Early transcriptional response to biotic stress in mixed starter fermentations involving Saccharomyces cerevisiae and Torulaspora delbrueckii

International Journal of Food Microbiology

Volumn 241, Issue , 2017, Pages 60-68

  Tronchoni, Jordi ^a   Curiel, Jose Antonio ^a   Morales, Pilar ^a   Torres Pérez, Rafael ^a   Gonzalez, Ramon ^a  

^a Ctra Burgos Km 6   (Spain)

Author keywords

Biotic stress; Interspecific interaction; Mixed starter; Non Saccharomyces; Wine fermentation

Indexed keywords

CARBON DIOXIDE; HEAT SHOCK PROTEIN; HSP12 PROTEIN, S CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEIN; TRANSCRIPTOME;

ARTICLE; BIOTIC STRESS; COCULTURE; DOWN REGULATION; FERMENTATION; GENE EXPRESSION; GENE MAPPING; GLYCOLYSIS; METABOLIC REGULATION; MIXED CELL CULTURE; NONHUMAN; ORGANISMAL INTERACTION; PRIORITY JOURNAL; RNA SEQUENCE; SACCHAROMYCES CEREVISIAE; TORULASPORA DELBRUECKII; TRANSCRIPTION REGULATION; TRANSCRIPTOMICS; UPREGULATION; WINE; ANALYSIS; CHEMISTRY; DRIED YEAST; FOOD CONTROL; FUNGAL GENOME; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; METABOLISM; MICROBIOLOGY; SEQUENCE ANALYSIS; SPECIES DIFFERENCE; TORULASPORA;

CARBON DIOXIDE; COCULTURE TECHNIQUES; FERMENTATION; FOOD MICROBIOLOGY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, FUNGAL; GENOME, FUNGAL; GLYCOLYSIS; HEAT-SHOCK PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE ANALYSIS, RNA; SPECIES SPECIFICITY; TORULASPORA; TRANSCRIPTION, GENETIC; TRANSCRIPTOME; WINE; YEAST, DRIED;

EID: 84991725981     PISSN: 01681605     EISSN: 18793460     Source Type: Journal    
DOI: 10.1016/j.ijfoodmicro.2016.10.017     Document Type: Article

References (41)

1. Albergaria, H., Francisco, D., Gori, K., Arneborg, N., Gírio, F., Saccharomyces cerevisiae CCMI 885 secretes peptides that inhibit the growth of some non-Saccharomyces wine-related strains. Appl. Microbiol. Biotechnol. 86 (2010), 965–972.
2. Anders, S., Py, P.T., Huber, W., HTSeq—a Python framework to work with high-throughput sequencing data. Bioinformatics 31 (2015), 166–169.
3. Andorra, I., Berradre, M., Mas, A., Esteve-zarzoso, B., Guillamon, J.M., Effect of mixed cultures fermentations on yeast populations and aroma profile. LWT-Food Sci Technol. 49 (2012), 8–13.
4. Avbelj, M., Zupan, J., Kranjc, L., Raspor, P., Quorum-Sensing Kinetics in Saccharomyces cerevisiae: a symphony of ARO genes and aromatic alcohols. J. Agric. Food Chem. 63 (2015), 8544–8550.
5. Balakrishnan, R., Park, J., Karra, K., Hitz, B.C., Binkley, G., Hong, E.L., et al. YeastMine—An Integrated Data Warehouse for Saccharomyces cerevisiae Data as a Multipurpose Tool-kit. 2012, Database-Oxford. 2012 (bar062).
6. Barbosa, C., Mendes-Faia, A., Lage, P., Mira, N.P., Mendes-Ferreira, A., Genomic expression program of Saccharomyces cerevisiae along a mixed-culture wine fermentation with Hanseniaspora guilliermondii. Microb. Cell Factories, 14, 2015, 124.
7. Borneman, A.R., Forgan, A.J., Pretorius, I.S., Chambers, P.J., Comparative genome analysis of a Saccharomcyes cerevisiae wine yeast strain. FEMS Yeast Res. 8 (2008), 1185–1195.
8. Branco, P., Francisco, D., Chambon, C., Hébraud, M., Arneborg, N., Almeida, M.G., et al. Identification of novel GAPDH-derived antimicrobial peptides secreted by Saccharomyces cerevisiae and involved in wine microbial interactions. Appl. Microbiol. Biotechnol. 98 (2014), 843–853.
9. Ciani, M., Comitini, F., Non-Saccharomyces wine yeasts have a promising role in biotechnological approaches to winemaking. Ann. Microbiol. 61 (2011), 25–32.
10. Ciani, M., Morales, P., Comitini, F., Tronchoni, J., Canonico, L., Curiel, J.A., et al. Non-conventional yeast species for lowering ethanol content of wines. Front. Microbiol., 7, 2016, 642.
11. Ciani, M., Capece, A., Comitini, F., Canonico, L., Siesto, G., Romano, P., Yeast interactions in inoculated wine fermentation. Front. Microbiol., 7, 2016, 555.
12. Contreras, A., Curtin, C., Varela, C., Yeast population dynamics reveal a potential “collaboration” between Metschnikowia pulcherrima and Saccharomyces uvarum for the production of reduced alcohol wines during Shiraz fermentation. Appl. Microbiol. Biotechnol. 99 (2015), 1885–1895.
13. Gonzalez, R., Quirós, M., Morales, P., Yeast respiration of sugars by non-Saccharomyces yeast species: a promising and barely explored approach to lowering alcohol content of wines. Trends Food Sci. Technol. 29 (2013), 55–61.
14. Granchi, L., Ganucci, D., Messini, A., Rosellini, D., Dynamics of yeast populations during the early stages of natural fermentations for the production of Brunello di Montalcino wines. Food Technol. Biotechnol. 36 (1998), 313–318.
15. Jarosz, D.F., Brown, J.C.S., Walker, G.A., Datta, M.S., Ung, W.L., Lancaster, A.K., et al. Cross-kingdom chemical communication drives a heritable, mutually beneficial prion-based transformation of metabolism. Cell 158 (2014), 1083–1093.
16. Jarosz, D.F., Lancaster, A.K., Brown, J.C.S., Lindquist, S., An evolutionarily conserved prion-like element converts wild fungi from metabolic specialists to generalists. Cell 158 (2014), 1072–1082.
17. Kim, D., Pertea, G., Trapnell, C., Pimentel, H., Kelley, R., Salzberg, S.L., TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol., 14, 2013, R36.
18. Luo, Z., Van Vuuren, H.J., Functional analyses of PAU genes in Saccharomyces cerevisiae. Microbiology 155 (2009), 4036–4049.
19. Marchal, A., Marullo, P., Durand, C., Moine, V., Dubourdieu, D., Fermentative conditions modulating sweetness in dry wines: genetics and environmental factors influencing the expression level of the Saccharomyces cerevisiae HSP12 gene. J. Agric. Food Chem. 63 (2015), 304–311.
20. Maturano, Y.P., Assof, M., Fabani, M.P., Nally, M.C., Jofré, V., Assaf, L.A.R., et al. Enzymatic activities produced by mixed Saccharomyces and non-Saccharomyces cultures: relationship with wine volatile composition. Anton Leeuw. Int. J. G. 108 (2015), 1239–1256.
21. Milanovic, V., Ciani, M., Oro, L., Comitini, F., Starmerella bombicola influences the metabolism of Saccharomyces cerevisiae at pyruvate decarboxylase and alcohol dehydrogenase level during mixed wine fermentation. Microb. Cell Factories, 11, 2012, 18.
22. Novo, M., Bigey, F., Beyne, E., Galeote, V., Gavory, F., Mallet, S., et al. Eukaryote-to-eukaryote gene transfer events revealed by the genome sequence of the wine yeast Saccharomyces cerevisiae EC1118. Proc. Natl. Acad. Sci. U. S. A. 106 (2009), 16333–16338.
23. Pérez, F., Ramírez, M., Regodón, J.A., Influence of killer strains of Saccharomyces cerevisiae on wine fermentation. Anton Leeuw. Int. J. G. 79 (2001), 393–399.
24. Praekelt, U.M., Meacock, P.A., HSP12, a new small heat shock gene of Saccharomyces cerevisiae: analysis of structure, regulation and function. Mol. Gen. Genet. 223 (1990), 97–106.
25. Rachidi, N., Martinez, M.J., Barre, P., Saccharomyces cerevisiae PAU genes are induced by anaerobiosis. Mol. Microbiol. 35 (2000), 1421–1430.
26. Renault, P., Coulon, J., de Revel, G., Barbe, J.C., Bely, M., Increase of fruity aroma during mixed T. delbrueckii/S. cerevisiae wine fermentation is linked to specific esters enhancement. Int. J. Food Microbiol. 207 (2015), 40–48.
27. Renault, P., Coulon, J., Moine, V., Thibon, C., Bely, M., Enhanced 3-sulfanylhexan-1-ol production in sequential mixed fermentation with Torulaspora delbrueckii/Saccharomyces cerevisiae reveals a situation of synergistic interaction between two industrial strains. Front. Microbiol., 7, 2016, 293.
28. Rivero, D., Berná, L., Stefanini, I., Baruffini, E., Bergerat, A., Csikász-Nagy, A., et al. Hsp12p and PAU genes are involved in ecological interactions between natural yeast strains. Environ. Microbiol. 17 (2015), 3069–3081.
29. Robinson, M.D., Oshlack, A., A scaling normalization method for differential expression analysis of RNA-seq data. Genome Biol., 11, 2010, R25.
30. Robinson, M.D., McCarthy, D.J., Smyth, G.K., EdgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26 (2010), 139–140.
31. Rossignol, T., Dulau, L., Julien, A., Blondin, B., Genome-wide monitoring of wine yeast gene expression during alcoholic fermentation. Yeast 20 (2003), 1369–1385.
32. Rossouw, D., Toit Du, M., Bauer, F.F., The impact of co-inoculation with Oenococcus oeni on the transcriptome of Saccharomyces cerevisiae and on the flavour-active metabolite profiles during fermentation in synthetic must. Food Microbiol. 29 (2012), 121–131.
33. Salvadó, Z., Arroyo-López, F.N., Barrio, E., Querol, A., Guillamón, J.M., Quantifying the individual effects of ethanol and temperature on the fitness advantage of Saccharomyces cerevisiae. Food Microbiol. 28 (2011), 1155–1161.
34. Smid, E.J., Lacroix, C., Microbe-microbe interactions in mixed culture food fermentations. Curr. Opin. Biotechnol. 24 (2013), 148–154.
35. Taillandier, P., Lai, Q.P., Julien-Ortiz, A., Brandam, C., Interactions between Torulaspora delbrueckii and Saccharomyces cerevisiae in wine fermentation: influence of inoculation and nitrogen content. World J. Microbiol. Biotechnol. 30 (2014), 1959–1967.
36. Trapnell, C., Hendrickson, D.G., Sauvageau, M., Goff, L., Rinn, J.L., Pachter, L., Differential analysis of gene regulation at transcript resolution with RNA-seq. Nat. Biotechnol. 31 (2013), 46–53.
37. van Vuuren, H., Jacobs, C.J., Killer yeasts in the wine industry: a review. Am. J. Enol. Vitic. 43 (1992), 119–128.
38. Velázquez, R., Zamora, E., Álvarez, M.L., Hernández, L.M., Ramírez, M., Effects of new Torulaspora delbrueckii killer yeasts on the must fermentation kinetics and aroma compounds of white table wine. Front. Microbiol., 6, 2015, 1222.
39. Wang, C., Mas, A., Esteve-Zarzoso, B., Interaction between Hanseniaspora uvarum and Saccharomyces cerevisiae during alcoholic fermentation. Int. J. Food Microbiol. 206 (2015), 67–74.
40. Wang, C., Mas, A., Esteve-Zarzoso, B., The interaction between Saccharomyces cerevisiae and non-Saccharomyces yeast during alcoholic fermentation is species and strain specific. Front. Microbiol., 7, 2016, 502.
41. Yang, X., Li, J., Lee, Y., Lussier, Y.A., GO-Module: functional synthesis and improved interpretation of Gene Ontology patterns. Bioinformatics 27 (2011), 1444–1446.