Bridging the gap: linking Torulaspora delbrueckii genotypes to fermentation phenotypes and wine aroma

Silva-Sousa, Flávia; Oliveira, Bruna; Franco-Duarte, Ricardo; Camarasa, Carole; João Sousa, Maria

doi:10.1093/femsyr/foae034

Title: Bridging the gap: linking Torulaspora delbrueckii genotypes to fermentation phenotypes and wine aroma

Journal Article · 05 November 2024 · FEMS Yeast Research

DOI: https://doi.org/10.1093/femsyr/foae034 · OSTI ID:2480761

; Oliveira, Bruna;

;

Abstract Climate change and consumer preferences are driving innovation in winemaking, with a growing interest in non-Saccharomyces species. Among these, Torulaspora delbrueckii (Td) has gained recognition for its ability to reduce volatile acidity and enhance aromatic complexity in wine. However, knowledge regarding its phenotypic and genomic diversity impacting alcoholic fermentation remains limited. Aiming to elucidate the metabolic differences between Td and Saccharomyces cerevisiae (Sc) and the Td intraspecies diversity, we conducted a comprehensive metabolic characterization of 15 Td strains. This analysis delved beyond standard fermentation parameters (kinetics and major metabolites production) to explore non-conventional aromas and establish genotype-phenotype links. Our findings confirmed that most Td strains produce less acetic acid and more succinate and glycerol than Sc. The overall aromatic profiles of Td strains differed from Sc, exhibiting higher levels of monoterpenes and higher alcohols, while producing less acetate esters, fatty acids, their corresponding ethyl esters, and lactones. Moreover, we identified the absence of genes responsible for specific aroma profiles, such as decreased ethyl esters production, as well as the absence of cell wall genes, which might negatively affect Td performance when compared to Sc. This work highlights the significant diversity within Td and underscores potential links between its genotype and phenotype.

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Sponsoring Organization:: USDOE Office of Nuclear Energy (NE), Nuclear Fuel Cycle and Supply Chain

OSTI ID:: 2480761

Journal Information:: FEMS Yeast Research, Journal Name: FEMS Yeast Research Vol. 24; ISSN 1567-1364

Publisher:: Oxford University PressCopyright Statement

Country of Publication:: United Kingdom

Language:: English

References (44)

Dynamic analysis of physiological properties of Torulaspora delbrueckii in wine fermentations and its incidence on wine quality Belda, Ignacio; Navascués, Eva; Marquina, Domingo Applied Microbiology and Biotechnology, Vol. 99, Issue 4 https://doi.org/10.1007/s00253-014-6197-2	journal	November 2014
Combined effects of nutrients and temperature on the production of fermentative aromas by Saccharomyces cerevisiae during wine fermentation Rollero, Stéphanie; Bloem, Audrey; Camarasa, Carole Applied Microbiology and Biotechnology, Vol. 99, Issue 5 https://doi.org/10.1007/s00253-014-6210-9	journal	November 2014
The impact of Torulaspora delbrueckii yeast in winemaking Benito, Santiago Applied Microbiology and Biotechnology, Vol. 102, Issue 7 https://doi.org/10.1007/s00253-018-8849-0	journal	February 2018
Engineering of the glycerol decomposition pathway and cofactor regulation in an industrial yeast improves ethanol production Zhang, Liang; Tang, Yan; Guo, Zhongpeng Journal of Industrial Microbiology and Biotechnology, Vol. 40, Issue 10 https://doi.org/10.1007/s10295-013-1311-5	journal	October 2013
Biological acidification during grape must fermentation using mixed cultures of Kluyveromyces thermotolerans and Saccharomyces cerevisiae Kapsopoulou, K.; Mourtzini, A.; Anthoulas, M. World Journal of Microbiology and Biotechnology, Vol. 23, Issue 5 https://doi.org/10.1007/s11274-006-9283-5	journal	October 2006
Contribution to the aroma of white wines by controlled Torulaspora delbrueckii cultures in association with Saccharomyces cerevisiae Azzolini, Michela; Tosi, Emanuele; Lorenzini, Marilinda World Journal of Microbiology and Biotechnology, Vol. 31, Issue 2 https://doi.org/10.1007/s11274-014-1774-1	journal	November 2014
The DAN1 gene of S. cerevisiae is regulated in parallel with the hypoxic genes, but by a different mechanism Sertil, Odeniel; Cohen, Brian D.; Davies, Kelvin J. A. Gene, Vol. 192, Issue 2 https://doi.org/10.1016/S0378-1119(97)00028-0	journal	June 1997
Role of Unsaturated Lipid and Ergosterol in Ethanol Tolerance of Model Yeast Biomembranes Vanegas, Juan M.; Contreras, Maria F.; Faller, Roland Biophysical Journal, Vol. 102, Issue 3 https://doi.org/10.1016/j.bpj.2011.12.038	journal	February 2012
Transformation of chemical constituents of lychee wine by simultaneous alcoholic and malolactic fermentations Chen, Dai; Liu, Shao-Quan Food Chemistry, Vol. 196 https://doi.org/10.1016/j.foodchem.2015.10.047	journal	April 2016
Chemical composition of bilberry wine fermented with non-Saccharomyces yeasts (Torulaspora delbrueckii and Schizosaccharomyces pombe) and Saccharomyces cerevisiae in pure, sequential and mixed fermentations Liu, Shuxun; Laaksonen, Oskar; Kortesniemi, Maaria Food Chemistry, Vol. 266 https://doi.org/10.1016/j.foodchem.2018.06.003	journal	November 2018
Fermentation behaviour and metabolic interactions of multistarter wine yeast fermentations Ciani, Maurizio; Beco, Luca; Comitini, Francesca International Journal of Food Microbiology, Vol. 108, Issue 2 https://doi.org/10.1016/j.ijfoodmicro.2005.11.012	journal	April 2006
Impact of mixed Torulaspora delbrueckii–Saccharomyces cerevisiae culture on high-sugar fermentation Bely, Marina; Stoeckle, Philippe; Masneuf-Pomarède, Isabelle International Journal of Food Microbiology, Vol. 122, Issue 3 https://doi.org/10.1016/j.ijfoodmicro.2007.12.023	journal	March 2008
Genetic characterization and phenotypic variability in Torulaspora delbrueckii species: Potential applications in the wine industry Renault, Philippe; Miot-Sertier, Cecile; Marullo, Philippe International Journal of Food Microbiology, Vol. 134, Issue 3 https://doi.org/10.1016/j.ijfoodmicro.2009.06.008	journal	September 2009
Characterisation of commercial and natural Torulaspora delbrueckii wine yeast strains van Breda, Valmary; Jolly, Neil; van Wyk, Jessy International Journal of Food Microbiology, Vol. 163, Issue 2-3 https://doi.org/10.1016/j.ijfoodmicro.2013.02.011	journal	May 2013
Exploitation of the non-Saccharomyces yeast Starmerella bacillaris (synonym Candida zemplinina) in wine fermentation: Physiological and molecular characterizations Englezos, Vasileios; Rantsiou, Kalliopi; Torchio, Fabrizio International Journal of Food Microbiology, Vol. 199 https://doi.org/10.1016/j.ijfoodmicro.2015.01.009	journal	April 2015
Increase of fruity aroma during mixed T. delbrueckii/S. cerevisiae wine fermentation is linked to specific esters enhancement Renault, Philippe; Coulon, Joana; de Revel, Gilles International Journal of Food Microbiology, Vol. 207 https://doi.org/10.1016/j.ijfoodmicro.2015.04.037	journal	August 2015
Influence of Torulaspora delbrueckii in varietal thiol (3-SH and 4-MSP) release in wine sequential fermentations Belda, Ignacio; Ruiz, Javier; Beisert, Beata International Journal of Food Microbiology, Vol. 257 https://doi.org/10.1016/j.ijfoodmicro.2017.06.028	journal	September 2017
Linking gene expression and oenological traits: Comparison between Torulaspora delbrueckii and Saccharomyces cerevisiae strains Tondini, Federico; Lang, Tom; Chen, Liang International Journal of Food Microbiology, Vol. 294 https://doi.org/10.1016/j.ijfoodmicro.2019.01.014	journal	April 2019
Analysing the impact of the nature of the nitrogen source on the formation of volatile compounds to unravel the aroma metabolism of two non-Saccharomyces strains Seguinot, Pauline; Bloem, Audrey; Brial, Pascale International Journal of Food Microbiology, Vol. 316 https://doi.org/10.1016/j.ijfoodmicro.2019.108441	journal	March 2020
Differences in the management of intracellular redox state between wine yeast species dictate their fermentation performances and metabolite production Tyibilika, Viwe; Setati, Mathabatha E.; Bloem, Audrey International Journal of Food Microbiology, Vol. 411 https://doi.org/10.1016/j.ijfoodmicro.2023.110537	journal	February 2024
Ethyl acetate production by the elusive alcohol acetyltransferase from yeast Kruis, Aleksander J.; Levisson, Mark; Mars, Astrid E. Metabolic Engineering, Vol. 41 https://doi.org/10.1016/j.ymben.2017.03.004	journal	May 2017
Dispersive Liquid–Liquid Microextraction for the Quantitation of Terpenes in Wine Bergler, G.; Nolleau, V.; Picou, C. Journal of Agricultural and Food Chemistry, Vol. 68, Issue 47 https://doi.org/10.1021/acs.jafc.9b08222	journal	March 2020
SLI1(YGR212W) is a major gene conferring resistance to the sphingolipid biosynthesis inhibitor ISP-1, and encodes an ISP-1 N-acetyltransferase in yeast Momoi, Michiko; Tanoue, Daisuke; Sun, Yidi Biochemical Journal, Vol. 381, Issue 1 https://doi.org/10.1042/BJ20040108	journal	June 2004
Saccharomyces cerevisiae PAU genes are induced by anaerobiosis: Anaerobic regulation of PAU genes Rachidi, Najma; Martinez, Marie-Joséée; Barre, Pierre Molecular Microbiology, Vol. 35, Issue 6 https://doi.org/10.1046/j.1365-2958.2000.01807.x	journal	March 2000
Saccharomyces cerevisiae Forms d-2-Hydroxyglutarate and Couples Its Degradation to d-Lactate Formation via a Cytosolic Transhydrogenase Becker-Kettern, Julia; Paczia, Nicole; Conrotte, Jean-François Journal of Biological Chemistry, Vol. 291, Issue 12 https://doi.org/10.1074/jbc.M115.704494	journal	March 2016
The Saccharomyces cerevisiae EHT1 and EEB1 Genes Encode Novel Enzymes with Medium-chain Fatty Acid Ethyl Ester Synthesis and Hydrolysis Capacity Saerens, Sofie M. G.; Verstrepen, Kevin J.; Van Laere, Stijn D. M. Journal of Biological Chemistry, Vol. 281, Issue 7 https://doi.org/10.1074/jbc.M512028200	journal	February 2006
Sterol uptake analysis in Saccharomyces and non-Saccharomyces wine yeast species Tesnière, Catherine; Pradal, Martine; Legras, Jean-Luc FEMS Yeast Research, Vol. 21, Issue 3 https://doi.org/10.1093/femsyr/foab020	journal	April 2021
Functional Divergence in a Multi-gene Family Is a Key Evolutionary Innovation for Anaerobic Growth in Saccharomyces cerevisiae Krause, David J.; Hittinger, Chris Todd Molecular Biology and Evolution, Vol. 39, Issue 10 https://doi.org/10.1093/molbev/msac202	journal	September 2022
Functional analyses of PAU genes in Saccharomyces cerevisiae Luo, Z.; van Vuuren, H. J. J. Microbiology, Vol. 155, Issue 12 https://doi.org/10.1099/mic.0.030726-0	journal	September 2009
Sugar utilization patterns and respiro-fermentative metabolism in the baker's yeast Torulaspora delbrueckii Alves-Araujo, C.; Pacheco, A.; Almeida, M. J. Microbiology, Vol. 153, Issue 3 https://doi.org/10.1099/mic.0.2006/003475-0	journal	March 2007
Ethanol tolerance of sugar transport, and the rectification of stuck wine fermentations Santos, Júlia; Sousa, Maria João; Cardoso, Helena Microbiology, Vol. 154, Issue 2 https://doi.org/10.1099/mic.0.2007/011445-0	journal	February 2008
Use ofTorulaspora delbrueckiiandSaccharomyces cerevisiaein semi-industrial sequential inoculation to improve quality of Palomino and Chardonnay wines in warm climates Puertas, B.; Jiménez, M. J.; Cantos-Villar, E. Journal of Applied Microbiology, Vol. 122, Issue 3 https://doi.org/10.1111/jam.13375	journal	January 2017
A glimpse at an early stage of microbe domestication revealed in the variable genome of Torulaspora delbrueckii, an emergent industrial yeast Silva, Margarida; Pontes, Ana; Franco‐Duarte, Ricardo Molecular Ecology, Vol. 32, Issue 10 https://doi.org/10.1111/mec.16428	journal	March 2022
Genomic and Transcriptomic Basis of Hanseniaspora vineae 's Impact on Flavor Diversity and Wine Quality Giorello, Facundo; Valera, Maria Jose; Martin, Valentina Applied and Environmental Microbiology, Vol. 85, Issue 1 https://doi.org/10.1128/AEM.01959-18	journal	October 2018
Oxygen Consumption by Anaerobic Saccharomyces cerevisiae under Enological Conditions: Effect on Fermentation Kinetics Rosenfeld, E.; Beauvoit, B.; Blondin, B. Applied and Environmental Microbiology, Vol. 69, Issue 1 https://doi.org/10.1128/AEM.69.1.113-121.2003	journal	January 2003
Reciprocal Regulation of Anaerobic and Aerobic Cell Wall Mannoprotein Gene Expression in Saccharomyces cerevisiae Abramova, N.; Sertil, O.; Mehta, S. Journal of Bacteriology, Vol. 183, Issue 9 https://doi.org/10.1128/JB.183.9.2881-2887.2001	journal	May 2001
Influence of invertase activity and glycerol synthesis and retention on fermentation of media with a high sugar concentration by Saccharomyces cerevisiae Myers, D. K.; Lawlor, D. T.; Attfield, P. V. Applied and Environmental Microbiology, Vol. 63, Issue 1 https://doi.org/10.1128/aem.63.1.145-150.1997	journal	January 1997
Influence of Oxygen on Alcoholic Fermentation by a Wine Strain ofTorulaspora delbrueckii: Kinetics and Carbon Mass Balance Brandam, Cédric; Lai, Quoc Phong; Julien-Ortiz, Anne Bioscience, Biotechnology, and Biochemistry, Vol. 77, Issue 9 https://doi.org/10.1271/bbb.130228	journal	September 2013
Winemaking and Bioprocesses Strongly Shaped the Genetic Diversity of the Ubiquitous Yeast Torulaspora delbrueckii Albertin, Warren; Chasseriaud, Laura; Comte, Guillaume PLoS ONE, Vol. 9, Issue 4 https://doi.org/10.1371/journal.pone.0094246	journal	April 2014
Contribution of Eat1 and Other Alcohol Acyltransferases to Ester Production in Saccharomyces cerevisiae Kruis, Aleksander J.; Gallone, Brigida; Jonker, Timo Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.03202	journal	December 2018
Large-Scale Screening of Thiol and Fermentative Aroma Production during Wine Alcoholic Fermentation: Exploring the Effects of Assimilable Nitrogen and Peptides Duc, Camille; Maçna, Faïza; Sanchez, Isabelle Fermentation, Vol. 6, Issue 4 https://doi.org/10.3390/FERMENTATION6040098	journal	October 2020
The Yeast Torulaspora delbrueckii: An Interesting But Difficult-To-Use Tool for Winemaking Ramírez, Manuel; Velázquez, Rocío Fermentation, Vol. 4, Issue 4 https://doi.org/10.3390/fermentation4040094	journal	November 2018
Systematic Comparison of Cell Wall-Related Proteins of Different Yeasts Lozančić, Mateja; Žunar, Bojan; Hrestak, Dora Journal of Fungi, Vol. 7, Issue 2 https://doi.org/10.3390/jof7020128	journal	February 2021
Torulaspora delbrueckii Phenotypic and Metabolic Profiling towards Its Biotechnological Exploitation Silva-Sousa, Flávia; Fernandes, Ticiana; Pereira, Fábio Journal of Fungi, Vol. 8, Issue 6 https://doi.org/10.3390/jof8060569	journal	May 2022

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