Vol. 37 No. 1 (2024): Revista ION
Articles

Adaptation of yeasts: factors influencing fermentative stress of the genus saccharomyces in winemaking. A review.

PDF (Español (España))
  • Diego Enrique Ochoa Flórez,
  • Daniel Salvador Duran Osorio,
  • Yanine Yubisay Trujillo Navarro
Diego Enrique Ochoa Flórez
Universidad de Pamplona
DOI: https://doi.org/10.18273/revion.v37n1-2024006

Published 2024-07-24

Keywords

  • Adaptation,
  • Biomass,
  • Fermentation stress,
  • Fermentation,
  • Must,
  • Modification of nutrient yeasts,
  • Saccharomyces,
  • Yields,
  • Yeast selection,
  • Tolerance,
  • Vinification
    • ...More
    Less

How to Cite

Ochoa Flórez, D. E., Duran Osorio, D. S. ., & Trujillo Navarro, Y. Y. . (2024). Adaptation of yeasts: factors influencing fermentative stress of the genus saccharomyces in winemaking. A review. Revista ION, 37(1), 83–98. https://doi.org/10.18273/revion.v37n1-2024006

Copyright (c) 2024 Diego Enrique Ochoa Flórez, Daniel Salvador Duran Osorio, Yanine Yubisay Trujillo Navarro

Creative Commons License

This work is licensed under a Creative Commons Attribution-NoDerivatives 4.0 International License.

Abstract

The adaptability of yeasts of the genus Saccharomyces is related to the biomass's predisposition to fermentation stress, directly affecting their metabolism and fermentation yields. The purpose of the review was to expose the factors of incidence of fermentative stress of the genus Saccharomyces and to evaluate the current trends used in the modification of yeasts to increase their ability to adapt to the fermentative medium. To this end, a search for information was carried out in scientific databases taking into account key descriptors, thesauri and search equations. The documents were selected and classified taking into account their specificity with the research objective and the most representative by country, research center and authors. Within what was found, based on the adaptation capacity of the yeasts, 6 stress factors were identified, which are: genetic, activation or inoculation, yeast mixture, nutritional, alcohol tolerance and fermentation conditions. Of these factors, genetic ones stand out, given that current genotypic and phenotypic modifications are based on the suppression of genes that increase the predisposition to stress. With respect to fermentation factors and nutrients, it is stated that fermentation variables must be controlled to ensure optimal media. Finally, achieving better fermentation conditions causes the yeasts to be more adapted to the environment, so these biomasses must be selected and classified in order to optimize the winemaking processes.

PDF (Español (España))

Downloads

Download data is not yet available.

References

  1. Álvarez R, Garces F, Louis EJ, Dequin S, Camarasa C. Beyond S. cerevisiae for winemaking: Fermentation-related trait diversity in the genus Saccharomyces. Food Microbiol 2023;113:104270. https://doi.org/10.1016/j.fm.2023.104270
  2. Joseph R, Bachhawat AK. Yeasts: Production and Commercial Uses. En: Encyclopedia of Food Microbiology. 2 ed. vol. 3. Elsevier; 2014. p. 823-830. https://doi.org/10.1016/B978-0-12-384730-0.00361-X
  3. Mavrommati M, Papanikolaou S, Aggelis G. Improving ethanol tolerance of Saccharomyces cerevisiae through adaptive laboratory evolution using high ethanol concentrations as a selective pressure. Process Biochem. 2023;124:280–289. https://doi.org/10.1016/j.procbio.2022.11.027
  4. Guadalupe-Daqui M, Chen M, ThompsonWitrick KA, Macintosh AJ. Yeast Morphology Assessment through Automated Image Analysis during Fermentation. Ferment. 2021;7(2):44. https://doi.org/10.3390/fermentation7020044
  5. Varize CS, Bücker A, Lopes LD, ChristofoletiFurlan RM, Raposo MS, Basso LC, et al. Increasing Ethanol Tolerance and Ethanol Production in an Industrial Fuel Ethanol Saccharomyces cerevisiae Strain. Ferment. 2022;8(10):470. https://doi.org/10.3390/fermentation8100470
  6. Qiu Y, Wu M, Bao H, Liu W, Shen Y. Engineering of Saccharomyces cerevisiae for co-fermentation of glucose and xylose: Current state and perspectives. Eng. Microbiol. 2023;3(3):100084. doi: https://doi.org/10.1016/j.engmic.2023.100084
  7. Tian J, Lin Y, Su X,Tan H, Gan C, Ragauskas AJ. Effects of Saccharomyces cerevisiae quorum sensing signal molecules on ethanol production in bioethanol fermentation process. Microbiol. Res. 2023;271:127367. https://doi.org/10.1016/j.micres.2023.127367
  8. Margalef-Català M, Araque I, Bordons A, Reguant C, Bautista-Gallego J. Transcriptomic and proteomic analysis of Oenococcus oeni adaptation to wine stress conditions. Front. Microbiol. 2016;7:1554. https://doi.org/10.3389/fmicb.2016.01554
  9. Hranilovic A, Gambetta JM, Jeffery DW, Grbin PR, Jiranek V. Lower-alcohol wines produced by Metschnikowia pulcherrima and Saccharomyces cerevisiae co-fermentations: The effect of sequential inoculation timing. Int. J. Food Microbiol. 2020;329:108651. https://doi.org/10.1016/j.ijfoodmicro.2020.108651
  10. Englezos V, Jolly NP, Di Gianvito P, Rantsiou K, Cocolin L. Microbial interactions in winemaking: Ecological aspects and effect on wine quality. Trends Food Sci. Technol. 2022;127:99–113. https://doi.org/10.1016/j.tifs.2022.06.015
  11. Medina K, Martin V, Boido E, Carrau F. Yeast Biotechnology for Red Winemaking. En: Red Wine Technol. Academic Press; 2019. pp. 69–83. https://doi.org/10.1016/B978-0-12-814399-5.00005-0
  12. Muñoz R, Gómez A, Robles V, Rodríguez P, Cebollero E, Tabera L, et al. Multilocus sequence typing of oenological Saccharomyces cerevisiae strains. Food Microbiol. 2009;26(8):841–846. https://doi.org/10.1016/j.fm.2009.05.009.
  13. Bao Y, Zhang M, Chen W, Chen H, Chen W, Zhong Q. Screening and evaluation of suitable non-Saccharomyces yeast for aroma improvement of fermented mango juice. Food Biosci. 2021;44:101414. https://doi.org/10.1016/j.fbio.2021.101414
  14. Zhao X, Xue Y, Tang F, Cai W, Hao G, Shan C. Quality improvement of jujube wine through mixed fermentation with Saccharomyces cerevisiae and Bacillus licheniformis. LWT. 2022;164:113444. https://doi.org/10.1016/j.lwt.2022.113444
  15. Ruiz-de-Villa C, Poblet M, Cordero-Otero R, Bordons A, Reguant C, Rozès N. Screening of Saccharomyces cerevisiae and Torulaspora delbrueckii strains about their effect on malolactic fermentation. Food Microbiol. 2023;112:104212. https://doi.org/10.1016/J.FM.2022.104212.
  16. Vicente J, Ruiz J, Tomasi S, de Celis M, Ruiz-de-Villa C, Gombau J, et al. Impact of rare yeasts in Saccharomyces cerevisiae wine fermentation performance: Population prevalence and growth phenotype of Cyberlindnera fabianii, Kazachstania unispora, and Naganishia globosa. Food Microbiol. 2023;110:104189. https://doi.org/10.1016/j.fm.2022.104189
  17. Quintero-Blanco J, Delodi E, Garzón A, Jimenez J. Sexually-Driven Combinatorial Diversity in Native Saccharomyces Wine Yeasts. Fermentation. 2022;8(10):569. https://doi.org/10.3390/fermentation8100569
  18. Peter J, De Chiara M, Friedrich A, Yue JX, Pflieger D, Bergström A, et al. Genome evolution across 1,011 Saccharomyces cerevisiae isolates. Nat. 2018;556:339–344. https://doi.org/10.1038/s41586-018-0030-5
  19. Kyriakou M, Christodoulou M, Ioannou A Fotopoulos V Koutinas M. Improvement of stress multi-tolerance and bioethanol production by Saccharomyces cerevisiae immobilised on biochar: Monitoring transcription from defence-related genes. Biochem. Eng. J. 2023;195:108914. https://doi.org/10.1016/J.BEJ.2023.108914
  20. Gibson BR, Lawrence SJ, Leclaire JPR, Powell CD, Smart KA. Yeast responses to stresses associated with industrial brewery handling. FEMS Microbiol. Rev. 2007;31(5):535–569. https://doi.org/10.1111/J.1574-6976.2007.00076.X
  21. Betlej et al. Long-Term Adaption to High Osmotic Stress as a Tool for Improving Enological Characteristics in Industrial Wine Yeast. Genes (Basel). 2020;11(5):576. https://doi.org/10.3390/genes11050576
  22. Ding J, Huang X, Zhang L, Zhao N, Yang D, Zang K. Tolerance and stress response to ethanol in the yeast Saccharomyces cerevisiae. Appl Microbiol Biotechnol 2009;85:253-263. https://doi.org/10.1007/s00253-009-2223-1
  23. Stanley D, Bandara A, Fraser S, Chambers PJ, Stanley GA. The ethanol stress response and ethanol tolerance of Saccharomyces cerevisiae. J. Appl. Microbiol. 2010;109(1):13–24. https://doi.org/10.1111/j.1365-2672.2009.04657.x
  24. Sunyer-Figueres M, Mas A, Beltran G, Torija MJ. Protective effects of melatonin on saccharomyces cerevisiae under ethanol stress. Antioxidants 2021;10(11):1735. https://doi.org/10.3390/antiox10111735
  25. Matallana E, Aranda A. Biotechnological impact of stress response on wine yeast. Lett. Appl. Microbiol. 2017;64(2):103–110. https://doi.org/10.1111/LAM.12677
  26. Zhang H, Hu W, Lu Y, Shen C, Yao H, Yang X, et al. PEP4-Allele Modification Provides an Industrial Brewing Yeast with Malate Stress Tolerance. Ferment. 2023;9(4):378. https://doi.org/10.3390/fermentation9040378
  27. Costa ACT, Russo M, Fernandes AAR, Broach JR, Fernandes PMB. Transcriptional Response of Multi-Stress-Tolerant Saccharomyces cerevisiae to Sequential Stresses. Fermentation. 2023;9(2):195. https://doi.org/10.3390/fermentation9020195
  28. Zylstra A, Heinemann M. Metabolic dynamics during the cell cycle. Curr. Opin. Syst. Biol. 2022;30:100415. https://doi.org/10.1016/J.COISB.2022.100415
  29. Marullo P, Dubourdieu D. Yeast selection for wine flavour modulation. En: Managing Wine Quality Woodhead. Publishing Limited; 2010. p. 293-345.
  30. Lorca Mandujano GP, Alves HC, Prado CD, Martins JGO, Novaes HR, Maia de Oliveira da Silva JP, et al. Identification and selection of a new Saccharomyces cerevisiae strain isolated from Brazilian ethanol fermentation process for application in beer production. Food Microbiol. 2022;103:103958. https://doi.org/10.1016/J.FM.2021.103958
  31. Canseco Grellet MA, Dantur KI, Perera MF, Ahmed PM, Castagnaro A, ArroyoLopez N, et al. Genotypic and phenotypic characterization of industrial autochthonous Saccharomyces cerevisiae for the selection of well-adapted bioethanol-producing strains. Fungal Biol. 2022;126(10):658–673. https://doi.org/10.1016/J.FUNBIO.2022.08.004
  32. Riveros RG, Kitazono AA. Identification of ferritin variants with increased cadmium selectivity by in vivo cloning and mutagenesis in Saccharomyces cerevisiae. Bioresour. Technol. Reports. 2023;22:101422. https://doi.org/0.1016/J.BITEB.2023.101422
  33. Kadyrova LY, Mieczkowski PA, Kadyrov FA. Genome-wide contributions of the MutSα- and MutSβ-dependent DNA mismatch repair pathways to the maintenance of genetic stability in Saccharomyces cerevisiae. J. Biol. Chem. 2023;299,(5):104705. https://doi.org/10.1016/J.JBC.2023.104705
  34. Ogbuewu IP, Mbajiorgu CA. Metaanalysis of Saccharomyces cerevisiae on enhancement of growth performance, rumen fermentation and haemato-biochemical characteristics of growing goats. Heliyon. 2023;9(3):e14178. https://doi.org/10.1016/j.heliyon.2023.e14178
  35. Lowe MS, Stone SM, Maxson BK, Snajdr E, Miller W. Boolean redux: Performance of advanced versus simple boolean searches and implications for upper-level instruction. J. Acad. Librariansh. 2020;46(6):102234. https://doi.org/10.1016/j.acalib.2020.102234
  36. Pourreza M, Ensan F. Towards semantic driven boolean query formalization for biomedical systematic literature reviews. Int. J. Med. Inform. 2023;170:104928. https://doi.org/10.1016/j.ijmedinf.2022.104928
  37. Balmaseda A, Rozès N, Bordons A, Reguant C. Molecular adaptation response of Oenococcus oeni in non-Saccharomyces fermented wines: A comparative multi-omics approach. Int. J. Food Microbiol. 2022;362:109490. https://doi.org/10.1016/j.ijfoodmicro.2021.109490
  38. Divol B, Bauer FF. Metabolic engineering of wine yeast and advances in yeast selection methods for improved wine quality. En: Managing Wine Quality. 2 ed. Woodhead Publishing Limited; 2010. p. 34-59. https://doi.org/10.1533/9781845699987.1.34
  39. Bastos R, Coelho E, Coimbra MA. Modifications of Saccharomyces pastorianus cell wall polysaccharides with brewing process. Carbohydr. Polym. 2015;124:322–330. https://doi.org/10.1016/j.carbpol.2015.02.031
  40. Reis SF, Messias S, Bastos R, Martins VJ, Correia VG, Pinheiro BA, et al. Structural differences on cell wall polysaccharides of brewer’s spent Saccharomyces and microarray binding profiles with immune receptors. Carbohydr. Polym. 2023;301(B):120325. https://doi.org/10.1016/j.carbpol.2022.120325
  41. Lappa IK, Kachrimanidou V, Pateraki C, Koulougliotis D, Eriotou E, Kopsahelis N. Indigenous yeasts: emerging trends and challenges in winemaking. Curr. Opin. Food Sci. 2020;32:133–143. https://doi.org/10.1016/j.cofs.2020.04.004
  42. Specht G. Yeast fermentation management for improved wine quality. En: Managing Wine Quality. Woodhead Publishing Limited; 2010. p. 3-33. https://doi.org/10.1533/9781845699987.1.3
  43. Pérez D, Denat M, Heras JM, Guillamón JM, Ferreira V, Querol A. Effect of non-wine Saccharomyces yeasts and bottle aging on the release and generation of aromas in semi-synthetic Tempranillo wines. Int. J. Food Microbiol. 2022;365:109554. https://doi.org/10.1016/j.ijfoodmicro.2022.109554
  44. Bencresciuto GF, Mandalà C, Migliori CA, Cortellino G, Vanoli M, Bardi L. Assessment of Starters of Lactic Acid Bacteria and Killer Yeasts: Selected Strains in Lab-Scale Fermentations of Table Olives (Olea europaea L.) cv. Leccino. Fermentation. 2023;9(2):182. https://doi.org/10.3390/fermentation9020182
  45. Malićanin M, Danilović B, Stamenković Stojanović S, Cvetković D, Lazić M, Karabegović I, et al. Pre-Fermentative Cold Maceration and Native Non-Saccharomyces Yeasts as a Tool to Enhance Aroma and Sensory Attributes of
  46. Chardonnay Wine. Horticulturae. 2022;8(3):212. https://doi.org/10.3390/horticulturae8030212
  47. Camilo S, Chandra M, Branco P, MalfeitoFerreira M. Wine Microbial Consortium: Seasonal Sources and Vectors Linking Vineyard and Winery Environments. Fermentation. 2022;8(7):324. https://doi.org/10.3390/fermentation8070324
  48. Cioch-Skoneczny M, Satora P, Skoneczny S, Pater A. Determination of the oenological properties of yeast strains isolated from spontaneously fermented grape musts obtained from cool climate grape varieties. Eur. Food Res. Technol. 2020;246(11):2299–2307. https://doi.org/10.1007/s00217-020-03574-0
  49. Corbu VM, Csutak O. Molecular and Physiological Diversity of Indigenous Yeasts Isolated from Spontaneously Fermented Wine Wort from Ilfov County, Romania. Microorganisms. 2023;11(1):37. https://doi.org/10.3390/microorganisms11010037
  50. Mehlomakulu NN, Setati ME, Divol B. Characterization of novel killer toxins secreted by wine-related non-Saccharomyces yeasts and their action on Brettanomyces spp. Int. J. Food Microbiol. 2014;188:83–91. https://doi.
  51. org/10.1016/J.IJFOODMICRO.2014.07.015
  52. Alves LF Bortolucci J, Reginato V, Guazzaroni ME, Mussatto SI. Improving Saccharomyces cerevisiae acid and oxidative stress resistance using a prokaryotic gene identified by functional metagenomics. Heliyon. 2023;9(4):e14838. https://doi.org/10.1016/J.HELIYON.2023.E14838
  53. Bissaro B, Várnai A, Røhr ÅK, Eijsink VGH. Oxidoreductases and Reactive Oxygen Species in Conversion of Lignocellulosic Biomass. Microbiol. Mol. Biol. Rev. 2018;82(4):e00029-18. https://doi.org/10.1128/mmbr.00029-18
  54. García M, Crespo J, Cabellos JM, Arroyo T. Growth of non-saccharomyces native strains under different fermentative stress conditions. Fermentation 2021;7(3):124. https://doi.org/10.3390/fermentation7030124
  55. Oliva Hernandez AA. Evaluación cinética y molecular de levaduras fructofílicas aisladas del mezcal tamaulipeco (Tesis de doctorado). Toulouse: Institut National Polytechnique de Toulouse - INPT. Nuevo León: Universidad autónoma de Nuevo León; 2012.
  56. Almeida JRM, Wiman M, Heer D, Brink DP, Sauer U, Hahn-Hägerdal B, et al. Physiological and Molecular Characterization of Yeast Cultures Pre-Adapted for Fermentation of Lignocellulosic Hydrolysate. Fermentation. 2023;9(1):72; https://doi.org/10.3390/fermentation9010072
  57. Contreras-Ruiz A, Alonso-del-Real J, Barrio E, Querol A. Saccharomyces cerevisiae wine strains show a wide range of competitive abilities and differential nutrient uptake behavior in co-culture with S. kudriavzevii. Food Microbiol. 2023;114:104276. https://doi. org/10.1016/j.fm.2023.104276
  58. Querol A, Pérez-Torrado R, Alonso-del-Real J, Minebois R, Stribny J, Oliveira BM, et al. New Trends in the Uses of Yeasts in Oenology. En: Advances in Food and Nutrition Research. 1 ed. vol. 85. Elsevier Inc; 2018. https://doi.org/10.1016/bs.afnr.2018.03.002
  59. Matei F, Kosseva MR. Microbiology of fruit wine production. Microbiology of Fruit Wine Production. En: Science and Technology of Fruit Wine Production. Academic Press. 2017. p. 73-103. http://dx.doi.org/10.1016/B978-0-12-800850-8.00002-8
  60. Drappier J, Thibon C, Rabot A, Geny-Denis L. Relationship between wine composition and temperature: Impact on Bordeaux wine typicity in the context of global warming—Review. Critical Reviews in Food Science and Nutrition. 2017;59(1):14-30. https://doi.org/10.1080/10408398.2017.1355776
  61. Berbegal C, Fragasso M, Russo P, Bimbo F, Grieco F, Spano G, et al. Climate Changes and Food Quality: The Potential of Microbial Activities as Mitigating Strategies in the Wine Sector. Ferment. 2019;5(4):85. https://doi.org/10.3390/fermentation5040085
  62. Yang C, Dong A, Deng L, Wang F, Liu J. Deciphering the change pattern of lipid metabolism in Saccharomyces cerevisiae responding to low temperature. Biochem. Eng. J. 2023;194:108884. https://doi.org/10.1016/j.bej.2023.108884
  63. Zhang B, Geberekidan M, Yan Z, Yi X, Bao J. Very High Thermotolerance of an Adaptive Evolved Saccharomyces cerevisiae in Cellulosic Ethanol Fermentation. Ferment. 2023;9(4):393. https://doi.org/10.3390/fermentation9040393
  64. Liu S, Dai J, Sun Y, Xiu Z, Wang X, Li F, et al. Effects of rice husk on the tolerance of Saccharomyces cerevisiae to high temperature and ethanol concentration. Fuel. 2023;333:126406. https://doi.org/10.1016/j.fuel.2022.126406
  65. Hou D, Xu X, Wang J, Liu C, Niu C, Zheng F, et al. Effect of environmental stresses during fermentation on brewing yeast and exploration on the novel flocculation-associated function of RIM15 gene. Bioresour. Technol. 2023;379:129004. https://doi.org/10.1016/j.biortech.2023.129004
  66. Itto-Nakama K, Watanabe S, Ohnuki S, Kondo N, Kikuchi R, Nakaruma T, et al. Prediction of ethanol fermentation under stressed conditions using yeast morphological data. J. Biosci. Bioeng. 2023;135(3):210–216. https://doi.org/10.1016/j.jbiosc.2022.12.008