10.1016/j.ijfoodmicro.2005.12.012
47. Perrone, B., Giacosa, S., Rolle, L., Cocolin, L., and Rantsiou, K. (2013). Investigation of the dominance behavior of Saccharomyces cerevisiae strains during wine fermentation. Int. J. Food Microbiol. 165, 156-162. doi: 10.1016/j.ijfoodmicro.2013.04.023
48. Pretorius, I. S. (2000). Tailoring wine yeast for the new millennium: novel approaches to the ancient art of winemaking. Yeast 16, 675-729. doi: 10.1002/1097-0061(20000615)16:8<675::AID-YEA585>3.0.CO;2-B
49. Ramírez, M., Velázquez, R., Maqueda, M., López-Piñeiro, A., and Ribas, J. C. (2015). A new wine Torulaspora delbrueckii killer strain with broad antifungal activity and its toxin-encoding double-stranded RNA virus. Front. Microbiol. 6:983. doi: 10.3389/fmicb.2015.00983
50. Reiter, J., Herker, E., Madeo, F., and Schmitt, M. J. (2005). Viral killer toxins induce caspase-mediated apoptosis in yeast. J. Cell. Biol. 168, 353-358. doi: 10.1083/jcb.200408071
51. Renault, P. E., Albertin, W., and Bely, M. (2013). An innovative tool reveals interaction mechanisms among yeast populations under oenological conditions. Appl. Microbiol. Biotechnol. 97, 4105-4119. doi: 10.1007/s00253-012-4660-5
52. Rodriguez-Porrata, B., Novo, M., Guillamon, J., Rozes, N., Mas, A., and Otero, R. C. (2008). Vitality enhancement of the rehydrated active dry wine yeast. Int. J. Food Microbiol. 126, 116-122. doi: 10.1016/j.ijfoodmicro.2008.05.016
53. Santos, A., San Mauro, M., Bravo, E., and Marquina, D. (2009). PMKT2, a new killer toxin from, and its promising biotechnological properties for control of the spoilage yeast Brettanomyces bruxellensis. Microbiology 155, 624-634. doi: 10.1099/mic.0.023663-0
54. Shimizu, K. (1993). "Killer yeasts, " in Wine Microbiology and Biotechnology, ed. G. H. Fleet (Chur: Harwood Academic), 243-264
55. Taillander, P., Lai, Q. P., Julien-Ortiz, A., and Brandam, C. (2014). Interaction between Torulaspora delbrueckii and Saccharomyces cerevisiae in wine fermentation: influence of inoculation and nitrogen content. World J. Microbiol. Biotechnol. 30, 1959-1967. doi: 10.1007/s11274-014-1618-z
56. Todd, B. E., Fleet, G. H., and Henschke, P. A. (2000). Promotion of autolysis through the interaction of killer and sensitive yeasts: potential application in sparkling wine production. Am. J. Enol. Vitic. 51, 65-72. doi: 10.1023/A:1012027718701
57. Torija, M. J., Rozès, N., Poblet, M., Guillamón, J. M., and Mas, A. (2003). Effects of fermentation temperature on the strain population of Saccharomyces cerevisiae. Int. J. Food Microbiol. 80, 47-53. doi: 10.1016/S0168-1605(02)00144-7
58. Viegas, C. A., Rosa, M. F., Sá-Correia, I., and Novais, J. M. (1989). Inhibition of yeast growth by octanoic and decanoic acids produced during ethanolic fermentation. Appl. Environ. Microbiol. 55, 210-221
59. Vigentini, I., Fabrizio, V., Faccincani, M., Picozzi, C., Comasio, A., and Foschino, R. (2014). Dynamics of Saccharomyces cerevisiae populations in controlled and spontaneous fermentations for Franciacorta D.O.C.G. base wine production. Ann. Microbiol. 64, 639-651. doi: 10.1007/s13213-013-0697-7
60. Villalba, M. L., Susana Sáez, J., del Monaco, S., Lopes, C. A., and Sangorrín, M. P. (2016). TdKT, a new killer toxin produced by Torulaspora delbrueckii effective against wine spoilage yeasts. Int. J. Food Microbiol. 217, 94-100. doi: 10.1016/j.ijfoodmicro.2015.10.006
61. Visser, W., Scheffers, W. A., Batenburg-Van Der Vegte, W. H., and Van Dijken, J. P. (1990). Oxygen requirements of yeasts. Appl. Environ. Microbiol. 56, 3785-3792
62. Williams, K. M., Liu, P., and Fay, J. C. (2015). Evolution of ecological dominance of yeast species in high-sugar environments. Evolution 69, 2079-2095. doi: 10.1111/evo.12707