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Molecular phylogeny of pectinase genes PGU in the yeast genus Saccharomyces

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Abstract

Using yeast genome databases and literature data, phylogenetic analysis of pectinase PGU genes from 112 Saccharomyces strains assigned to the biological species S. arboricola, S. bayanus (var. uvarum), S. cariocanus, S. cerevisiae, S. kudriavzevii, S. mikatae, S. paradoxus, and the hybrid taxon S. pastorianus (syn. S. carlsbergensis) was carried out. A superfamily of divergent PGU genes was found. Natural interspecies transfer of the PGU gene both from S. cerevisiae to S. bayanus and from S. paradoxus to S. cerevisiae may, however, occur. Within the Saccharomyces species, identity of the PGU nucleotide sequences was 98.8–100% for S. cerevisiae, 86.1–95.7% for S. bayanus (var. uvarum), 94–98.3% for S. kudriavzevii, and 96.8–100% for S. paradoxus/S. cariocanus. For the first time, a family of polymeric PGU1b, PGU2b, PGU3b and PGU4b genes is documented for the yeast S. bayanus var. uvarum, a variety important for winemaking.

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References

  • Baker, E., Wang, B., Bellora, N., Peris, D., Hulfachor, A.B., Koshalek, J.A., Adams, M., Libkind, D., and Hittinger, C.T., The genome sequence of Saccharomyces eubayanus and the domestication of lager-brewing yeasts, Mol. Biol. Evol., 2015, vol. 32, no. 11, pp. 2818–2831.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bing, J., Han, P.J., Liu, W.Q., Wang, Q.M., and Bai, F.Y., Evidence for a Far East Asian origin of lager beer yeast, Curr. Biol., 2014, vol. 24, no. 10, pp. R380–381.

    Article  CAS  PubMed  Google Scholar 

  • Blanco, P., Sieiro, C., Reboredo, N.M., and Villa, T.G., Genetic determination of polygalacturonase production in wild-type and laboratory strains of Saccharomyces cerevisiae, Arch. Microbiol., 1997, vol. 167, pp. 284–288.

    Article  CAS  PubMed  Google Scholar 

  • Blanco, P., Sieiro, S., Reboredo, N.M., and Villa, T.G., Cloning,molecular characterization,and expression of an endo-polygalacturonase-encoding gene from Saccharomyces cerevisiae IM1-8b, FEMS Microbiol. Lett., 1998, vol. 64, pp. 249–255.

    Article  Google Scholar 

  • 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 

  • Bussink, H.J., Buxton, F.P., Fraaye, B.A., de Graaff, L.H., and Visser, J., The polygalacturonase 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 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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 

  • Gognies, S. and Belarbi A., Endopolygalacturonase of Saccharomyces cerevisiae: involvement in pseudohyphae development of haploids and in pathogenicity on Vitis vinifera, Plant Sci., 2002, vol. 163, pp. 759–769.

    Article  CAS  Google Scholar 

  • 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, no. 3. pii: fov005. Epub 2015 Mar 4. doi 10.1093/femsyr/fov005

    Article  PubMed  Google Scholar 

  • Hirose, N.K., Kishida, M., Kawasaki, H.,and Sakai, T., Molecular cloning and expression of a polygalacturonase gene in Saccharomyces cerevisiae, J. Ferment. Bioeng., 1998, vol. 86, pp. 332–334.

    Article  CAS  Google Scholar 

  • Jia, J. and Wheals, A., Endopolygalacturonase genes and enzymes from Saccharomyces cerevisiae and Kluyveromyces marxianus, Curr. Genet., 2000, vol. 38, pp. 264–270.

    Article  CAS  PubMed  Google Scholar 

  • Kellis, M., Patterson, N., Endrizzi, M., Birren, B., and Lander, E.S., Sequencing and comparison of yeast species to identify genes and regulatory elements, Nature, 2003, vol. 423, pp. 241–254.

    Article  CAS  PubMed  Google Scholar 

  • 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. U. S. A., 2011, vol. 108, no. 35, pp. 14539–14544.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.N., 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 

  • Liti, G., Nguyen Ba, A.N., Blythe, M., Müller, C.A, Bergström, A., Cubillos, F.A., Dafhnis-Calas, F., Khoshraftar, 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, p. 69.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Louw, C., Young, P.R., Rensburg, P., and Divol, B., Regulation of endo-polygalacturonase activity in Saccharomyces cerevisiae, FEMS Yeast Res., 2010, vol. 10, pp. 44–57.

    Article  CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Naumov, G.I., Naumova, E.S., Lantto, R.A., Louis, E.J., and Korhola, M., Genetic homology between Saccharomyces cerevisiae and its sibling species S. paradoxus and S. bayanus: electrophoretic karyotypes, Yeast, 1992, vol. 8, pp. 599–612.

    Article  CAS  PubMed  Google Scholar 

  • Naumov, G., Naumova, E., 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 

  • 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, no. 6, pp. 735–742.

    CAS  Google Scholar 

  • 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. Syst. Evol. Microbiol., 2000, vol. 50, pp. 1931–1942.

    Article  CAS  PubMed  Google Scholar 

  • Naumov, G.I., Naumova, E.S., Aigle, M., Masneuf, 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 

  • 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 

  • 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 

  • 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. Syst. Bacteriol., 1997, vol. 47, pp. 341–344.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Naumova, E.S., Naumov, G.I., Michailova, Y.V., Martynenko, N.N., and Masneuf-Pomarède, I., Genetic diversity study of the yeast Saccharomyces bayanus var. uvarum reveals introgressed subtelomeric Saccharomyces cerevisiae genes, Res. Microbiol., 2011, vol. 162, pp. 204–213.

    Article  CAS  PubMed  Google Scholar 

  • Panon, G., Massiot, P., and Drilleau, J.-F., Production dènzymes pectinolytiques par les levures dintérêt cidricole, Sciences des Aliments, 1995, vol. 15, pp. 31–42.

    CAS  Google Scholar 

  • Šiekštele, R., Bartkeviciute, D., and Sasnauskas, K., Cloning,targeted disruption and heterologous expression of the Kluyveromyces marxianus endopolygalacturonase gene (EPG1), Yeast, 1999, vol. 15, pp. 311–322.

    Article  PubMed  Google Scholar 

  • Strope, P.K., Skelly, D.A., Kozmin, S.G., Mahadevan, G., Stone, E.A., Magwene, P.M., Dietrich, F.S., and McCusker, J.H., The 100-genomes strains,an S. cerevisiae resource that illuminates its natural phenotypic and genotypic variation and emergence as an opportunistic pathogen, Genome Res., 2015, vol. 25, pp. 762–774.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Talarek, N., Louis, E.J., Cullin, C., and Aigle, M., Developing methods and strains for genetic studies in the Saccharomyces bayanus var. uvarum species, Yeast, 2004, vol. 21, pp. 1195–1203.

    Article  CAS  PubMed  Google Scholar 

  • Tamura, K., Peterson, D., Stecher, G., Filipski, A., and Kumar, S., MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0, Mol. Biol. Evol., 2013, vol. 30, pp. 2725–2729.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vaughan Martini, A. and Kurtzman, C.P., Deoxyribonucleic acid relatedness among species of the genus Saccharomyces sensu stricto, Int. J. Syst. Bacteriol., 1985, vol. 35, pp. 508–511.

    Article  Google Scholar 

  • 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., 5th ed., Amsterdam: Elsevier, 2011, vol. 2, pp. 733–746.

    Article  Google Scholar 

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Correspondence to G. I. Naumov.

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Original Russian Text © G.I. Naumov, M.Yu. Shalamitskiy, N.N. Martynenko, E.S. Naumova, 2016, published in Mikrobiologiya, 2016, Vol. 85, No. 6, pp. 703–712.

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Naumov, G.I., Shalamitskiy, M.Y., Martynenko, N.N. et al. Molecular phylogeny of pectinase genes PGU in the yeast genus Saccharomyces . Microbiology 85, 717–726 (2016). https://doi.org/10.1134/S0026261716060163

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