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Pectinolytic Yeast Saccharomyces paradoxus as a New Gene Pool for Winemaking

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Abstract

A large-scale screening of pectinolytic activity in the yeast Saccharomyces paradoxus isolated from various natural sources in Europe, Asia, North America, and the Hawaiian Islands was carried out. Of the 98 studied strains, pectinolytic activity was absent only in five Hawaiian and two European strains. Most strains were able to secrete active endo-polygalacturonase. North American strains UCDFST 52-225, UCDFST 61-359, UCDFST 61-220, 95-3, and UCDFST 62-186 had very high pectinolytic activity, comparable to or even higher than that of the experimentally obtained tetraploid strain S. cerevisiae VKPM Y-718. Comparative analysis of the nucleotide and amino acid sequences of pectinase genes showed that the North American and Far Eastern populations of S. paradoxus were more genetically diverse than the European and Hawaiian ones. Phylogenetic analysis confirmed the species specificity of the PGU genes of Saccharomyces yeasts. Of the eight Saccharomyces species, high pectinolytic activity is characteristic of S. bayanus and S. paradoxus. Five North American strains with the highest pectinolytic activity are of interest for further molecular genetic studies and breeding work with wine yeasts. The ecological role of endo-polygalacturonase is discussed.

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REFERENCES

  1. Belda, I., Conchillo, L.B., Ruiz, J., Navascués, E., Marquina, D., and Santos, A., Selection and use of pectinolytic yeasts for improving clarification and phenolic extraction in winemaking, Int. J. Food Microbiol., 2016, vol. 223, pp. 1–8.

    Article  CAS  PubMed  Google Scholar 

  2. Belda, I., Ruiz, J., Esteban-Fernández, A., Navascués, E., Marquina, D., Santos, A., and Moreno-Arribas, M.V., Microbial contribution to wine aroma and its intended use for wine quality improvement, Molecules, 2017, vol. 22, pp. 189–218.

    Article  PubMed  PubMed Central  Google Scholar 

  3. Bendixsen, D.P., Frazão, J.G., and Stelkens, R., Saccharomyces yeast hybrids on the rise, Yeast, 2022, vol. 39, pp. 40–54.

    Article  CAS  PubMed  Google Scholar 

  4. Berbegal, C., Khomenko, I., Russo, P., Spano, G., Fragasso, M., Biasioli, F., and Capozzi, V., PTR-ToF-MS for the online monitoring of alcoholic fermentation in wine: assessment of VOCs variability associated with different combinations of Saccharomyces/Non-Saccharomyces as a case-study, Fermentation, 2020, vol. 6, pp. 55–72.

    Article  CAS  Google Scholar 

  5. Borovkova, A.N., Shalamitskii, M.Yu., and Naumo-va, E.S., Selection of Saccharomyces bayanus strains with high pectinolytic activity and phylogenetic analysis of PGU genes, Appl. Biochem. Microbiol., 2022, vol. 58, pp. 1–10.

    Article  Google Scholar 

  6. da Silva, E.G., de Fátima Borges, M., Medina, C., Hilsdorf Piccoli, R., and Freitas Schwan, R., Pectinolytic enzymes secreted by yeasts from tropical fruits, FEMS Yeast Res., 2005, vol. 5, pp. 859–865.

    Article  PubMed  Google Scholar 

  7. Divol, B. and Rensburg, P., PGU1 gene natural deletion is responsible for the absence of endo-polygalacturonase activity in some wine strains of Saccharomyces cerevisiae, FEMS Yeast Res., 2007, vol. 7, pp. 1328−1339.

    Article  CAS  PubMed  Google Scholar 

  8. Eschstruth, A. and Divol, B., Comparative characterization of endo-polygalacturonase (Pgu1) from Saccharomyces cerevisiae and Saccharomyces paradoxus under winemaking conditions, Appl. Microbiol. Biotechnol., 2011, vol. 91, pp. 623–634.

    Article  CAS  PubMed  Google Scholar 

  9. Fernández-González, M., Ubeda, J.F., Vasudevan, T.G., Cordero Otero, R.R., and Briones, A.I., Evaluation of polygalacturonase activity in Saccharomyces cerevisiae wine strains, FEMS Microbiol. Lett., 2004, vol. 237, pp. 261−266.

    Article  PubMed  Google Scholar 

  10. He, P.Y., Shao, X.Q., Duan, S.F., Han, D.Y., Li, K., Shi, J.Y., Zhang, R.P., Han, P.J., Wang, Q.M., and Bai, F.Y., Highly diverged lineages of Saccharomyces paradoxus in temperate to subtropical climate zones in China, Yeast, 2022, vol. 39, pp. 69–82.

    Article  CAS  PubMed  Google Scholar 

  11. Glushakova, A.M., Ivannikova, Y.V., Naumova, E.S., Chernov, I.Y., and Naumov, G.I., Massive isolation and identification of Saccharomyces paradoxus yeasts from plant phyllosphere, Microbiology (Moscow), 2007, vol. 76, pp. 205–210.

    Article  CAS  Google Scholar 

  12. Hebly, M., Brickwedde, A., Bolat, I., Driessen, M.R.M., de Hulster, E.A.F., van den Broek, M., Pronk, J.T., Geertman, J.-M., Daran, J.-M., and Daran-Lapujade, P., S. cerevisiae × S. eubayanus interspecific hybrid, the best of both worlds and beyond, FEMS Yeast Res., 2015, vol. 15, p. fov005.

    Article  PubMed  Google Scholar 

  13. Hutzler, M., Michel, M., Kunz, O., Kuusisto, T., Magalhães, F., Krogerus, K., and Gibson, B., Unique brewing-relevant properties of a strain of Saccharomyces jurei isolated from ash (Fraxinus excelsior), Front. Microbi-ol., 2021, vol. 12, p. 645271.

    Article  Google Scholar 

  14. Kumar, S., Stecher, G., and Tamura, K., MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets, Mol. Biol. Evol., 2016, vol. 33, pp. 1870–1874.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Kurtzman, C.P., Phylogenetic circumscription of Saccharomyces, Kluyveromyces and other members of the Saccharomycetaceae, and the proposal of the new genera Lachancea, Nakaseomyces, Naumovia, Vanderwaltozyma and Zygotorulaspora, FEMS Yeast Res., 2003, vol. 4, pp. 233–245.

    Article  CAS  PubMed  Google Scholar 

  16. Libkind, D., Hittinger, C.T., Valério, E., Gonçalves, C., Dover, J., Johnston, M., Gonçalves, P., and Sampaio, J.P., Microbe domestication and the identification of the wild genetic stock of lager-brewing yeast, Proc. Natl. Acad. Sci. USA, 2011, vol. 108, pp. 14539–14544.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Liti, G., Peruffo, A., James, S.A., Roberts, I.N., and Louis, E.J., Inferences of evolutionary relationships from a population survey of LTR-retrotransposons and telomeric-associated sequences in the Saccharomyces sensu stricto complex, Yeast, 2005, vol. 22, pp. 177–192.

    Article  CAS  PubMed  Google Scholar 

  18. Liti, G., David, B., Barton, H., and Louis, E.J., Sequence diversity, reproductive isolation and species concepts in Saccharomyces, Genetics, 2006, vol. 174, pp. 839–850.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Lõoke, M., Kristjuhan, K., and Kristjuhan, A., Extraction of genomic DNA from yeasts for PCR based applications, Biotechniques, 2011, vol. 50, pp. 325–328.

    Article  PubMed  PubMed Central  Google Scholar 

  20. Louw, C., La Grange, D., Pretorius, I.S, and van Rensburg, P., The effect of polysaccharide-degrading wine yeast transformants on the efficiency of wine processing and wine flavor, J. Biotechnol., 2006, vol. 125, pp. 447–461.

    Article  CAS  PubMed  Google Scholar 

  21. Louw, C., Young, P.R., van Rensburg, P., and Divol, B., Epigenetic regulation of PGU1 transcription in Saccharomyces cerevisiae, FEMS Yeast Res., 2010, vol. 10, pp. 158–167.

    Article  CAS  PubMed  Google Scholar 

  22. Morard, M., Benavent-Gil, Y., Ortiz-Tovar, G., Pérez-Través, L., Querol, A., Toft, Ch., and Barrio, E., Genome structure reveals the diversity of mating mechanisms in Saccharomyces cerevisiae × Saccharomyces kudriavzevii hybrids, and the genomic instability that promotes phenotypic diversity, Microb. Genom., 2020, vol. 6, p. e000333.

    PubMed  PubMed Central  Google Scholar 

  23. Naseeb, S., James, S.A., Alsammar, H., Michaels, C.J., Gini, B., Nueno-Palop, C., Bond, C.J., McGhie, H., Roberts, I.N., and Delneri, D., Saccharomyces jurei sp. nov., isolation and genetic identification of a novel yeast species from Quercus robur, Int. J. Syst. Evol. Microbiol., 2017, vol. 67, pp. 2046–2052.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Naumov, G.I., Genetic basis for classification and identification of the ascomycetous yeasts, Stud. Mycol., 1987, vol. 30, pp. 469–475.

    Google Scholar 

  25. Naumov, G.I., Saccharomyces bayanus var. uvarum comb. nov., a new variety established by genetic analysis, Microbiology (Moscow), 2000, vol. 69, pp. 338–342.

    Article  CAS  Google Scholar 

  26. Naumov, G.I., Ecological and biogeographical features of Saccharomyces paradoxus Batschinskaya yeast and related species: I. The early studies, Microbiology (Moscow), 2013, vol. 82, pp. 397–403.

    Article  CAS  Google Scholar 

  27. Naumov, G.I., Genetic relationship and biological status of the industrially important yeast Saccharomyces eubayanus Sampaio et al., Dokl. Biol. Sci., 2017, vol. 473, pp. 73–76.

    Article  CAS  PubMed  Google Scholar 

  28. Naumov, G.I., Naumova, E.S., and Gaillardin, C., Gene-tic and karyotypic identification of wine Saccharomyces bayanus yeasts isolated in France and Italy, Syst. Appl. Microbiol., 1993, vol. 16, pp. 274–279.

    Article  Google Scholar 

  29. Naumov, G.I., James, S.A., Naumova, E.S., Louis, E.J., and Roberts, I.N., Three new species in the Saccharomyces sensu stricto complex: Saccharomyces cariocanus, Saccharomyces kudriavzevii and Saccharomyces mikatae, Int. J. Evol. Microbiol., 2000, vol. 50, pp. 1931–1942.

    Article  CAS  Google Scholar 

  30. Naumova, E.S., Naumov, G.I., Masneuf-Pomarede, I., Aigle, M., and Dubourdieu, D., Molecular genetic study of introgression between Saccharomyces bayanus and S. cerevisiae, Yeast, 2005, vol. 22, pp. 1099–1115.

    Article  CAS  PubMed  Google Scholar 

  31. Naumov, G.I., Naumova, E.S., Martynenko, N.N., and Masneuf-Pomarède, I., Taxonomy, ecology, and genetics of the yeast Saccharomyces bayanus: a new object for science and practice, Microbiology (Moscow), 2011, vol. 80, pp. 735–742.

    Article  CAS  Google Scholar 

  32. Naumova, E.S., Borovkova, A.N., Naumov, G.I., and Shalamitskiy, M.Y., Natural polymorphism of pectinase PGU genes in the Saccharomyces yeasts, Microbiology (Moscow), 2021, vol. 90, pp. 349–360.

    Article  CAS  Google Scholar 

  33. Nespolo, R.F., Villarroel, C.A., Oporto, C.I., Tapia, S.M., Vega-Macaya, F., Urbina, K., De Chiara, M., Mozzachiodi, S., Mikhalev, E., Thompson, D., Larrondo, L.F., Saenz-Agudelo, P., Liti, G., and Cubillos, F.A., An out-of-patagonia migration explains the worldwide diversity and distribution of Saccharomyces eubayanus lineages, PLoS Genetics, 2020, vol. 16, p. e1008777.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Nikulin, J., Krogerus, K., and Gibson, B., Alternative Saccharomyces interspecies hybrid combinations and their potential for low-temperature wort fermentation, Yeast, 2018, vol. 35, pp. 113–127.

    Article  CAS  PubMed  Google Scholar 

  35. Peris, D., Pérez-Torrado, R., Hittinger, C.T., Barrio, E., and Querol, A., On the origins and industrial applications of Saccharomyces cerevisiae × Saccharomyces kudriavzevii hybrids, Yeast, 2018, vol. 35, pp. 51–69.

    Article  CAS  PubMed  Google Scholar 

  36. Pérez-Través, L., Lopes, C.A., Querol, A., and Barrio, E., On the complexity of the Saccharomyces bayanus taxon: hybridization and potential hybrid speciation, PLoS One, 2014, vol. 9, p. e93729.

    Article  PubMed  PubMed Central  Google Scholar 

  37. Pretorius, I.S., Tasting the terroir of wine yeast innovation, FEMS Yeast Res., 2020, vol. 20, p. foz084.

    Article  CAS  PubMed  Google Scholar 

  38. Redžepović, S., Orlić, S., Majdak, A., Kozina, B., Volschenk, H., and Viljoen-Bloom, M., Differential malic acid degradation by selected strains of Saccharomyces during alcoholic fermentation, Int. J. Food. Microbiol., 2003, vol. 83, pp. 49–61.

    Article  PubMed  Google Scholar 

  39. Rementeria, A., Rodriguez, J.A., Cadaval, A., Amenabar, R., Muguruza, J.R., Hernando, F.L., and Sevilla, M.J., Yeast associated with spontaneous fermentations of white wines from “Txakoli de Bizkaia” region (Basque Country, North Spain), Int. J. Food Microbiol., 2003, vol. 86, pp. 201–207.

    Article  CAS  PubMed  Google Scholar 

  40. Rollero, S., Zietsman, A.J.J., Buffetto, F., Schückel, J., Ortiz-Julien, A., and Divol, B., Kluyveromyces marxianus secretes a pectinase in shiraz grape must that impacts technological properties and aroma profile of wine, Agric. Food Chem., 2018, vol. 66, pp. 11739–11747.

    Article  CAS  Google Scholar 

  41. Sampaio, J.P. and Gonçalves, P., Natural populations of Saccharomyces kudriavzevii in Portugal are associated with oak bark and are sympatric with S. cerevisiae and S. paradoxus, Appl. Environ. Microbiol., 2008, vol. 74, pp. 2144–2152.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Serpova, E.V., Kishkovskaya, S.A., Martynenko, N.N., and Naumova, E.S., Molecular genetic identification of wine yeasts of Crimea, Biotekhnologiya, 2011, no. 6, pp. 47–54.

  43. Torriani, S., Zapparoli, G., and Suzzi, G., Genetic and phenotypic diversity of Saccharomyces sensu stricto strains isolated from Amarone wine, Antonie van Leeuwenhoek, 1999, vol. 5, pp. 207–215.

    Article  Google Scholar 

  44. Tufariello, M., Fragasso, M., Pico, J., Panighel, A., Castellarin, S.D., Flamini, R., and Grieco, F., Influence of Non-Saccharomyces on wine chemistry: a focus on aroma-related compounds, Molecules, 2021, vol. 26, pp. 644–666.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Van Rensburg, P. and Pretorius, I.S., Enzymes in winemaking: harnessing natural catalysts for efficient biotransformations, S. Afr. J. Enol. Viticult., 2000, vol. 21, pp. 52–73.

    CAS  Google Scholar 

  46. Vaughan-Martini, A. and Martini, A., Saccharomyces Meyen ex Reess (1870), in The Yeast, a Taxonomic Study, Kurtzman, C.P., Fell, J.W., and Boekhout, T., Eds., Amsterdam: Elsevier, 2011, 5th ed., vol. 2, pp. 733–746.

    Google Scholar 

  47. Wang, S.A. and Bai, F.Y., Saccharomyces arboricolus sp. nov., a yeast species from tree bark, Int. J. Syst. Evol. Microbiol., 2008, vol. 58, pp. 510–514.

    Article  CAS  PubMed  Google Scholar 

  48. Yue, J.X., Li, J., Aigrain, L., Hallin, J., Persson, K., Oliver, K., Bergstrom, A., Coupland, P., Warringer, J., Lagomarsino, M.C., Fischer, G., Durbin, R., and Liti, G., Contrasting evolutionary genome dynamics between domesticated and wild yeasts, Nature Genet., 2017, vol. 49, pp. 913–924.

    Article  CAS  PubMed  Google Scholar 

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The study was conducted according to the State Assignment AAAA-A20-120093090015-2.

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Correspondence to E. S. Naumova.

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Borovkova, A.N., Shalamitskiy, M.Y. & Naumova, E.S. Pectinolytic Yeast Saccharomyces paradoxus as a New Gene Pool for Winemaking. Microbiology 92, 256–268 (2023). https://doi.org/10.1134/S0026261722602822

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