Genetically Isolated Population of Saccharomyces bayanus in New Zealand and Australia

Cover Page

Cite item

Full Text

Open Access Open Access
Restricted Access Access granted
Restricted Access Subscription Access

Abstract

The genetic relatedness of yeasts in the Saccharomyces bayanus complex has been studied using the methods of molecular and classical genetics. A divergent population of S. bayanus has been found in New Zealand and Australia. The S. bayanus complex includes four genetic populations: S. bayanus var. bayanus, S. bayanus var. uvarum, S. eubayanus and New Zealand population. The strains of the New Zealand population differ significantly in the nucleotide sequences of nuclear (FSY1, HIS3, MET2) and mitochondrial (FUN14, COX2) genes and form semi-sterile hybrids with other populations: viability of ascospores is 6.2–23.3%. There is no complete interspecific postzygotic isolation between S. bayanus var. bayanus, S. bayanus var. uvarum, S. eubayanus, and New Zealand populations: all hybrids showed regular meiotic segregation of control auxotrophic markers. According to the results obtained, four genetic populations belong to the same biological species with genomic divergence at the level of taxonomic varieties.

About the authors

A. N. Borovkova

National Research Center “Kurchatov Institute”, Kurchatov Complex
for Genetic Research (GosNIIgenetika); Moscow State University

Email: lena_naumova@yahoo.com
Russia, 123098, Moscow; Russia, 119234, Moscow

G. I. Naumov

National Research Center “Kurchatov Institute”, Kurchatov Complex
for Genetic Research (GosNIIgenetika)

Email: lena_naumova@yahoo.com
Russia, 123098, Moscow

A. V. Shnyreva

Moscow State University

Email: lena_naumova@yahoo.com
Russia, 119234, Moscow

E. S. Naumova

National Research Center “Kurchatov Institute”, Kurchatov Complex
for Genetic Research (GosNIIgenetika)

Author for correspondence.
Email: lena_naumova@yahoo.com
Russia, 123098, Moscow

References

  1. Наумов Г.И., Наумова Е.С., Мартыненко Н.Н., Маснёф-Помаред И. Таксономия, экология и генетика дрожжей Saccharomyces bayanus – нового объекта в науке и практике // Микробиология. 2011. Т. 80. № 6. С. 723–730.
  2. Vaughan-Martini A., Martini A. Saccharomyces Meyen ex Reess (1870) // The Yeast, a Taxonomic Study / Eds Kurtzman C.P., Fell J.W., Boekhout T. 5th ed. Amsterdam: Elsevier, 2011. V. 2. P. 733–746. https://doi.org/10.1016/B978-0-444-52149-1.00061-6
  3. Naumov G.I., James S.A., Naumova E.S. et al. Three new species in the Saccharomyces sensu stricto complex: Saccharomyces cariocanus, Saccharomyces kudriavzevii and Saccharomyces mikatae // Int. J. Syst. Evol. Microbiol. 2000. V. 50. P. 1931–1942. https://doi.org/10.1099/00207713-50-5-1931
  4. Kurtzman C.P. Phylogenetic circumscription of Saccharomyces, Kluyveromyces and other members of the Saccharomycetaceae, and the proposal of the new genera Lachancea, Nakaseomyces, Naumovia, Vandervatozyma and Zygotorulaspora // FEMS Yeast Res. 2003. V. 4. P. 233–245. https://doi.org/10.1016/S1567-1356(03)00175-2
  5. Wang S.A., Bai F.Y. Saccharomyces arboricolus sp. nov., a yeast species from tree bark // Int. J. Syst. Evol. Microbiol. 2008. V. 58. P. 510–514. https://doi.org/10.1099/ijs.0.65331-0
  6. Naseeb S., James S.A., Alsammar H. et al. Saccharomyces jurei sp. nov., isolation and genetic identification of a novel yeast species from Quercus robur // Int. J. Syst. Evol. Microbiol. 2017. V. 67. P. 2046–2052. https://doi.org/10.1099/ijsem.0.002013
  7. Naumova E.S., Naumov G.I., Masneuf-Pomarede I. et al. Molecular genetic study of introgression between Saccharomyces bayanus and S. cerevisiae // Yeast. 2005. V. 22. P. 1099–1115. https://doi.org/10.1002/yea.1298
  8. Peris D., Pérez-Torrado R., Hittinger C.T. et al. On the origins and industrial applications of Saccharomyces cerevisiae × Saccharomyces kudriavzevii hybrids // Yeast. 2018. V. 35. P. 51–69. Epub 2017 Dec 6https://doi.org/10.1002/yea.3283
  9. Morard M., Benavent-Gil Y., Ortiz-Tovar G. et al. Genome structure reveals the diversity of mating mechanisms in Saccharomyces cerevisiae × Saccharomyces kudriavzevii hybrids, and the genomic instability that promotes phenotypic diversity // Microbial. Genomics. 2020. V. 6(3). P. e000333. https://doi.org/10.1099/mgen.0.000333
  10. Lopandic K. Saccharomyces interspecies hybrids as model organisms for studying yeast adaptation to stressful environments // Yeast. 2018. V. 35. P. 21–38. https://doi.org/10.1002/yea.3294
  11. Bendixsen D.P., Frazão J.G., Stelkens R. Saccharomyces yeast hybrids on the rise // Yeast. 2022. V. 39. P. 40–54. https://doi.org/10.1002/yea.3684
  12. Nguyen H.-V., Gaillardin C. Two subgroups within the Saccharomyces bayanus species evidenced by PCR amplification and restriction polymorphism of the non-transcribed spacer 2 in the ribosomal DNA unit // Syst. Appl. Microbiol. 1997. V. 20. P. 286–294. https://doi.org/10.1016/S0723-2020(97)80075-6
  13. Pérez-Través L., Lopes C.A., Querol A., Barrio E. On the complexity of the Saccharomyces bayanus taxon: Hybridization and potential hybrid speciation // PLoS One. 2014. V. 9(4). P. e93729. https://doi.org/10.1371/journal.pone.0093729
  14. Наумов Г.И. Новая разновидность S. bayanus var. uvarum, установленная генетическим анализом // Микробиология. 2000. Т. 69. № 2. С. 410–414.
  15. Naumov G.I., Naumova E.S., Gaillardin C. Genetic and karyotypic identification of wine Saccharomyces bayanus yeasts isolated in France and Italy // Syst. Appl. Microbiol. 1993. V. 16. P. 274–279. https://doi.org/10.1016/S0723-2020(11)80480-7
  16. Naumov G.I., Masneuf I., Naumova E.S. et al. Association of S. bayanus var. uvarum with some French wines: Genetic analysis of yeast populations // Res. Microbiol. 2000. V. 151. P. 683–691. https://doi.org/10.1016/S0923-2508(00)90131-1
  17. Naumov G.I., Naumova E.S., Aigle M. et al. Genetic reidentification of the pectinolytic yeast strain SCPP as Saccharomyces bayanus var. uvarum // Appl. Microbiol. Biotechnol. 2001. V. 55. P. 108–111. https://doi.org/10.1007/s002530000480
  18. Naumov G.I., Nguyen H.-V., Naumova E.S. et al. Genetic identification of Saccharomyces bayanus var. uvarum, a cider-fermenting yeast // Int. J. Food. Microbiol. 2001. V. 65. P. 163–171. https://doi.org/10.1016/S0168-1605(00)00515-8
  19. Masneuf-Pomarede I., Le Jeune C., Durrens P. et al. Molecular typing of wine yeast strains Saccharomyces bayanus var. uvarum using microsatellite markers // System. Appl. Microbiol. 2007. V. 30. P. 75–82. https://doi.org/10.1016/j.syapm.2006.02.006
  20. Almeida P., Gonçalves C., Teixeira S. et al. A gondwanan imprint on global diversity and domestication of wine and cider yeast Saccharomyces uvarum // Nat. Commun. 2014. V. 5. P. 4044–4055. https://doi.org/10.1038/ncomms5044
  21. Zhang H., Richards K.D., Wilson S. et al. Genetic characterization of strains of Saccharomyces uvarum from New Zealand wineries // Food Microbiol. 2015. V. 46. P. 92–99. https://doi.org/10.1016/j.fm.2014.07.016
  22. Rodríguez M.E., Pérez-Través L., Sangorrín M.P. et al. Saccharomyces uvarum is responsible for the traditional fermentation of apple chicha in Patagonia // FEMS Yeast Res. 2017. V. 17(1). P. fow109. https://doi.org/10.1093/femsyr/fow109
  23. McCarthy G.C., Morgan S.C., Martiniuk J.T. et al. An indigenous Saccharomyces uvarum population with high genetic diversity dominates uninoculated Chardonnay fermentations at a Canadian winery // PLoS One. 2021. V. 16(2). P. e0225615. https://doi.org/10.1371/journal.pone.0225615
  24. Libkind D., Hittinger C.T., Valério E. et al. Microbe domestication and the identification of the wild genetic stock of lager-brewing yeast // Proc. Natl Acad. Sci. USA. 2011. V. 108. P. 14539–14544. https://doi.org/10.1073/pnas.1105430108
  25. Pulvirenti A., Nguyen H.V., Caggia C. et al. Saccharomyces uvarum, a proper species within Saccharomyces sensu stricto // FEMS Microbiol. Lett. 2000. V. 192. P. 191–196. https://doi.org/10.1111/j.1574-6968.2000.tb09381.x
  26. Nguyen H.V., Gaillardin C. Evolutionary relationships between the former species Saccharomyces uvarum and the hybrids Saccharomyces bayanus and Saccharomyces pastorianus; reinstatement of Saccharomyces uvarum (Beijerinck) as a distinct species // FEMS Yeast Res. 2005. V. 5. P. 471–483. https://doi.org/10.1016/j.femsyr.2004.12.004
  27. Rainieri S., Kodama Y., Kaneko Y. et al. Pure and mixed genetic lines of Saccharomyces bayanus and Saccharomyces pastorianus and their contribution to the lager brewing strain genome // Appl. Environ. Microbiol. 2006. V. 72. P. 3968–3974. https://doi.org/10.1128/AEM.02769-05
  28. Nguyen H.-V., Lepingle A., Gaillardin C. Molecular typing demonstrates homogeneity of Saccharomyces uvarum strains and reveals the existence of hybrids between S. uvarum and S. cerevisiae, including the S. bayanus type strain CBS 380 // System. Appl. Microbiol. 2000. V. 23. P. 71–85. https://doi.org/10.1016/S0723-2020(00)80048-X
  29. Rainieri S., Zambonelli C., Hallsworth J.E. et al. Saccharomyces uvarum, a distinct group within Saccharomyces sensu stricto // FEMS Microbiol. Lett. 1999. V. 177. P. 177–185. https://doi.org/10.1111/j.1574-6968.1999.tb13729.x
  30. Bon E., Neuvéglise C., Casaregola S. et al. Genomic exploration of the hemiascomycetous yeasts: 5. Saccharomyces bayanus var. uvarum // FEBS Lett. 2000. V. 487. P. 37–41. https://doi.org/10.1016/s0014-5793(00)02276-6
  31. Nguyen H.-V., Legras J.L., Neuvéglise C., Gaillardin C. Deciphering the hybridisation history leading to the Lager lineage based on the mosaic genomes of Saccharomyces bayanus strains NBRC 1948 and CBS 380 // PLoS One. 2011. V. 6(10). P. e25821. https://doi.org/10.1371/journal.pone.0025821
  32. Bing J., Han P.J., Liu W.Q. et al. Evidence for a Far East Asian origin of lager beer yeast // Curr. Biol. 2014. V. 24. P. 380–381. https://doi.org/10.1016/j.cub.2014.04.031
  33. Peris D., Langdon Q.K., Moriarty R.V. et al. Complex ancestries of lager-brewing hybrids were shaped by standing variation in the wild yeast Saccharomyces eubayanus // PLoS Genet. 2016. V. 12. P. 1–20. https://doi.org/10.1371/journal.pgen.1006155
  34. Gayevskiy V., Goddard M.R. Saccharomyces eubayanus and Saccharomyces arboricola reside in North Island native New Zealand forests // Environ. Microbiol. 2016. V. 18. P. 1137–1147. https://doi.org/10.1111/1462-2920.13107
  35. Nespolo R.F., Villarroel C.A., Oporto C.I. et al. An out-of-patagonia migration explains the worldwide diversity and distribution of Saccharomyces eubayanus lineages // PLoS Genetics. 2020. V. 16(5). e1008777. https://doi.org/10.1371/journal.pgen.1008777
  36. Baker E., Wang B., Bellora N. et al. The genome sequence of Saccharomyces eubayanus and the domestication of Lager-brewing yeasts // Mol. Biol. Evol. 2015. V. 32(11). P. 2818–2831. https://doi.org/10.1093/molbev/msv168
  37. Hebly M., Brickwedde A., Bolat I. et al. S. cerevisiae × × S. eubayanus interspecific hybrid, the best of both worlds and beyond // FEMS Yeast Res. 2015. V. 15. № 3. P. fov005.https://doi.org/10.1093/femsyr/fov005
  38. Наумов Г.И. Генетическое родство и биологический статус индустриально важных дрожжей Saccharomyces eubayanus Sampaio et al. // ДАН. 2017. V. 473(5). P. 622–625. https://doi.org/10.7868/S0869565217110263
  39. Sampaio J.P. Microbe Profile: Saccharomyces eubayanus, the missing link to lager beer yeasts // Microbiology. 2018. V. 164. P. 1069–1071. https://doi.org/10.1099/mic.0.000677
  40. Lõoke M., Kristjuhan K., Kristjuhan A. Extraction of genomic DNA from yeasts for PCR based applications // Biotechniques. 2011. V. 50. P. 325–328. https://doi.org/10.2144/000113672
  41. Kumar S., Stecher G., Tamura K. MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets // Mol. Biol. Evol. 2016. V. 33. № 7. P. 1870–1874. https://doi.org/10.1093/molbev/msw054
  42. Boek J., La Croute D., Fink G.R. A positive selection for mutants lacking orotidine-5'-phosphate decarboxilase activity // Mol. Gen. Genet. 1984. V. 197. P. 345–346.
  43. Sherman F., Fink G.R., Hicks J.B. Laboratory course manual for methods in yeasts genetics // Methods in Yeast Genetics: A Gold Spring Harbor Laboratory Course Manual. N.Y.: Gold Spring Harbor Lab., 1986. P. 50–51.
  44. Fischer G., James S.A., Roberts I.N. et al. Chromosomal evolution in Saccharomyces // Nature. 2000. V. 405. P. 451–454.
  45. Kaneko Y., Banno I. Isolation and genetic characterization of auxotrophic mutants in Saccharomyces bayanus // IFO Res. Comm. 1989. V. 14. P. 104–110.
  46. Наумов Г.И., Газдиев Д.О., Наумова Е.С. Обнаружение биологического вида Saccharomyces bayanus в Дальневосточной Азии // Микробиология. 2003. Т. 72. № 6. С. 834–839.

Supplementary files

Supplementary Files
Action
1. JATS XML
2.

Download (570KB)
3.

Download (161KB)
4.

Download (105KB)
5.

Download (484KB)
6.

Download (299KB)

Copyright (c) 2023 А.Н. Боровкова, Г.И. Наумов, А.В. Шнырева, Е.С. Наумова