Revisiting the Taxonomic Synonyms and Populations of Saccharomyces cerevisiae—Phylogeny, Phenotypes, Ecology and Domestication
Abstract
:1. Introduction
2. Materials and Methods
2.1. Genome Sequencing, Read Alignment and Genotype Calling
2.2. Phylogenetic Analyses and Survey of Specific Genes
2.3. Phenotypic Analyses
3. Results
3.1. Global Phylogenetic Analysis Reveals an Unequal Distribution of Type Strains of Former Species
3.2. The Wine and Olives Clades Harbor Most Type Strains of Former Species
3.3. The Beer and Bread Clades Contain Multiple Type Strains of Former Species
3.4. Additional Clades Harboring Type Strains of Former Species
3.5. The Biogeography and Ecology of Wild Populations
3.6. Lifestyle Drives the Fate of Aquaporins
3.7. The Natural Reservoirs of RTM1 and BIO1/BIO6
3.8. The Complex Distribution of MEL Alleles
4. Discussion
Supplementary Materials
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
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Original Name | Strain Number# | Strain Number (Other Collections) | Strain Status | Population | Substrate of Isolation | Locality of Isolation |
---|---|---|---|---|---|---|
Saccharomyces aceti Santa María 1958 | CBS 4054 | – | type strain | WINE-PDM | red wine | Spain |
Saccharomyces annulatus Negroni 1929 | PYCC 6727 | CBS 1227 | type strain | WINE-MAIN | abscess on epididymis | New Zealand |
Saccharomyces boulardii Seguela, Bastide & Massot 1984 (invalid name) | YJS 5879 | - | type strain | WINE-MAIN | lychee | Vietnam |
Saccharomyces brasiliensis Lindner 1909; Saccharomyces logos van Laer ex Jörgenssen 1909 | PYCC 4602 | CBS 382 | type strain | BEER 2- DIASTATICUS | beer (Logos brewery) | Rio de Janeiro, Brazil |
Saccharomyces capensis van der Walt & Tscheuschner 1956 | CBS 2247 | - | type strain | WINE-PDM | grape must | South Africa |
Saccharomyces cerevisiae Meyen ex Hansen 1883 | PYCC 4455 | CBS 1171 | neotype strain | BEER 1 | brewer’s top yeast | Oranjeboom brewery, Rotterdam, Netherlands |
Saccharomyces cerevisiae Hansen var. onychophilus Zach 1934 | CBS 1464 | - | type strain | BREAD | nail of 4-year-old girl | Austria |
Saccharomyces cerevisiae Hansen var. orsati Steiner 1924 | CBS 1175 | - | type strain | WINE-MAIN | wine | unknown |
Saccharomyces chevalieri Guilliermond 1914 | PYCC 8489 | NRRL Y-12,633; CBS 400 | type strain | WEST AFRICA | palm wine from Elaeis guineensis | Ivory Coast |
Saccharomyces chodati Steiner 1924 | CBS 423 | - | type strain | WINE-MAIN | wine | Switzerland |
Saccharomyces cordubensis Santa María 1970 | CBS 6007 | - | type strain | WINE-PDM | wine | Spain |
Saccharomyces coreanus Saito 1910 | CBS 5635 | - | neotype strain | WINE-MAIN | grape must | South Africa |
Saccharomyces diastaticus Andrews & Gilliland ex van der Walt 1965 | PYCC 2608 | CBS 1782 | type strain | BEER 2-DIASTATICUS | super-attenuated beer | unknown |
Saccharomyces carlsbergensis Hansen var. mandschuricus (Saito) Stelling-Dekker 1931 | CBS 1508 | - | type strain | SAKE | starter for sorghum brandy | unknown |
Saccharomyces ellipsoideus Reess 1870 | PYCC 4653 | CBS 1395; NRRL Y-1529 | neotype strain | WINE—MAIN | unknown | unknown |
Saccharomyces ellipsoideus Hansen var. umbra Castelli 1933 | CBS 457 | - | type strain | WINE—MAIN | grape must | Italy |
Saccharomyces ellipsoideus Hansen var. alpinus Steiner 1924 | CBS 1192 | - | type strain | WINE—MAIN | wine | unknown |
Saccharomyces ellipsoideus Hansen var. montibensis Steiner 1924 | CBS 1479 | - | type strain | WINE—MAIN | wine | unknown |
Saccharomyces ellipsoideus Hansen ssp. thermophilus Steiner 1924 | CBS 1194 | - | type strain | WINE—MAIN | wine | unknown |
Saccharomyces fructuum Lodder & Kreger-van Rij 1952 | PYCC 4654 | CBS 1544 | type strain | OUTLIER | fermenting fruit juice | Netherlands |
Saccharomyces elongatus Krumbholz 1932 | CBS 439 | - | type strain | WINE—MAIN | Silvaner grapes | Germany |
Saccharomyces formosensis Nakazawa 1933 | CBS 440 | - | type strain | SAKE | molasses | Taiwan |
Saccharomyces gaditensis Santa María 1970 | CBS 6006 | - | type strain | WINE—PDM | wine | Spain |
Saccharomyces hienipiensis Santa María 1962 | PYCC 6733 | VKM Y-1235 | type strain | OLIVES | alpechin | Spain |
Saccharomyces hispalensis Santa María 1978 | PYCC 8023 | CBS 7002 | type strain | OLIVES | alpechin | Seville, Spain |
Saccharomyces hispanica Santa María 1968 | CBS 5835 | - | type strain | WINE-PDM | wine | Spain |
Saccharomyces ilicis Grönlund 1893 | CBS 1173 | - | type strain | OUTLIER | fruit of Ilex aquifolium | unknown |
Saccharomyces italicus Castelli 1939 | CBS 459 | - | type strain | WINE—MAIN | grape must | Italy |
Saccharomyces italicus var. melibiosi van Uden & Assis-Lopes 1957 | PYCC 2613 | CBS 2909 | type strain | OLIVES | feces of man | Portugal |
Saccharomyces lindneri Guilliermond 1914 | CBS 403 | PYCC 4571 | type strain | WEST AFRICA | ginger beer from Zinziber officinale | West Africa |
Saccharomyces mangini var. casei Saccchetti 1933 | PYCC 6721 | CBS 420; VKM Y-482 | type strain | DAIRY | stracchino cheese | Italy |
Saccharomyces marchalianus Kufferath 1920 | PYCC 8196 | CBS 1460 | type strain | WINE—MAIN | fermenting fruit | Indonesia |
Saccharomyces multisporus Jörgensen 1909 | CBS 4507 | - | type strain | WINE—MAIN | English top brewing yeast | unknown |
Population | Designation in Other Studies | Life Style (W-Wild; D-Domesticated; F-Feral) | Number of Type Strains of Former Saccharomyces Species | Comments |
---|---|---|---|---|
1–Wine-main | Wine [25]; Wine/European [6,9] | D | 17 | Global distribution probably associated with the widespread dissemination of winemaking |
2–Olives | Alpechin [9]; Olives [26,27] | D | 6 | Ancestral hybrids with S. paradoxus associated with processed olives |
3–Wine-PDM | Flor [25,28]; Georgian [9]; PDM-Prise de Mousse [12]; | D | 6 | Lalvin EC1118, a well-known commercial strain in this group is also known as “Prise de mousse” or Champagne strain [20,28]. This population also contains the Spanish flor yeasts of Xerez wine (Sherry) and similar wines [28] |
4–Cachaça-Bioethanol | Brazilian bioethanol [9]; Cachaça C1 and C2 [29]; Rum and bioethanol [25] | D | – | This group is a secondary domesticate derived from wine strains and includes two types of cachaça strains (C1 and C2) and bioethanol strains [29] |
5–Beer 2-Diastaticus | Beer 2 [30]; Mosaic beer [9] | D | 6 | Contains Saison-type low-gravity beer strains and beer-spoilage strains with diastase activity |
6–African beer | African beer [9] | D | – | Includes strains that ferment malted millet to produce bantu beer or malted sorghum to produce bili-bili or kaffir beer |
7–Wild Brazil 3-French Guiana–Mexican agave | Mexican agave, French Guiana human [9]; Wild Brazil B3 [31] | W/D | – | Complex clade composed of three subclades, one containing wild strains found in Brazil, another containing strains used in artisanal mezcal fermentation in Mexico and a third one containing gut-associated strains from French Guiana aborigines; this last group contains STA1 and was also found in cachiri, a traditional beer made from chewed and fermented starch-rich manioc [32] |
8–Mediterranean oak | - | W | – | Unique wild population with no evident links to the core group of Asian wild populations; no changes in designation since the original description [8] |
9–Dairy | Cheese [25]; French dairy [9]; Milk [33] | D | 1 | Recently revealed population associated with dairy products and adapted to galactose utilization |
10–Bread | Active dry yeast [33]; Mixed [30] | D | 2 | |
11–Beer 1 | Ale beer [9]; Beer [25]; Beer 1 [30] | D | 1 | Various sub-populations associated with different ale-beer types |
12–Chinese fermentations (bread and beverages) | Mantou (bread)/Baijiu (distilled)/Huangjiu (rice wine)/Qingkejiu (barley wine)/fermented milk [33] | D | – | Predominantly Chinese domesticated strains that are distinct from strains of the Sake clade |
13–Cocoa | West African cocoa [9] | D | – | |
14–China VIII | - | F | – | Found in the arboreal niche in China, but with several domestication signatures (MAL gene expansion, AQY inactivation, presence of region B) |
15–Sake | Asia [27,30]; Asian fermentation, Sake [6,9] | D | 3 | |
16–Philippines | Asian islands [9]; Philippines [27] | W/D | – | |
17–North America–Japan-Far East Russia–China VI-VII | China VI-VII [33,34]; Far East Russia [9]; North American [6] | W | – | A wild Chinese population also found in North America, Japan and Russia |
18–China VI-VII | - | W | – | No changes in designation since the original description [34] |
19–West Africa | African palm wine [9]; West Africa [6]; | D | 2 | |
20–Wild Brazil 1–China V | Ecuadorean [9]; Wild Brazil B1 [31] | W | – | A wild Chinese population also found in Brazil and Ecuador |
21–China I | - | W | – | No changes in designation since the original description [34] |
22–Malaysia | - | W | – | No changes in designation since the original description [6] |
23–China III | - | W | – | No changes in designation since the original description [34] |
24–China IV | - | W | – | No changes in designation since the original description [34] |
25–China I | - | W | – | No changes in designation since the original description [34] |
26–China IX | - | W | – | No changes in designation since the original description [34] |
27–China II | - | W | – | No changes in designation since the original description [34] |
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Pontes, A.; Hutzler, M.; Brito, P.H.; Sampaio, J.P. Revisiting the Taxonomic Synonyms and Populations of Saccharomyces cerevisiae—Phylogeny, Phenotypes, Ecology and Domestication. Microorganisms 2020, 8, 903. https://doi.org/10.3390/microorganisms8060903
Pontes A, Hutzler M, Brito PH, Sampaio JP. Revisiting the Taxonomic Synonyms and Populations of Saccharomyces cerevisiae—Phylogeny, Phenotypes, Ecology and Domestication. Microorganisms. 2020; 8(6):903. https://doi.org/10.3390/microorganisms8060903
Chicago/Turabian StylePontes, Ana, Mathias Hutzler, Patrícia H. Brito, and José Paulo Sampaio. 2020. "Revisiting the Taxonomic Synonyms and Populations of Saccharomyces cerevisiae—Phylogeny, Phenotypes, Ecology and Domestication" Microorganisms 8, no. 6: 903. https://doi.org/10.3390/microorganisms8060903
APA StylePontes, A., Hutzler, M., Brito, P. H., & Sampaio, J. P. (2020). Revisiting the Taxonomic Synonyms and Populations of Saccharomyces cerevisiae—Phylogeny, Phenotypes, Ecology and Domestication. Microorganisms, 8(6), 903. https://doi.org/10.3390/microorganisms8060903