Skip to main content
SpringerLink
Log in

Natural Polymorphism of Pectinase PGU Genes in the Saccharomyces Yeasts

  • EXPERIMENTAL ARTICLES
  • Published:
Microbiology Aims and scope Submit manuscript

Abstract

The distribution and properties of the pectinase-encoding PGU genes in different species of Saccharomyces yeasts was studied. Application of molecular karyotyping and Southern hybridization revealed that S. arboricola, S. cariocanus, S. cerevisiae, S. kudriavzevii, and S. paradoxus species had a single PGU gene located on chromosome X. The other three species had polymeric PGU genes of different chromosomal localization: S. mikatae and S. jurei (chromosomes X and VIII), S. bayanus (X, I, and XIV). This is the first report on comparative analysis of the nucleotide and amino acid sequences of the PGU genes was carried out in all eight species of the genus Saccharomyces. Species-specificity of the PGU genes was revealed, as well as their intraspecific polymorphism in S. kudriavzevii and S. paradoxus, associated with the geographical origin of the strains. The most divergent proteins were Pgu1a (S. arboricola) and Pgu1b, Pgu2b, Pgu3b (S. bayanus), for which the level of similarity to the Pgu proteins of other Saccharomyces species did not exceed 89%. The highest similarity (>95%) was noted for the Pgu proteins of S. cerevisiae, S. paradoxus, and S. cariocanus, as well as S. mikatae and S. jurei. Significant intraspecific polymorphism of endo-polygalacturonase secretion was observed in the studied Saccharomyces species, except for the species S. bayanus, all studied strains of which had a relatively high activity. The ability to secrete active endo-polygalacturonase is probably a specific feature of this species.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.
Fig. 5.

Similar content being viewed by others

REFERENCES

  1. Bon, E., Neuvéglise, C., Casaregola, S., Artiguenave, F., Wincker, P., Aigle, M., and Durrens, P., Genomic exploration of the hemiascomycetous yeasts: 5. Saccharomyces bayanus var. uvarum, FEBS Lett., 2000, vol. 487, pp. 37–41.

    Article  CAS  PubMed  Google Scholar 

  2. Borovkova, A.N., Michailova, Yu.V., and Naumova, E.S., Molecular genetic features of biological species of the genus Saccharomyces, Microbiology (Moscow), 2020, vol. 89, pp. 387–395.

    Article  CAS  Google Scholar 

  3. Bussink, H.J., Buxton, F.P., Fraaye, B.A., de Graaff, L.H., and Visser, J., The polygalacturonases of Aspergillus niger are encoded by a family of diverged genes, Eur. J. Biochem., 1992, vol. 208, pp. 83–90.

    Article  CAS  PubMed  Google Scholar 

  4. 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 

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

    Article  CAS  PubMed  Google Scholar 

  6. 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 

  7. Fischer, G., James, S.A., Roberts, I.N., Oliver, S.G., and Louis, E.S., Chromosomal evolution in Saccharomyces, Nature, 2000, vol. 405, pp. 451–454.

    Article  CAS  PubMed  Google Scholar 

  8. Fraissinet-Tacher, L., Reymond-Cotton, P., and Fevre, M., Characterization of a multigene family encoding an endopolygalacturonase in Sclerotinia sclerotiorum, Curr. Genet., 1995, vol. 29, pp. 96–99.

    Article  Google Scholar 

  9. Gainvors, A., Karam, N., Lequart, C., and Belarbi, A., Use of Saccharomyces cerevisiae for the clarification of fruit juices, Biotechnol. Lett., 1994, vol. 16, pp. 1329–1334.

    CAS  Google Scholar 

  10. Gognies, S., Gainvors, A., Aigle, M., and Belarbi, A., Cloning, sequence analysis and overexpression of a Saccharomyces cerevisiae endopolygalacturonase-encoding gene (PGL1), Yeast, 1999, vol. 15, pp. 11−22.

    Article  CAS  PubMed  Google Scholar 

  11. Hittinger, C.T., Rokas, A., and Carroll, S.B., Parallel inactivation of multiple GAL pathway genes and ecological diversification in yeasts, Proc. Natl. Acad. Sci. USA, 2004, vol. 101, pp. 14144‒14149.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Imshemenetskii, A.A., Kondrat’eva, T.F., Lin’kova, M.A., Datunashvili, E.N., Bur’yan, N.I., Pokrovskaya, S.S., Skorikova, T.K., and Sonina, E.G., Patent SU 1495368, 1985.

  13. 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 

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

    Article  CAS  PubMed  Google Scholar 

  15. 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 

  16. 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 

  17. Liti, G., Carter, D.M., Moses, A.M., Warringer, J., Parts, L., James, S.A., Davey, R.P., Roberts, I.N., Burt, A., Koufopanou, V., Tsai, I.J., Bergman, C.M., Bensasson, D., O’Kelly, M.J.T., van Oudenaarden, A., et al., Population genomics of domestic and wild yeasts, Nature, 2009, vol. 458, pp. 337–341.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Liti, G., Nguyen Ba, A.N., Blythe, M., Müller, C.A., Bergström, A., Cubillos, F.A., Dafhnis-Calas, F., Khosh-raftar, S., Malla, S., Mehta, N., Siow, C.C., Warringer, J., Moses, A.M., Louis, E.J., and Nieduszynski, C.A., High quality de novo sequencing and assembly of the Saccharomyces arboricolus genome, BMC Genomics, 2013, vol. 14, art. 69. https://doi.org/10.1186/1471-2164-14-69

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. 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 

  20. 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 

  21. 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  CAS  Google Scholar 

  22. 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 

  23. Naumov, G.I., Genetic identification of biological species in the Saccharomyces sensu stricto complex, J. Indust. Microbiol., 1996, vol. 17, pp. 295–302.

    CAS  Google Scholar 

  24. Naumov, G.I., Genetic identification of Saccharomyces kudriavzevii yeast from a European population, Ekol. Ge-net., 2009, vol. 7, no. 1, pp. 9–11.

    Google Scholar 

  25. 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 

  26. Naumov, G.I., Naumova, E.S., and Gaillardin, C., Genetic 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 

  27. Naumov, G.I., Naumova, E.S., and Sniegowski, P.D., Differentiation of European and Far East Asian populations of Saccharomyces paradoxus by allozyme analysis, Int. J. System. Bacteriol., 1997a, vol. 47, pp. 341–344.

    Article  CAS  Google Scholar 

  28. 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., 2000a, vol. 50, pp. 1931–1942.

    Article  CAS  Google Scholar 

  29. Naumov, G.I., Masneuf-Pomarède, I., Naumova, E.S., Aigle, M., and Dubourdieu, D., Association of S. bayanus var. uvarum with some French wines: genetic analysis of yeast populations, Res. Microbiol., 2000b, vol. 151, pp. 683–691.

    Article  CAS  PubMed  Google Scholar 

  30. Naumov, G.I., Naumova, E.S., Aigle, M., Masneuf-Pomarede, I., and Belarbi, A., Genetic reidentification of the pectinolytic yeast strain SCPP as Saccharomyces bayanus var. uvarum, Appl. Microbiol. Biotechnol., 2001a, vol. 55, pp. 108–111.

    Article  CAS  PubMed  Google Scholar 

  31. Naumov, G.I., Nguyen, H.-V., Naumova, E.S., Michel, A., Aigle, M., and Gaillardin, C., Genetic identification of Saccharomyces bayanus var. uvarum, a cider-fermenting yeast, Int. J. Food Microbiol., 2001b, vol. 65, pp. 163–171.

    Article  CAS  PubMed  Google Scholar 

  32. Naumov, G.I., Naumova, E.S., Antunovics, A., and Sipiczki, M., Saccharomyces bayanus var. uvarum in Tokaj wine-making of Slovakia and Hungary, Appl. Microbiol. Biotechnol., 2002, vol. 59, pp. 727–730.

    Article  CAS  PubMed  Google Scholar 

  33. Naumov, G.I., Naumova, E.S., and Masneuf-Pomarède, I., Genetic identification of new biological species Saccharomyces arboricolus Wang et Bai, Antonie van Leeuwenhoek, 2010, vol. 98, pp. 1–7.

    Article  PubMed  Google Scholar 

  34. 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 

  35. Naumov, G.I., Shalamitskiy, M.Y., Naumova, E.S., and Martynenko, N.N., Molecular phylogeny of pectinase genes PGU in the yeast genus Saccharomyces, Microbiology (Moscow), 2016a, vol. 85, pp. 717–726.

    Article  CAS  Google Scholar 

  36. Naumov, G.I., Shalamitskiy, M.Y., and Naumova, E.S., New family of pectinase genes PGU1b–PGU3b of the pectinolytic yeast Saccharomyces bayanus var. uvarum, Dokl. Biochem. Biophys., 2016b, vol. 467, pp. 89–91.

    Article  CAS  PubMed  Google Scholar 

  37. Naumova, E.S., Naumov, G.I., and Korhola M., Molecular karyotypes of various genetic lines of the yeast Saccharomyces cerevisiae, Bioteknologiya, 1993, no. 4, pp. 1–4.

  38. Naumova, E.S., Naumov, G.I., Masneuf-Pomarède, 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 

  39. Naumova, E.S., Serpova, E.V., Korshunova, I.V., and Naumov, G.I., Molecular polymorphism of α-galactosidase MEL genes of Saccharomyces yeasts, Microbiology (Moscow), 2011, vol. 80, pp. 502–513.

    Article  CAS  Google Scholar 

  40. Naumova, E.S., Shalamitskiy, M.Yu., and Naumov, G.I., Molecular polymorphism of pectinase genes PGU of Saccharomyces bayanus var. uvarum yeast, Appl. Biochem. Microbiol., 2019, vol. 55, pp. 882–887.

    Article  CAS  Google Scholar 

  41. Panon, G., Massiot, P., and Drilleau, J.-F., Production d’enzymes pectinolytiques par les levures d`intérêt cidricole, Sciences des Aliments, 1995, vol. 15, pp. 31–42.

    CAS  Google Scholar 

  42. Pérez-Torrado, R., Barrio, E., and Querol, A., Alternative yeasts for winemaking: Saccharomyces non-cerevisiae and its hybrids, Crit. Rev. Food Sci. Nutr., 2018, vol. 58, pp. 1780–1790.

    Article  PubMed  CAS  Google Scholar 

  43. 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), Ind. J. Food. Microbiol., 2003, vol. 86, pp. 201–207.

    Article  CAS  Google Scholar 

  44. 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 

  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., Boekhout, T., Eds., Amsterdam: Elsevier, 2011, vol. 2, 5th ed., 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 

Download references

Funding

This work was conducted as a part of State Assignment no. AAAA-A20-120093090015-2.

Author information

Authors and Affiliations

  1. State Research Institute of Genetics and Selection of Industrial Microorganisms, National Research Center “Kurchatov Institute”, 117519, Moscow, Russia

    E. S. Naumova, A. N. Borovkova & G. I. Naumov

  2. Department of Mycology and Algology, Moscow State University, 119234, Moscow, Russia

    A. N. Borovkova

  3. Magarach All-Russian National Institute for Vine and Winemaking, Russian Academy of Sciences, 298600, Yalta, Russia

    M. Yu. Shalamitskiy

Authors
  1. E. S. Naumova
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. N. Borovkova
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. M. Yu. Shalamitskiy
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. G. I. Naumov
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to E. S. Naumova.

Ethics declarations

Conflict of interests. The authors declare that they have no conflict of interest.

Statement on the welfare of animals. This article does not contain any studies involving animals or human participants performed by any of the authors.

Additional information

Translated by D. Timchenko

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Naumova, E.S., Borovkova, A.N., Shalamitskiy, M.Y. et al. Natural Polymorphism of Pectinase PGU Genes in the Saccharomyces Yeasts. Microbiology 90, 349–360 (2021). https://doi.org/10.1134/S0026261721030085

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0026261721030085

Keywords:

Search

Navigation