1887

Abstract

Two strains, D5088 and D5095, representing a novel yeast species belonging to the genus were isolated from oak tree bark and surrounding soil located at an altitude of 1000 m above sea level in Saint Auban, France. Sequence analyses of the internal transcribed spacer (ITS) region and 26S rRNA D1/D2 domains indicated that the two strains were most closely related to and . Genetic hybridization analyses showed that both strains are reproductively isolated from all other species and, therefore, represent a distinct biological species. The species name sp. nov. is proposed to accommodate these two strains, with D5088 (=CBS 14759=NCYC 3947) designated as the type strain.

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2017-06-01
2024-12-07
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References

  1. Martini AV, Martini A. Three newly delimited species of Saccharomyces sensu stricto. Antonie van Leeuwenhoek 1987; 53:77–84 [View Article][PubMed]
    [Google Scholar]
  2. Wang SA, Bai FY. Saccharomyces arboricolus sp. nov., a yeast species from tree bark. Int J Syst Evol Microbiol 2008; 58:510–514 [View Article][PubMed]
    [Google Scholar]
  3. Naumov GI, James SA, Naumova ES, Louis EJ, Roberts IN. Three new species in the Saccharomyces sensu stricto complex: Saccharomyces cariocanus, Saccharomyces kudriavzevii and Saccharomyces mikatae. Int J Syst Evol Microbiol 2000; 50:1931–1942 [View Article][PubMed]
    [Google Scholar]
  4. Naumov GI, Naumova ES, Hagler AN, Mendonça-Hagler LC, Louis EJ. A new genetically isolated population of the Saccharomyces sensu stricto complex from Brazil. Antonie van Leeuwenhoek 1995; 67:351–355 [View Article][PubMed]
    [Google Scholar]
  5. Naumov GI, Naumova ES, Louis EJ. Two new genetically isolated populations of the Saccharomyces sensu stricto complex from Japan. J Gen Appl Microbiol 1995; 41:499–505 [View Article]
    [Google Scholar]
  6. Libkind D, Hittinger CT, Valério E, Gonçalves C, Dover J et al. Microbe domestication and the identification of the wild genetic stock of lager-brewing yeast. Proc Natl Acad Sci USA 2011; 108:14539–14544 [View Article][PubMed]
    [Google Scholar]
  7. Masneuf I, Hansen J, Groth C, Piskur J, Dubourdieu D. New hybrids between Saccharomyces sensu stricto yeast species found among wine and cider production strains. Appl Environ Microbiol 1998; 64:3887–3892[PubMed]
    [Google Scholar]
  8. Querol A, Bond U. The complex and dynamic genomes of industrial yeasts. FEMS Microbiol Lett 2009; 293:1–10 [View Article][PubMed]
    [Google Scholar]
  9. Nguyen HV, Legras JL, Neuvéglise C, Gaillardin C. Deciphering the hybridisation history leading to the lager lineage based on the mosaic genomes of Saccharomyces bayanus strains NBRC1948 and CBS380. PLoS One 2011; 6:e25821 [View Article][PubMed]
    [Google Scholar]
  10. Liti G, Barton DB, Louis EJ. Sequence diversity, reproductive isolation and species concepts in Saccharomyces. Genetics 2006; 174:839–850 [View Article][PubMed]
    [Google Scholar]
  11. Liti G, Carter DM, Moses AM, Warringer J, Parts L et al. Population genomics of domestic and wild yeasts. Nature 2009; 458:337–341 [View Article][PubMed]
    [Google Scholar]
  12. Hittinger CT. Saccharomyces diversity and evolution: a budding model genus. Trends Genet 2013; 29:309–317 [View Article][PubMed]
    [Google Scholar]
  13. Boynton PJ, Greig D. The ecology and evolution of non-domesticated Saccharomyces species. Yeast 2014; 31:449–462 [View Article][PubMed]
    [Google Scholar]
  14. Bing J, Han PJ, Liu WQ, Wang QM, Bai FY. Evidence for a Far East Asian origin of lager beer yeast. Curr Biol 2014; 24:R380–R381 [View Article][PubMed]
    [Google Scholar]
  15. Gayevskiy V, Goddard MR. Saccharomyces eubayanus and Saccharomyces arboricola reside in North Island native New Zealand forests. Environ Microbiol 2016; 18:1137–1147 [View Article][PubMed]
    [Google Scholar]
  16. Peris D, Sylvester K, Libkind D, Gonçalves P, Sampaio JP et al. Population structure and reticulate evolution of Saccharomyces eubayanus and its lager-brewing hybrids. Mol Ecol 2014; 23:2031–2045 [View Article][PubMed]
    [Google Scholar]
  17. Greig D. Reproductive isolation in Saccharomyces. Heredity 2009; 102:39–44 [View Article][PubMed]
    [Google Scholar]
  18. Duina AA, Miller ME, Keeney JB. Budding yeast for budding geneticists: a primer on the Saccharomyces cerevisiae model system. Genetics 2014; 197:33–48 [View Article][PubMed]
    [Google Scholar]
  19. Schoch CL, Seifert KA, Huhndorf S, Robert V, Spouge JL et al. Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi. Proc Natl Acad Sci USA 2012; 109:6241–6246 [View Article][PubMed]
    [Google Scholar]
  20. White TJ, Bruns TD, Lee S, Taylor JW. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In Innis M, Gelfand DH, Sninsky JJ, White TJ. (editors) PCR Protocols San Diego, Calif: Academic Press; 1990 pp. 315–322
    [Google Scholar]
  21. Kurtzman CP, Robnett CJ. Molecular relationships among hyphal ascomycetous yeasts and yeastlike taxa. Canadian Journal of Botany 1995; 73:824–830 [View Article]
    [Google Scholar]
  22. Naumov GI, Naumova ES, Masneuf-Pomarède I. Genetic identification of new biological species Saccharomyces arboricolus Wang et Bai. Antonie van Leeuwenhoek 2010; 98:1–7 [View Article][PubMed]
    [Google Scholar]
  23. Kurtzman CP, Robnett CJ. Phylogenetic relationships among yeasts of the 'Saccharomyces complex' determined from multigene sequence analyses. FEMS Yeast Res 2003; 3:417–432 [View Article][PubMed]
    [Google Scholar]
  24. Ciardo DE, Schär G, Böttger EC, Altwegg M, Bosshard PP. Internal transcribed spacer sequencing versus biochemical profiling for identification of medically important yeasts. J Clin Microbiol 2006; 44:77–84 [View Article][PubMed]
    [Google Scholar]
  25. Vu D, Groenewald M, Szöke S, Cardinali G, Eberhardt U et al. DNA barcoding analysis of more than 9 000 yeast isolates contributes to quantitative thresholds for yeast species and genera delimitation. Stud Mycol 2016; 85:91–105 [View Article][PubMed]
    [Google Scholar]
  26. Charron G, Leducq JB, Bertin C, Dubé AK, Landry CR. Exploring the northern limit of the distribution of Saccharomyces cerevisiae and Saccharomyces paradoxus in North America. FEMS Yeast Res 2014; 14:281–288 [View Article][PubMed]
    [Google Scholar]
  27. Naumov GI, Lee CF, Naumova ES. Molecular genetic diversity of the Saccharomyces yeasts in Taiwan: Saccharomyces arboricola, Saccharomyces cerevisiae and Saccharomyces kudriavzevii. Antonie van Leeuwenhoek 2013; 103:217–228 [View Article][PubMed]
    [Google Scholar]
  28. Naumov GI, Naumova ES, Hagler AN, Mendonça-Hagler LC, Louis EJ. A new genetically isolated population of the Saccharomyces sensu stricto complex from Brazil. Antonie van Leeuwenhoek 1995; 67:351–355 [View Article][PubMed]
    [Google Scholar]
  29. Johnson LJ, Koufopanou V, Goddard MR, Hetherington R, Schäfer SM et al. Population genetics of the wild yeast Saccharomyces paradoxus. Genetics 2004; 166:43–52 [View Article][PubMed]
    [Google Scholar]
  30. Naumov GI, Naumova ES, Sniegowski PD. Saccharomyces paradoxus and Saccharomyces cerevisiae are associated with exudates of north American Oaks. Can J Microbiol 1998; 44:1045–1050[PubMed] [CrossRef]
    [Google Scholar]
  31. Sniegowski PD, Dombrowski PG, Fingerman E. Saccharomyces cerevisiae and Saccharomyces paradoxus coexist in a natural woodland site in North America and display different levels of reproductive isolation from european conspecifics. FEMS Yeast Res 2002; 1:299–306[PubMed]
    [Google Scholar]
  32. González SS, Barrio E, Gafner J, Querol A. Natural hybrids from Saccharomyces cerevisiae, Saccharomyces bayanus and Saccharomyces kudriavzevii in wine fermentations. FEMS Yeast Res 2006; 6:1221–1234 [View Article][PubMed]
    [Google Scholar]
  33. Hyma KE, Fay JC. Mixing of vineyard and oak-tree ecotypes of Saccharomyces cerevisiae in North American vineyards. Mol Ecol 2013; 22:2917–2930 [View Article][PubMed]
    [Google Scholar]
  34. Naumov GI, Naumova ES, Sancho ED. Genetic reidentification of Saccharomyces strains associated with black knot disease of trees in Ontario and Drosophila species in California. Can J Microbiol 1996; 42:335–339 [View Article]
    [Google Scholar]
  35. Kurtzman CP, Fell JW, Boekhout T, Robert V. Methods for isolation, phenotypic characterization and maintenance of yeasts. In Kurtzman CP, Fell JW, Boekhout T. (editors) The Yeasts, a Taxonomic Study, 5th ed. Amsterdam: Elsevier; 2011 pp. 87–110 [CrossRef]
    [Google Scholar]
  36. O’Donnell K. Fusarium and its near relatives. In Reynolds DR, Taylor JW. (editors) The Fungal Holomorph: Mitotic, Meiotic and Pleomorphic Speciation in Fungal Systematics Wallingford: CAB International; 1993 pp. 225–233
    [Google Scholar]
  37. James SA, Collins MD, Roberts IN. Use of an rRNA internal transcribed spacer region to distinguish phylogenetically closely related species of the genera Zygosaccharomyces and Torulaspora. Int J Syst Bacteriol 1996; 46:189–194 [View Article][PubMed]
    [Google Scholar]
  38. Pearson WR, Lipman DJ. Improved tools for biological sequence comparison. Proc Natl Acad Sci USA 1988; 85:2444–2448 [View Article][PubMed]
    [Google Scholar]
  39. Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 1994; 22:4673–4680 [View Article][PubMed]
    [Google Scholar]
  40. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: molecular evolutionary Genetics analysis version 6.0. Mol Biol Evol 2013; 30:2725–2729 [View Article][PubMed]
    [Google Scholar]
  41. Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 1987; 4:406–425[PubMed]
    [Google Scholar]
  42. Huxley C, Green ED, Dunham I. Rapid assessment of S. cerevisiae mating type by PCR. Trends Genet 1990; 6:236[PubMed] [CrossRef]
    [Google Scholar]
  43. Güldener U, Heck S, Fielder T, Beinhauer J, Hegemann JH. A new efficient gene disruption cassette for repeated use in budding yeast. Nucleic Acids Res 1996; 24:2519–2524 [View Article][PubMed]
    [Google Scholar]
  44. Delneri D, Colson I, Grammenoudi S, Roberts IN, Louis EJ et al. Engineering evolution to study speciation in yeasts. Nature 2003; 422:68–72 [View Article][PubMed]
    [Google Scholar]
  45. Naumov GI, Naumova ES, Querol A. Genetic study of natural introgression supports delimitation of biological species in the Saccharomyces sensu stricto complex. Syst Appl Microbiol 1997; 20:595–601 [View Article]
    [Google Scholar]
  46. Naumov GI. Genetic basis for classification and identification of the ascomycetous yeasts. Stud Mycol 1987; 30:469–475
    [Google Scholar]
  47. Roeder GS. Meiotic chromosomes: it takes two to tango. Genes Dev 1997; 11:2600–2621 [View Article][PubMed]
    [Google Scholar]
  48. Greig D, Travisano M, Louis EJ, Borts RH. A role for the mismatch repair system during incipient speciation in Saccharomyces. J Evol Biol 2003; 16:429–437 [View Article][PubMed]
    [Google Scholar]
  49. Coyne JA, Orr HA. Speciation Sunderland: Sinauer; 2004 pp. 256–267
    [Google Scholar]
  50. Hou J, Friedrich A, de Montigny J, Schacherer J. Chromosomal rearrangements as a major mechanism in the onset of reproductive isolation in Saccharomyces cerevisiae. Curr Biol 2014; 24:1153–1159 [View Article][PubMed]
    [Google Scholar]
  51. Martini AV. Martini A. Saccharomyces Meyen ex Reess (1870). In Kurtzman CP, Fell JW, Boekhout T. (editors) The Yeasts, a Taxonomic Study, 5th ed. Amsterdam: Elsevier; 2011 pp. 733–746 [CrossRef]
    [Google Scholar]
  52. Vaughan-Martini A, Martini A. Saccharomyces Meyen ex Reess (1870). In Kurtzman CP, Fell JW, Boekhout T. (editors) The Yeasts, a Taxonomic Study, 5th ed. Amsterdam: Elsevier; 2011 pp. 733–746 [CrossRef]
    [Google Scholar]
  53. Scheda R, Yarrow D. Variation in the fermentative pattern of some Saccharomyces species. Arch Mikrobiol 1968; 61:310–316 [View Article][PubMed]
    [Google Scholar]
  54. Scheda R, Yarrow D. The instability of physiological properties used as criteria in the taxonomy of yeasts. Archiv für Mikrobiologie 1966; 55:209–225 [View Article]
    [Google Scholar]
  55. Naumov GI, Naumova ES, Michels CA. Genetic variation of the repeated MAL loci in natural populations of Saccharomyces cerevisiae and Saccharomyces paradoxus. Genetics 1994; 136:803–812[PubMed]
    [Google Scholar]
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