Biogeography and Ecology of the Genus Saccharomyces

  • José Paulo SampaioEmail author
  • Paula Gonçalves


The genus Saccharomyces is intimately associated with alcoholic fermentations conducted by humans. Its most emblematic species, Saccharomyces cerevisiae, represents not only an important case of microbe domestication, exemplified by products such as wine, beer, and bread, but also a case of complex and yet poorly understood ecological adaptations and interactions in natural systems. Moreover, the long coexistence with humans in wineries and breweries has fostered anthropocentric concepts that are difficult to eradicate. Here we critically review, using a historical perspective, recent findings on the natural ecology and biogeography of the different species that form the genus Saccharomyces.


Saccharomyces Ecology Biogeography Population genomics Microbe domestication 



This work was supported by FCT Portugal grant UID/Multi/04378/2013. We thank Feng-Yan Bai, Qing-Ming Wang, and Polona Zalar for sharing unpublished data.


  1. Almeida P, Gonçalves C, Teixeira S, Libkind D, Bontrager M, Masneuf-Pomarède I, Albertin W, Durrens P, Sherman DJ, Marullo P, Todd Hittinger C, Gonçalves P, Sampaio JP (2014) A Gondwanan imprint on global diversity and domestication of wine and cider yeast Saccharomyces uvarum. Nat Commun 5:4044PubMedPubMedCentralGoogle Scholar
  2. Almeida P, Barbosa R, Zalar P, Imanishi Y, Shimizu K, Turchetti B, Legras J-L, Serra M, Dequin S, Couloux A, Guy J, Bensasson D, Gonçalves P, Sampaio JP (2015) A population genomics insight into the Mediterranean origins of wine yeast domestication. Mol Ecol 24:5412–5427CrossRefPubMedGoogle Scholar
  3. Bachinskaya AA (1914) Storiya razvitiya i kyl’tury novago drozhzhevogo griboka – Saccharomyces paradoxus. (Development and cultivation of a new yeast – Saccharomyces paradoxus). I Zhurnal Mikrobiol 1:231–250Google Scholar
  4. Barbosa R, Almeida P, Safar SVB, Santos RO, Morais PB, Nielly-Thibault L, Leducq J-B, Landry CR, Gonçalves P, Rosa CA, Sampaio JP (2016) Evidence of natural hybridization in Brazilian wild lineages of Saccharomyces cerevisiae. Genome Biol Evol 8:317–329CrossRefPubMedPubMedCentralGoogle Scholar
  5. Bing J, Han PJ, Liu WQ, Wang QM, Bai FY (2014) Evidence for a Far East Asian origin of lager beer yeast. Curr Biol 24:R380–R381CrossRefPubMedGoogle Scholar
  6. Blackwell M (2017) Yeast in insects and other invertebrates. In: Buzzini P, Lachance MA, Yurkov AM (eds) Yeasts in natural ecosystems: diversity. Springer International Publishing, pp 397–433Google Scholar
  7. Bond U (2009) Chapter 6: The genomes of lager yeasts. Adv Appl Microbiol 69:159–182CrossRefPubMedGoogle Scholar
  8. Borneman AR, Pretorius IS (2015) Genomic insights into the Saccharomyces sensu stricto complex. Genetics 199:281–291Google Scholar
  9. Borneman AR, Desany BA, Riches D, Affourtit JP, Forgan AH, Pretorius IS, Egholm M, Chambers PJ (2012) The genome sequence of the wine yeast VIN7 reveals an allotriploid hybrid genome with Saccharomyces cerevisiae and Saccharomyces kudriavzevii origins. FEMS Yeast Res 12:88–96CrossRefPubMedGoogle Scholar
  10. Borneman AR, Schmidt SA, Pretorius IS (2013) At the cutting-edge of grape and wine biotechnology. Trends Genet 29:263–271CrossRefPubMedGoogle Scholar
  11. Borneman AR, Forgan AH, Kolouchova R, Fraser JA, Schmidt SA (2016) Whole genome comparison reveals high levels of inbreeding and strain redundancy across the spectrum of commercial wine strains of Saccharomyces cerevisiae. G3 (Bethesda) 6:957–971CrossRefGoogle Scholar
  12. Boynton PJ, Greig D (2014) The ecology and evolution of non-domesticated Saccharomyces species. Yeast 31:449–462PubMedPubMedCentralGoogle Scholar
  13. Boynton PJ, Stelkens R, Kowallik V, Greig D (2017) Measuring microbial fitness in a field reciprocal transplant experiment. Mol Ecol Resour (in press)Google Scholar
  14. Buser CC, Newcomb RD, Gaskett AC, Goddard MR (2014) Niche construction initiates the evolution of mutualistic interactions. Ecol Lett 17:1257–1264CrossRefPubMedGoogle Scholar
  15. Charron G, Leducq JB, Bertin C, Dublé AK, Landry CR (2014) Exploring the northern limit of the distribution of Saccharomyces cerevisiae and Saccharomyces paradoxus in North America. FEMS Yeast Res 14:281–288CrossRefPubMedGoogle Scholar
  16. Christiaens JF, Franco LM, Cools TL, de Meester L, Michiels J, Wenseleers T, Hassan BA, Yaksi E, Verstrepen KJ (2014) The fungal aroma gene ATF1 promotes dispersal of yeast cells through insect vectors. Cell Rep 9:425–432CrossRefPubMedGoogle Scholar
  17. Cliften P, Sudarsanam P, Desikan A, Fulton L, Fulton B, Majors J, Waterston R, Cohen BA, Johnston M (2003) Finding functional features in Saccharomyces genomes by phylogenetic footprinting. Science 301:71–76CrossRefPubMedGoogle Scholar
  18. Cromie GA, Hyma KE, Ludlow CL, Garmendia-Torres C, Gilbert TL, May P, Huang AA, Dudley AM, Fay JC (2013) Genomic sequence diversity and population structure of Saccharomyces cerevisiae assessed by RAD-seq. G3 (Bethesda) 3:2163–2171CrossRefGoogle Scholar
  19. Cubillos FA, Billi E, Zörgö E, Parts L, Fargier P, Omholt S, Blomberg A, Warringer J, Louis EJ, Liti G (2011) Assessing the complex architecture of polygenic traits in diverged yeast populations. Mol Ecol 20:1401–1413CrossRefPubMedGoogle Scholar
  20. da Cunha AB, Shehata AME-T, de Oliveira W (1957) A study of the diets and nutritional preferences of tropical species of Drosophila. Ecology 38:98–106CrossRefGoogle Scholar
  21. Dunn B, Sherlock G (2008) Reconstruction of the genome origins and evolution of the hybrid lager yeast Saccharomyces pastorianus. Genome Res 18:1610–1623CrossRefPubMedPubMedCentralGoogle Scholar
  22. Fay JC, Benavides JA (2005) Evidence for domesticated and wild populations of Saccharomyces cerevisiae. PLoS Genet 1:e5CrossRefPubMedCentralGoogle Scholar
  23. Gallone B, Steensels J, Prahl T, Soriaga L, Saels V, Herrera-Malaver B, Merlevede A, Roncoroni M, Voordeckers K, Miraglia L, Teiling C, Steffy B, Taylor M, Schwartz A, Richardson T, White C, Baele G, Maere S, Verstrepen KJ (2016) Domestication and divergence of Saccharomyces cerevisiae beer yeasts. Cell 166:1397–1410CrossRefPubMedPubMedCentralGoogle Scholar
  24. Garcia DM, Dietrich D, Clardy J, Jarosz DF (2016) A common bacterial metabolite elicits prion-based bypass of glucose repression. Elife 5:e17978CrossRefPubMedPubMedCentralGoogle Scholar
  25. Gayevskiy V, Goddard MR (2016) Saccharomyces eubayanus and Saccharomyces arboricola reside in North Island native New Zealand forests. Environ Microbiol 18:1137–1147CrossRefPubMedGoogle Scholar
  26. Goddard MR, Greig D (2015) Saccharomyces cerevisiae: a nomadic yeast with no niche? FEMS Yeast Res 15:fov009Google Scholar
  27. Gonçalves P, Valério E, Correia C, de Almeida JMGCF, Sampaio JP (2011) Evidence for divergent evolution of growth temperature preference in sympatric Saccharomyces species. PLoS One 6:e20739CrossRefPubMedPubMedCentralGoogle Scholar
  28. Gonçalves M, Pontes A, Almeida P, Barbosa R, Serra M, Libkind D, Hutzler M, Gonçalves P, Sampaio JP (2016) Distinct domestication trajectories in top-fermenting beer yeasts and wine yeasts. Curr Biol 26:2750–2761CrossRefPubMedGoogle Scholar
  29. González SS, Barrio E, Gafner J, Querol A (2006) Natural hybrids from Saccharomyces cerevisiae, Saccharomyces bayanus and Saccharomyces kudriavzevii in wine fermentations. FEMS Yeast Res 6:1221–1234CrossRefPubMedGoogle Scholar
  30. González SS, Barrio E, Querol A (2008) Molecular characterization of new natural hybrids of Saccharomyces cerevisiae and S. kudriavzevii in brewing. Appl Environ Microbiol 74:2314–2320CrossRefPubMedPubMedCentralGoogle Scholar
  31. Hanson SJ, Byrne KP, Wolfe KH (2014) Mating-type switching by chromosomal inversion in methylotrophic yeasts suggests an origin for the three-locus Saccharomyces cerevisiae system. Proc Natl Acad Sci U S A 111:E4851–E4858CrossRefPubMedPubMedCentralGoogle Scholar
  32. Hittinger CT, Gonçalves P, Sampaio JP, Dover J, Johnston M, Rokas A (2010) Remarkably ancient balanced polymorphisms in a multi-locus gene network. Nature 464:54–58CrossRefPubMedPubMedCentralGoogle Scholar
  33. Hoang D, Kopp A, Chandler JA (2015) Interactions between Drosophila and its natural yeast symbionts—Is Saccharomyces cerevisiae a good model for studying the fly-yeast relationship? Peer J 3:e1116CrossRefPubMedPubMedCentralGoogle Scholar
  34. Jarosz DF, Brown JCS, Walker GA, Datta MS, Ung WL, Lancaster AK, Rotem A, Chang A, Newby GA, Weitz DA, Bisson LF, Lindquist S (2014a) Cross-kingdom chemical communication drives a heritable, mutually beneficial prion-based transformation of metabolism. Cell 158:1083–1093CrossRefPubMedPubMedCentralGoogle Scholar
  35. Jarosz DF, Lancaster AK, Brown JCS, Lindquist S (2014b) An evolutionarily conserved prion-like element converts wild fungi from metabolic specialists to generalists. Cell 158:1072–1082CrossRefPubMedPubMedCentralGoogle Scholar
  36. Kellis M, Patterson N, Endrizzi M, Birren B, Lander ES (2003) Sequencing and comparison of yeast species to identify genes and regulatory elements. Nature 423:241–254CrossRefPubMedGoogle Scholar
  37. Kowallik V, Greig D (2016) A systematic forest survey showing an association of Saccharomyces paradoxus with oak leaf litter. Environ Microbiol Rep 8:833–841CrossRefGoogle Scholar
  38. Kuehne HA, Murphy HA, Francis CA, Sniegowski PD (2007) Allopatric divergence, secondary contact, and genetic isolation in wild yeast populations. Curr Biol 17:407–411CrossRefPubMedGoogle Scholar
  39. Landry CR, Townsend JP, Hartl DL, Cavalieri D (2006) Ecological and evolutionary genomics of Saccharomyces cerevisiae. Mol Ecol 15:575–591CrossRefPubMedGoogle Scholar
  40. Leducq J-B, Charron G, Samani P, Dubé AK, Sylvester K, James B, Almeida P, Sampaio JP, Hittinger CT, Bell G, Landry CR (2014) Local climatic adaptation in a widespread microorganism. Proc R Soc B Biol Sci 281:20132472CrossRefGoogle Scholar
  41. Leducq J-B, Nielly-Thibault L, Charron G, Eberlein C, Verta J-P, Samani P, Sylvester K, Hittinger CT, Bell G, Landry CR (2016) Speciation driven by hybridization and chromosomal plasticity in a wild yeast. Nat Microbiol 1:15003CrossRefPubMedGoogle Scholar
  42. Legras JL, Merdinoglu D, Cornuet JM, Karst F (2007) Bread, beer and wine: Saccharomyces cerevisiae diversity reflects human history. Mol Ecol 16:2091–2102CrossRefPubMedGoogle Scholar
  43. Legras J-L, Erny C, Charpentier C (2014) Population structure and comparative genome hybridization of European flor yeast reveal a unique group of Saccharomyces cerevisiae strains with few gene duplications in their genome. PLoS One 9:e108089CrossRefPubMedPubMedCentralGoogle Scholar
  44. Li R-Q, Chen Z-D, Lu A-M, Soltis DE, Soltis PS, Manos PS (2004) Phylogenetic relationships in Fagales based on DNA sequences from three genomes. Int J Plant Sci 165:311–324CrossRefGoogle Scholar
  45. Libkind D, Hittinger CT, Valeŕio E, Gonçalves C, Dover J, Johnston M, Gonçalves P, Sampaio JP (2011) Microbe domestication and the identification of the wild genetic stock of lager-brewing yeast. Proc Natl Acad Sci U S A 108:14539–14544CrossRefPubMedPubMedCentralGoogle Scholar
  46. Liti G, Barton DBH, Louis EJ (2006) Sequence diversity, reproductive isolation and species concepts in Saccharomyces. Genetics 174:839–850CrossRefPubMedPubMedCentralGoogle Scholar
  47. Liti G, Carter DM, Moses AM, Warringer J, Parts L, James SA, Davey RP, Roberts IN, Burt A, Koufopanou V, Tsai IJ, Bergman CM, Bensasson D, O’Kelly MJT, van Oudenaarden A, Barton DBH, Bailes E, Nguyen AN, Jones M, Quail MA, Goodhead I, Sims S, Smith F, Blomberg A, Durbin R, Louis EJ (2009) Population genomics of domestic and wild yeasts. Nature 458:337–341CrossRefPubMedPubMedCentralGoogle Scholar
  48. Lopes CA, Barrio E, Querol A (2010) Natural hybrids of S. cerevisiae × S. kudriavzevii share alleles with European wild populations of Saccharomyces kudriavzevii. FEMS Yeast Res 10:412–421CrossRefPubMedGoogle Scholar
  49. Ludlow CL, Cromie GA, Garmendia-Torres C, Sirr A, Hays M, Field C, Jeffery EW, Fay JC, Dudley AM (2016) Independent origins of yeast associated with coffee and cacao fermentation. Curr Biol 26:965–971CrossRefPubMedPubMedCentralGoogle Scholar
  50. Marsit S, Dequin S (2015) Diversity and adaptive evolution of Saccharomyces wine yeast: a review. FEMS Yeast Res 15:fov067Google Scholar
  51. Martini AV (1989) Saccharomyces paradoxus comb. nov., a newly separated species of the Saccharomyces sensu stricto complex based upon nDNA/nDNA homologies. Syst Appl Microbiol 12:179–182Google Scholar
  52. Martini A (1993) Origin and domestication of the wine yeast Saccharomyces cerevisiae. J Wine Res 4:165–176CrossRefGoogle Scholar
  53. Montrocher R, Verner M-C, Briolay J, Gautier C, Marmeisse R (1998) Phylogenetic analysis of the Saccharomyces cerevisiae group based on polymorphisms of the rDNA spacer sequences. Int J Syst Bacteriol 48:295–303CrossRefPubMedGoogle Scholar
  54. Nakao Y, Kanamori T, Itoh T, Kodama Y, Rainieri S, Nakamura N, Shimonaga T, Hattori M, Ashikari T (2009) Genome sequence of the lager brewing yeast, an interspecies hybrid. DNA Res 16:115–129CrossRefPubMedPubMedCentralGoogle Scholar
  55. Naumov G, Naumova E, Korhola M (1992) Genetic identification of natural Saccharomyces sensu stricto yeasts from Finland, Holland and Slovakia. A van Leeuwenhoek 61:237–243Google Scholar
  56. Naumov GI, James SA, Naumova ES, Louis EJ, Roberts IN (2000) Three new species in the Saccharomyces sensu stricto complex: Saccharomyces cariocanus, Saccharomyces kudriavzevii and Saccharomyces mikatae. Int J Syst Evol Microbiol 50:1931–1942Google Scholar
  57. Naumov GI, Lee C-F, Naumova ES (2013) Molecular genetic diversity of the Saccharomyces yeasts in Taiwan: Saccharomyces arboricola, Saccharomyces cerevisiae and Saccharomyces kudriavzevii. A van Leeuwenhoek 103:217–228CrossRefGoogle Scholar
  58. Novo M, Bigey F, Beyne E, Galeote V, Gavory F, Mallet S, Cambon B, Legras J-L, Wincker P, Casaregola S, Dequin S (2009) Eukaryote-to-eukaryote gene transfer events revealed by the genome sequence of the wine yeast Saccharomyces cerevisiae EC1118. Proc Natl Acad Sci U S A 106:16333–16338CrossRefPubMedCentralGoogle Scholar
  59. Pérez-Ortín JE, Querol A, Puig S, Barrio E (2002) Molecular characterization of a chromosomal rearrangement involved in the adaptive evolution of yeast strains. Genome Res 12:1533–1539CrossRefPubMedPubMedCentralGoogle Scholar
  60. Peris D, Sylvester K, Libkind D, Gonçalves P, Sampaio JP, Alexander WG, Hittinger CT (2014) Population structure and reticulate evolution of Saccharomyces eubayanus and its lager-brewing hybrids. Mol Ecol 23:2031–2045CrossRefPubMedGoogle Scholar
  61. Peris D, Langdon QK, Moriarty RV, Sylvester K, Bontrager M, Charron G, Leducq J-B, Landry CR, Libkind D, Hittinger CT (2016) Complex ancestries of lager-brewing hybrids were shaped by standing variation in the wild yeast Saccharomyces eubayanus. PLoS Genet 12:e1006155CrossRefPubMedPubMedCentralGoogle Scholar
  62. Phaff HJ, Miller MW, Recca JA, Shifrine M, Mrak EM (1956) Yeasts found in the alimentary canal of Drosophila. Ecology 37:533–538CrossRefGoogle Scholar
  63. Piškur J, Rozpedowska E, Polakova S, Merico A, Compagno C (2006) How did Saccharomyces evolve to become a good brewer? Trends Genet 22:183–186CrossRefPubMedGoogle Scholar
  64. Pretorius IS (2000) Tailoring wine yeast for the new millennium: novel approaches to the ancient art of winemaking. Yeast 16:675–729CrossRefPubMedGoogle Scholar
  65. Robinson HA, Pinharanda A, Bensasson D (2016) Summer temperature can predict the distribution of wild yeast populations. Ecol Evol 6:1236–1250CrossRefPubMedPubMedCentralGoogle Scholar
  66. Rodríguez ME, Pérez-Través L, Sangorrín MP, Barrio E, Lopes CA (2014) Saccharomyces eubayanus and Saccharomyces uvarum associated with the fermentation of Araucaria araucana seeds in Patagonia. FEMS Yeast Res 14:948–965CrossRefPubMedGoogle Scholar
  67. Salvadó Z, Arroyo-López FN, Guillamón JM, Salazar G, Querol A, Barrio E (2011) Temperature adaptation markedly determines evolution within the genus Saccharomyces. Appl Environ Microbiol 77:2292–2302CrossRefPubMedPubMedCentralGoogle Scholar
  68. Sampaio JP, Gonçalves P (2008) Natural populations of Saccharomyces kudriavzevii in Portugal are associated with oak bark and are sympatric with S. cerevisiae and S. paradoxus. Appl Environ Microbiol 74:2144–2152CrossRefPubMedPubMedCentralGoogle Scholar
  69. Schacherer J, Shapiro J, Ruderfer DM, Kruglyak L (2009) Comprehensive polymorphism survey elucidates population structure of Saccharomyces cerevisiae. Nature 458:342–345CrossRefPubMedPubMedCentralGoogle Scholar
  70. Stefanini I, Dapporto L, Legras J-L, Calabretta A, Di Paola M, De Filippo C, Viola R, Capretti P, Polsinelli M, Turillazzi S, Cavalieri D (2012) Role of social wasps in Saccharomyces cerevisiae ecology and evolution. Proc Natl Acad Sci U S A 109:13398–13403CrossRefPubMedPubMedCentralGoogle Scholar
  71. Stefanini I, Dapporto L, Berná L, Polsinelli M, Turillazzi S, Cavalieri D (2016) Social wasps are a Saccharomyces mating nest. Proc Natl Acad Sci U S A 113:2247–2251CrossRefPubMedPubMedCentralGoogle Scholar
  72. Strope PK, Skelly DA, Kozmin SG, Mahadevan G, Stone EA, Magwene PM, Dietrich FS, McCusker JH (2015) The 100-genomes strains, an S. cerevisiae resource that illuminates its natural phenotypic and genotypic variation and emergence as an opportunistic pathogen. Genome Res 125:762–774CrossRefGoogle Scholar
  73. Török T, Mortimer R, Romano P, Suzzi G, Polsinelli M (1996) Quest for wine yeasts—An old story revisited. J Ind Microbiol Biotechnol 17:303–313CrossRefGoogle Scholar
  74. Turakainen H, Kristo P, Korhola M (1994) Consideration of the evolution of the Saccharomyces cerevisiae MEL gene family on the basis of the nucleotide sequences of the genes and their flanking regions. Yeast 10:1559–1568CrossRefPubMedGoogle Scholar
  75. van der Walt JP (1970) Saccharomyces (Meyen) emend. Reess. In: Lodder J (ed) The yeasts, a taxonomic study, 2nd edn. North-Holland, Amsterdam, pp 555–718Google Scholar
  76. Vaughan-Martini A, Kurtzman CP (1985) Deoxyribonucleic acid relatedness among species of the genus Saccharomyces sensu stricto. Int J Syst Bacteriol 35:508–511Google Scholar
  77. Vaughan-Martini A, Martini A (1995) Facts, myths and legends on the prime industrial microorganism. J Ind Microbiol 14:514–522CrossRefPubMedGoogle Scholar
  78. Wang S-A, Bai F-Y (2008) Saccharomyces arboricolus sp. nov., a yeast species from tree bark. Int J Syst Evol Microbiol 58:510–514CrossRefPubMedGoogle Scholar
  79. Wang Q-M, Liu W-Q, Liti G, Wang S-A, Bai F-Y (2012) Surprisingly diverged populations of Saccharomyces cerevisiae in natural environments remote from human activity. Mol Ecol 21:5404–5417CrossRefPubMedGoogle Scholar
  80. Warringer J, Zörgö E, Cubillos FA, Zia A, Gjuvsland A, Simpson JT, Forsmark A, Durbin R, Omholt SW, Louis EJ, Liti G, Moses A, Blomberg A (2011) Trait variation in yeast is defined by population history. PLoS Genet 7:e1002111CrossRefPubMedPubMedCentralGoogle Scholar
  81. Wiens F, Zitzmann A, Lachance M-A, Yegles M, Pragst F, Wurst FM, von Holst D, Guan SL, Spanagel R (2008) Chronic intake of fermented floral nectar by wild treeshrews. Proc Natl Acad Sci U S A 105:10426–10431CrossRefPubMedPubMedCentralGoogle Scholar
  82. Will JL, Kim HS, Clarke J, Painter JC, Fay JC, Gasch AP (2010) Incipient balancing selection through adaptive loss of aquaporins in natural Saccharomyces cerevisiae populations. PLoS Genet 6:e1000893CrossRefPubMedPubMedCentralGoogle Scholar
  83. Yarrow D (1984) Saccharomyces Meyen ex Reess. In: Kreger-van Rij N (ed) The yeasts, a taxonomic study, 3rd edn. Elsevier, Amsterdam, pp 379–395Google Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  1. 1.UCIBIO-REQUIMTE, Departamento de Ciências da Vida, Faculdade de Ciências e TecnologiaUniversidade Nova de LisboaCaparicaPortugal

Personalised recommendations