Comparison of fermentation and wines produced by inoculation of Hanseniaspora vineae and Saccharomyces cerevisiae

Frontiers in Microbiology

Volumn 7, Issue MAR, 2016, Pages

  Lleixà, Jessica ^a   Martín, Valentina ^b   Portillo, María del C ^a   Carrau, Francisco ^b   Beltran, Gemma ^a   Mas, Albert ^a  

^a UNIVERSITAT ROVIRA I VIRGILI   (Spain)

^b UNIVERSIDAD DE LA REPÚBLICA   (Uruguay)

Author keywords

Alcoholic fermentation; Hanseniaspora; Massive sequencing; Non Saccharomyces; PCR DGGE

Indexed keywords

AROMA; FERMENTATION; FUNGAL CELL CULTURE; HANSENIASPORA; HONEY; INOCULATION; MICROFLORA; PERCEPTION; POLYMERASE CHAIN REACTION; POPULATION DYNAMICS; SACCHAROMYCES CEREVISIAE; WINE;

EID: 84964331061     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2016.00338     Document Type: Article

References (36)

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. Andorrà, I., Landi, S., Mas, A., Guillamón, J. M., and Esteve-Zarzoso, B. (2008). Effect of enological practices on microbial populations using culture-independent techniques. Food Microbiol. 25, 849-856. doi: 10.1016/j.fm.2008.05.005.
3. Andorrà, I., Monteiro, M., Esteve-Zarzoso, B., Albergaria, H., and Mas, A. (2011). Analysis and direct quantification of Saccharomyces cerevisiae and Hanseniaspora guilliermondii populations during alcoholic fermentation by fluorescence in situ hybridisation, flow cytometry and quantitative PCR. Food Microbiol. 28, 1483-1491. doi: 10.1016/j.fm.2011.08.009.
4. Beltran, G., Torija, M. J., Novo, M., Ferrer, N., Poblet, M., Guillamón, J. M., et al. (2002). Analysis of yeast populations during alcoholic fermentation: a six year follow-up study. Syst. Appl. Microbiol. 25, 287-293. doi: 10.1078/0723-2020-00097.
5. Boido, E. (2002). Modificaciones Producidas por la Fermentación Maloláctica en la Fracción Aromática de los Vinos Tannat. Ph. D., thesis. Universidad de la República, Facultad de Química, Montevideo, Uruguay.
6. Boido, E., Lloret, A., Medina, K., Fariña, L., Carrau, F., Versini, G., et al. (2003). Aroma composition of Vitis vinifera cv. Tannat: the typical red wine from Uruguay. J. Agric. Food Chem. 51, 5408-5413. doi: 10.1021/jf030087i.
7. Cabtree, H. G. (1929). Observations on the carbohydrate metabolism of tumours. Biochem. J. 23, 536-545. doi: 10.1042/bj0230536.
8. Caporaso, J. G., Bittinger, K., Bushman, F. D., DeSantis, T. Z., Andersen, G. L., and Knight, R. (2010b). PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinformatics 26, 266-267. doi: 10.1093/bioinformatics/btp636.
9. Caporaso, J. G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F. D., Costello, E. K., et al. (2010a). QIIME allows analysis of highthroughput community sequencing data. Nat. Methods 7, 335-336. doi: 10.1038/nmeth.f.303.
10. Chemidlin Prévost-Bouré, N., Christen, R., Dequiedt, S., Mougel, C., Lelièvre, M., Jolivet, C., et al. (2011). Validation and application of a PCR primer set to quantify fungal communities in the soil environment by real time quantitative PCR. PLoS ONE 6:e24166. doi: 10.1371/journal.pone.0024166.
11. DeSantis, T. Z., Hugenholtz, P., Larsen, N., Rojas, M., Brodie, E. L., Keller, K., et al. (2006). Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl. Environ. Microb. 72, 5069-5072. doi: 10.1128/AEM.03006-05.
12. Edgar, R. C. (2010). Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460-2461. doi: 10.1093/bioinformatics/btq461.
13. Esteve-Zarzoso, B., Belloch, C., Uruburu, F., and Querol, A. (1999). Identification of yeasts by RFLP analysis of the 5.8S rRNA gene and the two ribosomal internal transcribed spacers. Int. J. Syst. Bacteriol. 49, 329-337. doi: 10.1099/00207713-49-1-329.
14. Fariña, L., Villar, V., Ares, G., Carrau, F., Dellacassa, E., and Boido, E. (2015). Volatile composition and aroma profile of Uruguayan Tannat wines. Food Res. Int. 69, 244-255. doi: 10.1016/j.foodres.2014.12.029.
15. Fleet, G. H. (2008). Wine yeasts for the future. FEMS Yeast Res. 8, 979-995. doi: 10.1111/j.1567-1364.2008.00427.x.
16. Haas, B. J., Gevers, D., Earl, A. M., Feldgarden, M., Ward, D. V., Giannoukos, G., et al. (2011). Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons. Genome Res. 21, 494-504. doi: 10.1101/gr.112730.110.
17. Jolly, N. P., Varela, C., and Pretorius, I. S. (2014). Not your ordinary yeast: non-Saccharomyces yeasts in wine production uncovered. FEMS Yeast Res. 14, 215-237. doi: 10.1111/1567-1364.12111.
18. Kurtzman, C. P., and Robnett, C. J. (1998). Identification and phylogeny of ascomycetous yeasts from analysis of nuclear large subunit (26S) ribosomal DNA partial sequences. Antonie van Leeuwenhoek 73, 331-371. doi: 10.1023/A:1001761008817.
19. Legras, J. L., and Karst, F. (2003). Optimisation of interdelta analysis for Saccharomyces cerevisiae strain characterization. FEMS Microbiol. Lett. 221, 249-255. doi: 10.1016/S0378-1097(03)00205-2.
20. Maturano, P. Y., Rodríguez Assaf, L. A., Toro, E. M., Nally, C. M., Vallejo, M., Castellanos de Figueroa, L. I., et al. (2012). Multi-enzyme production by pure and mixed cultures of Saccharomyces and non-Saccharomyces yeasts during wine fermentation. Int. J. Food Microbiol. 155, 43-50. doi: 10.1016/j.ijfoodmicro.2012.01.015.
21. 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.
22. Meroth, C. B., Hammes, W. P., and Hertel, C. (2003). Identification and population dynamics of yeasts in Sourdough fermentation processes by using PCR-denaturing gradient gel electrophoresis. Appl. Environ. Microbiol. 69, 7453-7461. doi: 10.1128/AEM.69.12.7453-7461.2003.
23. Millet, V., and Lonvaud-Funel, A. (2000). The viable but non-culturable of wine micro-organisms during storage. Lett. Appl. Microbiol. 30, 136-141. doi: 10.1046/j.1472-765x.2000.00684.x.
24. Mills, D. A., Johannsen, E. A., and Cocolin, L. (2002). Yeast diversity and persistence in botrytis-affected wine fermentations. Appl. Environ. Microbiol. 68, 4884-4893. doi: 10.1128/AEM.68.10.4884-4893.2002.
25. Pérez-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.
26. Prakitchaiwattana, C. J., Fleet, G. H., and Heard, G. M. (2004). Application and evaluation of denaturing gradient gel electrophoresis to analyse the yeast ecology of wine grapes. FEMS Yeast Res. 4, 865-877. doi: 10.1016/j.femsyr.2004.05.004.
27. 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.
28. Price, M. N., Dehal, P. S., and Arkin, A. P. (2009). FastTree: computing large minimum evolution trees with profiles instead of a distance matrix. Mol. Biol. Evol. 26, 1641-1650. doi: 10.1093/molbev/msp077.
29. Pruesse, E., Quast, C., Knittel, K., Fuchs, B. M., Ludwig, W., Peplies, J., et al. (2007). SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res. 35, 7188-7196. doi: 10.1093/nar/gkm864.
30. Strauss, M. L. A., Jolly, N. P., Lambrechts, M. G., and van Rensburg, P. (2001). Screening for the production of extracellular hydrolytic enzymes by non-Saccharomyces wine yeasts. J. Appl. Microbiol. 91, 182-190. doi: 10.1046/j.1365-2672.2001.01379.x.
31. Swangkeaw, J., Vichitphan, S., Butzke, C. E., and Vichitphan, K. (2011). Characterization of ß-glucosidases from Hanseniaspora sp. and Pichia anomala with potentially aroma-enhancing capabilities in juice and wine. World J. Microbiol. Biotechnol. 27, 423-430. doi: 10.1007/s11274-010-0474-8.
32. Torija, M. J., Rozès, N., Poblet, M., Guillamón, J. M., and Mas, A. (2001). Yeast population dynamics in spontaneous fermentations: comparison between two different wine-producing areas over a period of three years. Antonie van Leeuwenhoek 79, 345-352. doi: 10.1023/A:1012027718701.
33. 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.
34. Viana, F., Gil, J. V., Vallés, S., and Manzanares, P. (2009). Increasing the levels of 2-phenethyl acetate in wine through the use of a mixed culture of Hanseniaspora osmophila and Saccharomyces cerevisiae. Int. J. Food Microbiol. 135, 68-74. doi: 10.1016/j.ijfoodmicro.2009.07.025.
35. Wang, C., Esteve-Zarzoso, B., Cocolin, L., Mas, A., and Rantsiou, K. (2015). Viable and culturable populations of Saccharomyces cerevisiae, Hanseniaspora uvarum and Starmerella bacillaris (synonym Candida zemplinina) during Barbera must fermentation. Food Res Int. 78, 195-200. doi: 10.1016/j.foodres.2015.10.014.
36. Wang, Q., Garrity, G. M., Tiedje, J. M., and Cole, J. R. (2007). Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microb. 73, 5261-5267. doi: 10.1128/AEM.00062-07.