The oenological potential of hanseniaspora uvarum in simultaneous and sequential co-fermentation with Saccharomyces cerevisiae for industrial wine production

Frontiers in Microbiology

Volumn 7, Issue MAY, 2016, Pages

  Tristezza, Mariana ^a   Tufariello, Maria ^a   Capozzi, Vittorio ^b   Spano, Giuseppe ^b   Mita, Giovanni ^a   Grieco, Francesco ^a  

^a CNR   (Italy)

^b UNIVERSITY OF FOGGIA   (Italy)

Author keywords

Co inoculation; Hanseniaspora uvarum; Mixed fermentations; Oenological non Saccharomyces; Saccharomyces cerevisiae; Sequential inoculation; Starter multi strains; Wine alcoholic fermentation

Indexed keywords

GENOMIC DNA;

ARTICLE; CHEMICAL ANALYSIS; CONTROLLED STUDY; EXTRACTIVE FERMENTATION; FUNGAL STRAIN; HANSENIASPORA UVARUM; INDUSTRIAL PRODUCTION; INFRARED SPECTROSCOPY; INOCULATION; MASS FRAGMENTOGRAPHY; MICROBIAL GROWTH; MICROBIAL POPULATION DYNAMICS; MICROFERMENTATION; ORGANOLEPTIC PROPERTY; PRINCIPAL COMPONENT ANALYSIS; SACCHAROMYCES CEREVISIAE; WINE; WINE INDUSTRY; YEAST;

EID: 84973520168     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2016.00670     Document Type: Article

References (74)

1. Andorrà, I., Berradre, M., Rozès, N., Mas, A., Guillamón, J. M., and Esteve-Zarzoso, B. (2010). Effect of pure and mixed cultures of the main wine yeast species on grape must fermentations. Eur. Food Res. Technol. 231, 215-224. doi: 10.1007/s00217-010-1272-0
2. Bleve, G., Lezzi, C., Chiriatti, M. A., D'Ostuni, I., Tristezza, M., Di Venere, D., et al. (2011). Selection of non-conventional yeasts and their use in immobilized form for the bioremediation of olive oil mill wastewaters. Bioresour. Technol. 102, 982-989. doi: 10.1016/j.biortech.2010.09.059
3. Capone, S., Tufariello, M., and Siciliano, P. (2013). Analytical characterization of Negroamaro red wines by "Aroma Wheels". Food Chem. 141, 2906-2915. doi: 10.1016/j.foodchem.2013.05.105
4. Capozzi, V., Garofalo, C., Chiriatti, M. A., Grieco, F., and Spano, G. (2015). Microbial terroir and food innovation: the case of yeast biodiversity in wine. Microbiol. Res. 181, 75-83. doi: 10.1016/j.micres.2015.10.005
5. Capozzi, V., and Spano, G. (2011). Food microbial biodiversity and "Microbes of Protected Origin". Front. Microbiol. 2:237. doi: 10.3389/fmicb.2011.00237
6. Caridi, A., and Ramondino, D. (1999). Biodiversità fenotipica in ceppi di Hanseniaspora di origine enologica. Enotecnico 45, 71-74.
7. Ciani, M., Beco, L., and Comitini, F. (2006). Fermentation behavior and metabolic interactions of multistarter wine yeast fermentations. Int. J. Food Microbiol. 108, 239-245. doi: 10.1016/j.ijfoodmicro.2005.11.012
8. 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
9. Ciani, M., and Fatichenti, F. (1999). Selective sugar consumption by apiculate yeasts. Lett. Appl. Microbiol. 28, 203-206. doi: 10.1046/j.1365-2672.1999.00505.x
10. Ciani, M., and Ferraro, L. (1996). Enhanced glycerol content in wines made with immobilized Candida stellata cells. Appl. Environ. Microbiol. 62, 128-132.
11. Ciani, M., and Maccarelli, F. (1998), Enological properties of non-Saccharomyces yeasts associated with wine-making. World J. Microbiol. Biotechnol. 14, 199-203. doi: 10.1023/A:1008825928354
12. Comitini, F., Gobbi, M., Domizio, P., Romani, C., Lencioni, L., Mannazzu, I., et al. (2011). Selected non-Saccharomyces wine yeasts in controlled multistarter fermentations with Saccharomyces cerevisiae. Food Microbiol. 28, 873-882. doi: 10.1016/j.fm.2010.12.001
13. De Benedictis, M., Bleve, G., Grieco, F., Tristezza, M., Tufariello, M., and Grieco, F. (2011), An optimized procedure for the enological selection of non-Saccharomyces starter cultures. Anton. Leeuw. Int. J. G. 99, 189-200. doi: 10.1007/s10482-010-9475-8
14. Domizio, P., Lencioni, L., Ciani, M., Di Blasi, S., Pontremolesi, C., and Sabatelli, M. P. (2007). Spontaneous and inoculated yeast population dynamics and their effect on organoleptic characters of Vinsanto wine under different process conditions. Int. J. Food Microbiol. 115, 281-289. doi: 10.1016/j.ijfoodmicro.2006.10.052
15. 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
16. Erten, H. (2002). Relations between elevated temperatures and fermentation behaviour of Kloeckera apiculata and Saccharomyces cerevisiae associated with winemaking in mixed cultures. World J. Microbiol. Biotechnol. 18, 373-378. doi: 10.1023/A:1015221406411
17. Etievant, P. X. (1991). "Wine," in Volatile Compounds of Food and Beverages, ed H. Maarse (New York, NY: Dekker), 483-546.
18. Ferreira, V., Lopez, R., and Cacho, J. F. (2000). Quantitative determination of the odorants of young red wines from different grape varieties. J. Sci. Food Agric. 80, 1659-1667. doi: 10.1002/1097-0010(20000901)80:11<1659::AID-JSFA693>3.0.CO;2-6
19. Fleet, G. H. (2003). Yeast interactions and wine flavor. Int. J. Food Microbiol. 86, 11-22. doi: 10.1016/S0168-1605(03)00245-9
20. Fleet, G. H. (2008). Wine yeast for the future. FEMS Yeast Res. 8, 979-995. doi: 10.1111/j.1567-1364.2008.00427.x
21. Fleet, G. H., and Heard, G. M. (1993). "Yeasts: growth during fermentation" in Wine Microbiology and Biotechnology, ed G. H. Fleet (Philadelphia, PA: Harwood), 27-55.
22. Garavaglia, J., de Souza Schneider, R. D. C., Mendes, S. D. C., Welke, J. E., Zini, C. A., Caramão, E. B., et al. (2015). Evaluation of Zygosaccharomyces bailii BCV 08 as a co-starter in wine fermentation for the improvement of ethyl esters production. Microbiol. Res. 173, 59-65. doi: 10.1016/j.micres.2015.02.002
23. Garde-Cerdán, T., and Ancín-Azpilicueta, C. (2006). Contribution of wild yeasts to the formation of volatile compounds in inoculated wine fermentations. Eur. Food Res. Technol. 222, 15-25. doi: 10.1007/s00217-005-0029-7
24. Garofalo, C., El Khoury, M., Lucas, P., Bely, M., Russo, P., Spano, G., et al. (2015). Autochthonous starter cultures and indigenous grape variety for regional wine production. J. Appl. Microbiol. 118, 1395-1408. doi: 10.1111/jam.12789
25. Gil, M., Cabellos, J. M., Arroyo, T., and Prodanov, M. (2006). Characterization of the volatile fraction of young wines from the Denomination of Origin "Vinos de Madrid" (Spain). Anal. Chim. Acta 563, 145-153. doi: 10.1016/j.aca.2005.11.060
26. 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
27. Gómez-Mínguez, M. J., Cacho, J. F., Ferreira, V., Vicario, I. M., and Heredia, F. J. (2007). Volatile components of Zalema white wines. Food Chem. 100, 1464-1473. doi: 10.1016/j.foodchem.2005.11.045
28. Grieco, F., Tristezza, M., Vetrano, C., Bleve, G., Panico, E., Grieco, F., et al. (2011). Exploitation of autochthonous micro-organism potential to enhance the quality of Apulian wines. Ann. Microbiol. 61, 67-73. doi: 10.1007/s13213-010-0091-7
29. Guth, H. (1997). Identification of character impact odorants of different white wine varieties. J. Agric. Food Chem. 45, 3022-3026. doi: 10.1021/jf9608433
30. Hammer, Ø., Harper, D. A. T., and Ryan, P. D. (2001). PAST: Paleontological Statistics Software Package for education and data analysis. Palaeontol. Electron. 4, 9.
31. Heard, G. M., and Fleet, G. H. (1985). Growth of natural yeast flora during the fermentation of inoculated wines. Appl. Environ. Microbiol. 50, 727-728.
32. Jacobs, C. J., Fourie, I., and van Vuuren, H. J. J. (1988). Occurrence and detection of killer yeasts on Chenin Blanc grapes and grape skins. S. Afr. J. Enol. Vitic. 9, 28-31.
33. Jolly, N. P., Augustyn, O. P. H., and Pretorius, I. S. (2006). The role and use of non-Saccharomyces yeasts in wine production. S. Afr. J. Enol. Vitic. 27, 15-39.
34. Lambrechts, M. G., and Pretorius, I. S. (2000). Yeast and its importance to wine aroma. S. Afr. J. Enol. Vitic. 21, 97-129.
35. Lu, Y., Huang, D., Lee, P. R., and Liu, S.-Q. (2015). Assessment of volatile and non-volatile compounds in durian wines fermented with four commercial non-Saccharomyces yeasts. J. Sci. Food Agric. 96, 1511-1521. doi: 10.1002/jsfa.7253
36. Mallouchos, A., Skandamis, P., Loukatos, P., Komaitis, M., Koutinas, A., and Kanellaki, M. (2003). Volatile compounds of wines produced by cells immobilized on grape skins. J. Agric. Food Chem. 51, 3060-3066. doi: 10.1021/jf026177p
37. Marchal, A., Marullo, P., Moine, V., and Dubourdieu, D. (2011). Influence of yeast macromolecules on sweetness in dry wines: role of the Saccharomyces cerevisiae protein Hsp12. J. Agric. Food Chem. 59, 2004-2010. doi: 10.1021/jf103710x
38. Masneuf-Pomarede, I., Bely, M., Marullo, P., and Albertin, W. (2016). The genetics of non-conventional wine yeasts: current knowledge and future challenges. Front. Microbiol. 6:1563. doi: 10.3389/fmicb.2015.01563
39. Medina, K., Boido, E., Fariña, L., Gioia, O., Gomez, M. E., Barquet, M., et al. (2013). Increased flavour diversity of Chardonnay wines by spontaneous fermentation and co-fermentation with Hanseniaspora vineae. Food Chem. 141, 2513-2521. doi: 10.1016/j.foodchem.2013.04.056
40. Mendoza, L., and Farías, M. E. (2010). Improvement of wine organoleptic characteristics by non-Saccharomyces yeasts. Curr. Res. Technol. Ed. Top. Appl. Microbiol. Microb. Biotechnol. 2, 908-919.
41. Mendoza, L. M., Manca de Nadra, M. C., and Farias, M. F. (2007). Kinetics and metabolic behavior of a composite culture of Kloeckera apiculata and Saccharomyces cerevisiae wine related strains. Biotechnol. Lett. 29, 1057-1063. doi: 10.1007/s10529-007-9355-0
42. Mendoza, L. M., Merín, M. G., Morata, V. I., and Farías, M. E. (2011). Characterization of wines produced by mixed culture of autochthonous yeasts and Oenococcus oeni from the northwest region of Argentina. J. Ind. Microbiol. Biotechnol. 38, 1777-1785. doi: 10.1007/s10295-011-0964-1
43. Mingorance-Cazorla, L., Clemente-Jiménez, J. M., Martinez-Rodriguez, S., Las Heras-Vazquez, F. J., and Rodriguez-Vico, F. (2003). Contribution of different natural yeasts to the aroma of two alcoholic beverages. World J. Microbiol. Biotechnol. 19, 297-304. doi: 10.1023/A:1023662409828
44. Moreira, N., Mendes, F., de Pinho, P. G., Hogg, T., and Vasconcelos, I. (2008). Heavy sulphur compounds, higher alcohols and esters production profile of Hanseniaspora uvarum and Hanseniaspora guilliermondii grown as pure and mixed cultures in grape must. Int. J. Food Microbiol. 124, 231-238. doi: 10.1016/j.ijfoodmicro.2008.03.025
45. Moreira, N., Mendes, F., Hogg, T., and Vasconcelos, I. (2005). Alcohols, esters and heavy sulphur compounds production by pure and mixed cultures of apiculate wine yeasts. Int. J. Food Microbiol. 103, 285-294. doi: 10.1016/j.ijfoodmicro.2004.12.029
46. Moreira, N., Pina, C., Mendes, F., Couto, J. A., Hogg, T., and Vasconcelos, I. (2011). Volatile compounds contribution of Hanseniaspora guilliermondii and Hanseniaspora uvarum during red wine vinifications. Food Control. 22, 662-667. doi: 10.1016/j.foodcont.2010.07.025
47. Pallmann, C., Brown, J., Olineka, T., Cocolin, L., Mills, D., and Bisson, L. (2001). Use of WL medium to profile native flora fermentations. Am. J. Enol. Vit. 52, 198-203.
48. Pérez-Coello, M. S., Briones Pérez, A. I., Ubeda Iranzo, J. F., and Martin Alvarez, P. J. (1999). Characteristics of wines fermented with different Saccharomyces cerevisiae strains isolated from the La Mancha region. Food Microbiol. 16, 563-573. doi: 10.1006/fmic.1999.0272
49. Rantsiou, K., Dolci, P., Giacosa, S., Torchio, F., Tofalo, R., Torriani, S., et al. (2012). Candida zemplinina can reduce acetic acid produced by Saccharomyces cerevisiae in sweet wine fermentations. Appl. Environ. Microbiol. 78, 1987-1994. doi: 10.1128/AEM.06768-11
50. Rapp, A. (1990). Natural flavours of wine: correlation between instrumental analysis and sensory perception. J. Anal. Chem. 337, 777-785. doi: 10.1007/BF00322252
51. Rapp, A., and Mandery, H. (1986). Wine aroma. Experientia 42, 873-883. doi: 10.1007/BF01941764
52. Rapp, A., and Versini, G. (1991). "Influence of nitrogen compounds in grapes on aroma compounds in wine," in Proceedings of the International Symposium on Nitrogen in Grapes and Wine, Seattle, USA (Davis, CA: American Society of Enology and Viticulture), 156-164.
53. Rocha, S. M., Rodrigues, F., Coutinho, P., Delgadillo, I., and Coimbra, M. A. (2004). Volatile composition of Baga red wine assessment of the identification of the would-be impact odourants. Anal. Chim. Acta 513, 257-262. doi: 10.1016/j.aca.2003.10.009
54. Rojas, V., Gil, J. V., Pinaga, F., and Manzanares, P. (2001). Studies on acetate ester production by non-Saccharomyces wine yeasts. Int. J. Food Microbiol. 70, 283-289. doi: 10.1016/S0168-1605(01)00552-9
55. Rojas, V., Gil, J. V., Piñaga, F., and Manzanares, P. (2003). Acetate ester formation in wine by mixed cultures in laboratories fermentations. Int. J. Food Microbiol. 86, 181-188. doi: 10.1016/S0168-1605(03)00255-1
56. Romano, P., Fiore, C., Paraggio, M., Caruso, M., and Capece, A. (2003). Function of yeast species and strains in wine flavour. Int. J. Food Microbiol. 86, 169-180. doi: 10.1016/S0168-1605(03)00290-3
57. Romano, P., Suzzi, G., Comi, G., and Zironi, R. (1992). Higher alcohol and acetic acid production by apiculate wine yeasts. J. Appl. Bacteriol. 73, 126-130. doi: 10.1111/j.1365-2672.1992.tb01698.x
58. Romano, P., Suzzi, G., Comi, G., Zironi, R., and Maifreni, M. (1997). Glycerol and other fermentation products of apiculate wine yeasts. J. Appl. Microbiol. 82, 615-618. doi: 10.1111/j.1365-2672.1997.tb02870.x
59. Saurina, J. (2010). Characterization of wines using compositional profiles and chemometric. Trends Anal. Chem. 29, 234-245. doi: 10.1016/j.trac.2009.11.008
60. Spano, G., Russo, P., Lonvaud-Funel, A., Lucas, P., Alexandre, H., Grandvalet, C., et al. (2010). Biogenic amines in fermented foods. Eur. J. Clin. Nutr. 64(suppl. 3), S95-S100. doi: 10.1038/ejcn.2010.218
61. Suárez-Lepe, J. A., and Morata, A. (2012). New trends in yeast selection for winemeking. Trends Food Sci. Technol. 23, 39-50. doi: 10.1016/j.tifs.2011.08.005
62. Suzzi, G., Schirone, M., Sergi, M., Marianella, R. M., and Fasoli, G., Aguzzi, et al. (2012). Multistarter from organic viticulture for red wine Montepulciano d'Abruzzo production. Front. Microbiol 3:135. doi: 10.3389/fmicb.2012.00135
63. Swiegers, J. H., Bartowsky, E. J., Henschke, P. A., and Pretorius, I. S. (2005). Yeast and bacterial modulation of wine aroma and flavour. Aust. J. Grape Wine Res. 11, 139-173. doi: 10.1111/j.1755-0238.2005.tb00285.x
64. Swiegers, J. H., and Pretorius, I. S. (2005). Yeast modulation of wine flavor. Adv. Appl. Microbiol. 57, 131-175. doi: 10.1016/S0065-2164(05)57005-9
65. Tofalo, R., Schirone, M., Torriani, S., Rantsiou, K., Cocolin, L., Perpetuini, G., et al. (2012). Diversity of Candida zemplinina strains from grapes and Italian wines. Food Microbiol. 29, 18-26. doi: 10.1016/j.fm.2011.08.014
66. Toro, M. E., and Vazquez, F. (2002). Fermentation behaviour of controlled mixed and sequential cultures of Candida cantarellii and Saccharomyces cerevisiae wine yeasts. World J. Microbiol. Biotechnol. 18, 347-354. doi: 10.1023/A:1015242818473
67. Tristezza, M., Gerardi, C., Logrieco, A., and Grieco, F. (2009). An optimized protocol for the production of interdelta markers in Saccharomyces cerevisiae by using capillary electrophoresis. J. Microbiol. Meth. 78, 286-291. doi: 10.1016/j.mimet.2009.06.012
68. Tristezza, M., Vetrano, C., Bleve, G., Grieco, F., Tufariello, M., Quarta, A., et al. (2012). Autochthonous fermentation starters for the industrial production of Negroamaro wines. J. Ind. Microbiol. Biotechnol. 39, 81-92. doi: 10.1007/s10295-011-1002-z
69. Tristezza, M., Vetrano, C., Bleve, G., Spano, G., Capozzi, V., Logrieco, A., et al. (2013). Biodiversity and safety aspects of yeast strains characterized from vineyards and spontaneous fermentations in the Apulia Region, Italy. Food Microbiol. 36, 335-342. doi: 10.1016/j.fm.2013.07.001
70. Tufariello, M., Capone, S., and Siciliano, P. (2012). Volatile components of Negroamaro red wines produced in Apulian Salento area. Food Chem. 132, 2155-2164. doi: 10.1016/j.foodchem.2011.11.122
71. Viana, F., Belloch, C., Vallés, S., and Manzanares, P. (2011). Monitoring a mixed starter of Hanseniaspora vineae-Saccharomyces cerevisiae in natural must: impact on 2-phenylethyl acetate production. Int. J. Food Microbiol. 151, 235-240. doi: 10.1016/j.ijfoodmicro.2011.09.005
72. Viana, F., Gil, J. V., Genovés, S., Vallés, S., and Manzanares, P. (2008). Rational selection of non-Saccharomyces wine yeast for mixed starters based on ester formation and enological traits. Food Microbiol. 25, 778-785. doi: 10.1016/j.fm.2008.04.015
73. Wang, C., Mas, A., and Esteve-Zarzoso, B. (2015). Interaction between Hanseniaspora uvarum and Saccharomyces cerevisiae during alcoholic fermentation. Int. J. Food Microbiol. 206, 67-74. doi: 10.1016/j.ijfoodmicro.2015.04.022
74. Zironi, R., Romano, P., Suzzi, G., Battistuta, F., and Comi, G. (1993). Volatile metabolites produced in wine by mixed and sequential cultures of Hanseniaspora guilliermondii or Kloeckera apiculata and Saccharomyces cerevisiae. Biotechnol. Lett. 15, 235-238. doi: 10.1007/BF00128311