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Genetic identification of biological species in theSaccharomyces sensu stricto complex

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Journal of Industrial Microbiology

Abstract

Studies on taxonomic and evolutionary genetics of theSaccharomyces sensu stricto complex are considered in light of the biological species concept. Genetic variability of some physiological properties traditionally used in yeast taxonomy is discussed. Genetic hybridization analysis and molecular karyotyping revealed six biological species in theSaccharomyces sensu stricto complex. DNA-DNA reassociation data are concordant with the data obtained by genetic analysis. A new system for naming the cultivatedSaccharomyces yeast (groups of cultivars) is proposed.

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References

  1. Arabidze GV. 1968. Biochemical peculiarities of yeasts of theS. uvarum species. Appl Biochem Microbiol 4: 603–606 (in Russian).

    Google Scholar 

  2. Banno I and Y Kaneko. 1989. A genetic analysis of taxonomic relation betweenSaccharomyces cerevisiae andSaccharomyces bayanus. Yeast 5: S373-S377.

    PubMed  Google Scholar 

  3. Bashtannaya II. 1970. Functional peculiarities of yeast races under conditions of primary wine making of Moldavia and their life activity at low temperatures. Thesis, Moldavian Academy of Sciences, Kishinev (in Russian).

    Google Scholar 

  4. Batschinskaya AA. 1914. Entwicklungsgeschichte und Kultur des neuen HefepilzesSaccharomyces paradoxus. J Microbiol Epidemiol Immunobiol 1: 231–247.

    Google Scholar 

  5. Bicknell JN and HC Douglas. 1970. Nucleic acid homologies among species ofSaccharomyces. J Bacteriol 101: 505–512.

    PubMed  Google Scholar 

  6. Carlson M, JL Celenza and FJ Eng. 1985. Evolution of the dispersedSUC gene family ofSaccharomyces by rearrangements of chromosome telomeres. Mol Cell Biol 5: 2894–2902.

    PubMed  Google Scholar 

  7. Charron MJ, E Reed, SR Haut and CA Michels. 1985. Molecular evolution of the telomere-associatedMAL loci ofSaccharomyces. Genetics 122: 307–316.

    Google Scholar 

  8. Gilliland RB. 1949. A yeast hybrid heterozygotic in four fermentation characters. Compt Rend Trav Lab Carlsberg Ser Physiol 24: 347–356.

    Google Scholar 

  9. Gilliland RB. 1953. The genetics of super-attenuation. In: Europ Brewery Convention, Proc Congress, pp 121–134, Nice.

  10. Gilliland RB. 1954. A study of a wild yeast—Saccharomyces diastaticus. Wallerstein Lab Comm 17: 165–167.

    Google Scholar 

  11. Giudici P, C Zambonelli, P Passarelli and L Castellari. 1995. Improvement of wine composition with cryotolerantSaccharomyces strains. Am J Enol Vitic 46: 143–147.

    Google Scholar 

  12. Hawthorne D and P Philippsen. 1994. Genetic and molecular analysis of hybrids in the genusSaccharomyces involvingS. cerevisiae, S. uvarum and a new species,S. douglasii. Yeast 10: 1285–1296.

    PubMed  Google Scholar 

  13. Jensen V. 1967. Taxonomic studies on soil yeasts I. The genusSaccharomyces (Meyen) Reess. Arsskr K Vet Landbohoejsk, Copenhagen: 179–194.

  14. Jonston JR and RK Mortimer. 1986. Electrophoretic karyotyping of laboratory and commercial strains ofSaccharomyces and other yeasts. Int J Syst Bacteriol 36: 569–572.

    Google Scholar 

  15. Kaneko Y and I Banno. 1991. Reexamination ofSaccharomyces bayanus strains by DNA-DNA hybridization and electrophoretic karyotyping. IFO Res Comm 15: 30–41.

    Google Scholar 

  16. Kishimoto M. 1994. Fermentation characteristics of hybrids between cryophilic wine yeastSaccharomyces bayanus and the mesophilic wine yeastSaccharomyces cerevisiae. J Ferment Bioeng 77: 432–435.

    Google Scholar 

  17. Kishimoto M, E Soma and Sh Goto. 1994. Classification of cryophilic wine yeasts based on electrophoretic karyotype, G+C content and DNA similarity. J Gen Appl Microbiol 40: 83–93.

    Google Scholar 

  18. Kondrat'eva VI and GI Naumov. 1979. Comparative genetics of yeast XX. Study of natural heterothallicSaccharomyces. Soviet Genetics 15: 663–670.

    Google Scholar 

  19. Kudrjawzew WI. 1960. Die Systematik der Hefen. Akademie Verlag, Berlin, 324 pp.

    Google Scholar 

  20. Lemos GA, P Valente, D Pimentel, AN Hagler and LC Mendonça-Hagler. 1995. Characterization ofSaccharomyces paradoxus and a new species ofSaccharomyces from Brazilian ecosystem. Abstracts. Seventh International Symposium on Microbial Ecology (ISME-7). Santos-Saõ-Paulo, Brazil, 27 August – 1 September 1995, pp 3–40.13.

  21. Lindner P. 1903. Atlas der Mikroskopischen Grandlagen der Garungskunde. Verlagsbuchhandlung Paue Parey, Berlin.

    Google Scholar 

  22. Louis EJ, ES Naumova, A Lee, G Naumov and JE Haber. 1994. The chromosome end in yeast: its mosaic nature and influence on recombinational dynamics. Genetics 136: 789–802.

    PubMed  Google Scholar 

  23. Ludwig R. 1910. Beitrage zur Kenntniss der Organismen in Eichenschleimfluss. Inaugural Dissertation at University of Berlin.

  24. Molnár O, R Messner, H Prillinger, U Stahl and E Slavikova. 1995. Genotypic identification ofSaccharomyces species using random amplified polymorphic DNA analysis. Syst Appl Microbiol 18: 136–145.

    Google Scholar 

  25. Mortimer RK, P Romano, G Suzzi and M Polsinelli. 1994. Genome renewal: a new phenomenon revealed from a genetic study of 43 strains ofSaccharomyces cerevisiae derived from natural fermentation of grape must. Yeast 10: 1543–1552.

    PubMed  Google Scholar 

  26. Naumov GI. 1972. Comparative genetics of yeasts I. Complementation of maltose genes in the maltose negative species ofSaccharomyces. Soviet Genetics 5: 1232–1238.

    Google Scholar 

  27. Naumov GI. 1975. Comparative genetics of yeasts XIV. Analysis of wine strains ofSaccharomyces neutral to killer strain of type k2. Soviet Genetics 10: 100–105.

    Google Scholar 

  28. Naumov GI. 1977. Comparative genetics of yeast XVI. Genes for maltose fermentation inSaccharomyces carlsbergensis N.C.Y.C. 74. Soviet Genetics 12: 1374–1386.

    Google Scholar 

  29. Naumov GI. 1980. The biological speciesSaccharomyces terrestris. Dokl Biol Sci 249: 1248–1250.

    Google Scholar 

  30. Naumov GI. 1985. Taxonomic genetics of theSaccharomyces cerevisiae yeasts: fermentation of sugars. In: Main Problems of Genetics of Microorganisms (Naumov GI, VI Kondratieva and ES Naumova, eds), pp 35–44, Nauka, Moscow (in Russian).

    Google Scholar 

  31. Naumov GI. 1986. Genetic differentiation and ecology of the yeastSaccharomyces paradoxus Batschinskaia. Dokl Biol Sci 289–291: 213–216.

    Google Scholar 

  32. Naumov GI. 1986. Comparative genetics of yeast XXIII. Unusual inheritance of toxin formation inSaccharomyces paradoxus Batschinskaia. Soviet Genetics 21: 1406–1410.

    Google Scholar 

  33. Naumov GI. 1987. Genetic basis for classification and identification of the ascomycetous yeasts. Stud Mycol 30: 469–475.

    Google Scholar 

  34. Naumov GI. 1988. A hybridological study of the yeastSaccharomyces from the expedition collection of VI Kudriavzev (during 1934 and 1936). Mikol Fitopatol 22: 296–301 (in Russian).

    Google Scholar 

  35. Naumov GI. 1989. Differentiation of the gene pool of culturedSaccharomyces yeasts: eight groups of cultivars.Dokl Biol Sci 306: 336–338.

    Google Scholar 

  36. Naumov GI. 1989. Occurrence ofSaccharomyces paradoxus in Estonia. Eesti NSV Tead Akad Toim Biol 38: 9–12 (in Russian).

    Google Scholar 

  37. Naumov GI and NK Gudkova. 1979. Comparative genetics of yeast XVIII. Microevolution ofSaccharomyces bayanus. Soviet Genetics 15: 380–387.

    Google Scholar 

  38. Naumov GI and NK Gudkova. 1979. Regressive evolution ofSaccharomyces. Dokl Biol Sci 245: 791–793.

    Google Scholar 

  39. Naumov GI, VI Kondratieva and ES Naumova. 1986. Methods for hybridization of homothallic yeast diplonts and haplonts. Soviet Biotechnol 6: 29–32.

    Google Scholar 

  40. Naumov GI, VI Kondratieva, TI Naumova and NK Gudkova. 1983. Genetic bases for classification ofSaccharomyces cerevisiae. A study of survival of hybrid ascospores. Zh Obs Biol 44: 648–660 (in Russian).

    Google Scholar 

  41. Naumov GI and ES Naumova. 1990.Saccharomyces douglasii: a synonym ofS. paradoxus as defined by hybridization analysis. Dokl Biol Sci 311: 208–209.

    Google Scholar 

  42. Naumov GI and ES Naumova. 1991. A wild yeast population ofSaccharomyces cerevisiae found in Siberia. Microbiology (Moscow) 60: 137–140.

    Google Scholar 

  43. Naumov GI, ES Naumova, ZM Azbukina, M Korhola and C Gaillardin. 1993. Genetic and karyotypic identification ofSaccharomyces yeasts from Far East Asia. Cryptogamie Mycol 14: 85–93.

    Google Scholar 

  44. Naumov GI, ES Naumova, AN Hagler, LC Mendonça-Hagler and EJ Louis. 1995. A new genetically isolated population of theSaccharomyces sensu stricto complex from Brazil. Antonie von Leeuwenhoek 67: 351–355.

    Google Scholar 

  45. Naumov G, E Naumova and C Gaillardin. 1993. Genetic and karyotypic identification of wineSaccharomyces bayanus yeasts isolated in France and Italy. Syst Appl Microbiol 16: 274–279.

    Google Scholar 

  46. Naumov GI, ES Naumova, C Gaillardin, H Turakainen and M Korhola. 1994. Identification of new chromosomes ofSaccharomyces bayanus using gene probes fromS. cerevisiae. Hereditas 120: 121–126.

    PubMed  Google Scholar 

  47. Naumov G, E Naumova and M Korhola. 1992. Genetic identification of naturalSaccharomyces sensu stricto yeasts from Finland, Holland and Slovakia. Antonie van Leeuwenhoek 61: 237–243.

    PubMed  Google Scholar 

  48. Naumov GI, ES Naumova and MP Korhola. 1995. Chromosomal polymorphism ofMEL genes in some populations ofSaccharomyces cerevisiae. FEMS Microbiol Lett 127: 41–45.

    PubMed  Google Scholar 

  49. Naumov GI, ES Naumova, RA Lantto, EJ Louis and M Korhola. 1992. Genetic homology betweenSaccharomyces cerevisiae and its sibling speciesS. paradoxus andS. bayanus: electrophoretic karyotypes. Yeast 8: 599–612.

    PubMed  Google Scholar 

  50. Naumov GI, ES Naumova and EJ Louis. 1995. Two new genetically isolated populations of theSaccharomyces sensu stricto complex from Japan.J Gen Appl Microbiol 41: 499–505.

    Google Scholar 

  51. Naumov GI, ES Naumova and EJ Louis. 1995. Genetic mapping of the α-galactosidaseMEL gene family on right and left telomeres ofSaccharomyces cerevisiae. Yeast 11: 481–483.

    PubMed  Google Scholar 

  52. Naumov GI, ES Naumova and CA Michels. 1994. Genetic variation of the repeatedMAL loci in natural populations ofSaccharomyces cerevisiae andSaccharomyces paradoxus. Genetics 136: 803–812.

    PubMed  Google Scholar 

  53. Naumov GI, ES Naumova and ED Sancho. 1994. Sibling species of theSaccharomyces sensu stricto complex in Spain. Microbiologia SEM 10: 403–412.

    Google Scholar 

  54. Naumov GI, ES Naumova and ED Sancho. 1996. Genetic reidentification ofSaccharomyces strains associated with black knot disease of trees in Ontario andDrosophila species in California. Can J Microbiol 42: 335–339.

    Google Scholar 

  55. Naumov GI, ES Naumova, ED Sancho and M Korhola. 1993. Taxogenetics of theSaccharomyces sensu stricto yeasts from Western and South Africa. Cryptogamie Mycol 14: 263–270.

    Google Scholar 

  56. Naumov GI, ES Naumova, ED Sancho and MP Korhola. 1996. PolymericSUC genes in natural populations ofSaccharomyces cerevisiae. FEMS Microbiol Lett 135: 31–35.

    PubMed  Google Scholar 

  57. Naumov GI, ES Naumova, H Turakainen and M Korhola. 1996. Identification of the α-galactosidaseMEL genes in some populations ofSaccharomyces cerevisiae: a new geneMEL11. Genet Res Camb 67: 101–108.

    Google Scholar 

  58. Naumov G, E Naumova, H Turakainen, P Suominen and M Korhola. 1991. Polymeric genesMEL8, MEL9 andMEL10—new members of α-galactosidase gene family inSaccharomyces cerevisiae. Curr Genet 20: 269–276.

    PubMed  Google Scholar 

  59. Naumov GI and TI Naumova. 1978. Comparative genetics of yeast XVII. A new type of killer strain inSaccharomyces yeast. Soviet Genetics 14: 98–103.

    Google Scholar 

  60. Naumov GI and TA Nikonenko. 1987. Genomic divergence in cultivated and wild yeasts of theSaccharomyces sensu stricto: four twin species. Dokl Biol Sci 294: 330–332.

    Google Scholar 

  61. Naumov GI and TA Nikonenko. 1988. The East Asia is a probable native land of the cultured yeastsSaccharomyces cerevisiae. Izv Sibirsk Otd Akad Nauk SSSR, Ser Biol Nauk 20: 97–101 (in Russian).

    Google Scholar 

  62. Naumov GI and TA Nikonenko. 1988. New isolates ofSaccharomyces paradoxus from oak exudates. Biol Nauki (Moscow) 7: 84–87 (in Russian).

    Google Scholar 

  63. Naumov GI and TA Nikonenko. 1989. Occurrence and physiological characteristics of biological speciesSaccharomyces bayanus from hybridological analysis. Microbiology (Moscow) 57: 526–530.

    Google Scholar 

  64. Naumov GI and II Tolstorukov. 1974. Comparative genetics of yeast X. Reidentification of mutators of mating types inSaccharomyces. Soviet Genetics 9: 57–63.

    PubMed  Google Scholar 

  65. Naumov G, H Turakainen, E Naumova, S Aho and M Korhola. 1990. A new family of polymorphic genes inSaccharomyces cerevisiae: α-galactosidase genesMEL1-MEL7. Mol Gen Genet 224: 119–128.

    PubMed  Google Scholar 

  66. Naumov GI and VV Yurkevich. 1970. Variability of biochemical properties used in yeast taxonomy of the genusSaccharomyces. Advances of Modern Biology 70: 315–324 (in Russian).

    Google Scholar 

  67. Naumova ES, GI Naumov, CA Michels and DR Beritashvili. 1991. Identification of chromosomal DNA patterns of the speciesSaccharomyces bayanus andS. pastorianus. Dokl Biol Sci 316: 744–746.

    Google Scholar 

  68. Naumova E, G Naumov and A Panek. 1994. Polymorphism of trehalose accumulation in sibling species ofSaccharomyces sensu stricto. Revista Braesiliera de Genetika 17: 133–138.

    Google Scholar 

  69. Naumova ES, TV Chernookova, TK Skorikova, VI Kondratieva, NI Bur'yan and GI Naumov. 1993. Selection of champagne yeast strains on the basis of interspecific hybridization ofSaccharomyces cerevisiae x S. bayanus. Russian Biotechnology 7: 8–13.

    Google Scholar 

  70. Naumova TI and GI Naumov. 1975. Comparative genetics of yeast XII. Study of antagonistic relations of yeast of the genusSaccharomyces. Soviet Genetics 9: 469–473.

    Google Scholar 

  71. Nilsson-Tillgren T, MC Kieland-Brandt, S Holmberg, JGL Petersen and TC Gjermansen. 1983. Is larger yeast a species hybrid? Utilization of intrinsic genetic variation in breeding. In: Genetics of Industrial Microorganisms (Ikeda Y and T Beppu, eds), pp 143–147, Kodanska Ltd, Tokyo.

    Google Scholar 

  72. Oshima Y. 1993. Homothallism, mating-type switching, and the controlling element model inSaccharomyces cerevisiae. In: The Early Days of Yeast Genetics (Hall MN and P Linder, eds), pp 291–304, CSHL Press.

  73. Ouchi K, H Saito and Y Ikeda. 1970. Genetic relatedness of yeast strains studied by the DNA-DNA hybridization method. Agr Biol Chem 34: 95–101.

    Google Scholar 

  74. Perkins DD, BC Turner and EG Barry. 1979. Strains ofNeurospora collected from nature. Evolution 30: 281–313.

    Google Scholar 

  75. Petersen RH. 1995. There's more to a mushroom than meets the eye: mating studies in theAgaricales. Mycologia 87: 1–17.

    Google Scholar 

  76. Price CW, GB Fuson and HJ Phaff. 1978. Genome comparison in yeast systematics: delimitation of species within the generaSchwanyomyces, Saccharomyces, Debaryomyces andPichia. Microbiol Rev 42: 161–193.

    PubMed  Google Scholar 

  77. Rodrigues de Sousa H, A Madeira-Lopes and I Spencer-Martins. 1995. The significance of active fructose transport and maximum temperature for growth in the taxonomy ofSaccharomyces sensu stricto. Syst Appl Microbiol 18: 44–51.

    Google Scholar 

  78. Rosini G, F Federici, AE Vaughan and A Martini. 1982. Systematics of the species of the yeast genusSaccharomyces associated with the fermentation industry. Eur J Appl Microbiol Biotechnol 15: 188–193.

    Google Scholar 

  79. Santa Maria J and D Vidal. 1973. Genetic control of ‘flor’ formation bySaccharomyces. J Bacteriol 113: 1078–1080.

    PubMed  Google Scholar 

  80. Vaughan Martini A. 1989.Saccharomyces paradoxus comb nov, a newly separated species of theSaccharomyces sensu stricto complex based upon nDNA/nDNA homologies. Syst Appl Microbiol 12: 179–182.

    Google Scholar 

  81. Vaughan Martini A and CP Kurtzman. 1985. Deoxyribonucleic acid relatedness among species of the genusSaccharomyces sensu stricto. Int J Syst Bacteriol 35: 508–511.

    Google Scholar 

  82. Vaughan Martini A and A Martini. 1987. Three newly delimited species ofSaccharomyces sensu stricto. Antonie van Leeuwenhoek 53: 77–84.

    PubMed  Google Scholar 

  83. Vezinhet F, B Blondin and J-N Hallet. 1990. Chromosomal DNA patterns and mitochondrial DNA polymorphism as tools for identification of enological strains ofSaccharomyces cerevisiae. Appl Microbiol Biotechnol 32: 568–571.

    Google Scholar 

  84. Walt van der JP. 1970. The genusSaccharomyces emend Reess. In: The Yeasts. A Taxonomic Study, 2nd edn (Lodder J, ed), pp 575–718, North-Holland Publishing, Amsterdam.

    Google Scholar 

  85. Winge Ö and O Laustsen. 1939. On 14 new yeast types, produced by hybridization. Compt Rend Trav Lab Carlsberg Ser Physiol 22: 337–352.

    Google Scholar 

  86. Winge Ö and C Roberts. 1952. The relation between the polymeric genes for maltose, raffinose, and sucrose fermentation in yeast. Compt Rend Trav Lab Carlsberg Ser Physiol 25: 141–171.

    Google Scholar 

  87. Winge Ö and C Roberts. 1958. Yeast genetics. In: The Chemistry and Biology of Yeasts (Cook AH, ed), pp 123–156, Academic Press, New York.

    Google Scholar 

  88. Yamada Y, K Mikata and I Banno. 1993. Reidentification of 121 strains of the genusSaccharomyces. Bull JFCC 9: 95–119 (in Japanese).

    Google Scholar 

  89. Zambonelli C, P Passarelli, S Rainieri and P Guidici. 1993. Taxonomic and technological implications of sterility in hybrids from cryotolerant and non-cryotolerantSaccharomyces strains. Ann Microbiol Enzymol 43: 217–223.

    Google Scholar 

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This paper is dedicated to Danish scientists Ö Winge and V Jensen in recognition of their contributions to zymology.

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Naumov, G. Genetic identification of biological species in theSaccharomyces sensu stricto complex. Journal of Industrial Microbiology & Biotechnology 17, 295–302 (1996). https://doi.org/10.1007/BF01574704

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