Folia Microbiologica

, Volume 63, Issue 2, pp 217–227 | Cite as

Four Saccharomyces species differ in their tolerance to various stresses though they have similar basic physiological parameters

  • Jana Zemančíková
  • Marie Kodedová
  • Klára Papoušková
  • Hana Sychrová
Original Article
First Online:
Received:
Accepted:

Abstract

Saccharomyces species, which are mostly used in the food and beverage industries, are known to differ in their fermentation efficiency and tolerance of adverse fermentation conditions. However, the basis of their difference has not been fully elucidated, although their genomes have been sequenced and analyzed. Five strains of four Saccharomyces species (S. cerevisiae, S. kudriavzevii, S. bayanus, and S. paradoxus), when grown in parallel in laboratory conditions, exhibit very similar basic physiological parameters such as membrane potential, intracellular pH, and the degree to which they are able to quickly activate their Pma1 H+-ATPase upon glucose addition. On the other hand, they differ in their ability to proliferate in media with a very low concentration of potassium, in their osmotolerance and tolerance to toxic cations and cationic drugs in a growth-medium specific manner, and in their capacity to survive anhydrobiosis. Overall, S. cerevisiae (T73 more than FL100) and S. paradoxus are the most robust, and S. kudriavzevii the most sensitive species. Our results suggest that the difference in stress survival is based on their ability to quickly accommodate their cell size and metabolism to changing environmental conditions and to adjust their portfolio of available detoxifying transporters.

Keywords

Saccharomyces Stress tolerance Intracellular pH Membrane potential 
This is a preview of subscription content, log in to check access.

Notes

Acknowledgements

The authors wish to thank Dr. A. Querol and Prof. F. Lacroute for the strains and Dr. O. Zimmermannova for critical reading of the manuscript.

Funding

This work was supported by the Czech National Science Foundation (grant number GA CR 15-03708S) and the European Union (grant number FP7-ITN-264717 Cornucopia).

Supplementary material

12223_2017_559_MOESM1_ESM.tif (823 kb)
Fig. S1 Cell diameter. The size of exponentially growing cells in YPD, YPD supplemented with 1 mol/L KCl and YNB was estimated and the intervals containing the most typical 60% of the cell populations are shown as a grey box. The mean diameter is represented by a line inside the box. Average results are shown ± SD. Asterisk indicates a significant difference in cell size between YPD and YNB media and upon transfer into media supplemented with 1 mol/L KCl (* P < 0.05, ** P < 0.01, *** P < 0.001). Sc, S. cerevisiae; Sk, S. kudriavzevii; Sb, S. bayanus; Sp, S. paradoxus. (TIFF 823 kb)
12223_2017_559_Fig7_ESM.gif (19 kb)

High resolution image (GIF 19 kb)

12223_2017_559_MOESM2_ESM.tif (3.1 mb)
Fig. S2 Use of various carbon sources. Growth on solid YNB media supplemented with indicated carbon sources. Sc, S. cerevisiae; Sk, S. kudriavzevii; Sb, S. bayanus; Sp, S. paradoxus. (TIFF 3172 kb)
12223_2017_559_Fig8_ESM.gif (64 kb)

High resolution image (GIF 64 kb)

References

  1. Arino J, Ramos J, Sychrova H (2010) Alkali metal cation transport and homeostasis in yeasts. Microbiol Mol Biol Rev 74:95–120CrossRefPubMedPubMedCentralGoogle Scholar
  2. Barreto L et al (2011) A genomewide screen for tolerance to cationic drugs reveals genes important for potassium homeostasis in Saccharomyces cerevisiae. Eukaryot Cell 10:1241–1250CrossRefPubMedPubMedCentralGoogle Scholar
  3. Beker MJ, Rapoport AI (1987) Conservation of yeasts by dehydration. In:Scheper Th, Belkin S, Bley Th, Bohlmann J, Gu M.B, Hu W.-S, Mattiasson B, Nielsen J, Seitz H, Ulber R, Zeng A.-P, Zhong J.-J, Zhou W (eds) Advances in Biochemical Engineering / Biotechnology, vol 35. Springer Verlag Berlin Heidelberg NewYork London Paris Tokyo, pp 127–171Google Scholar
  4. Belloch C, Orlic S, Barrio E, Querol A (2008) Fermentative stress adaptation of hybrids within the Saccharomyces sensu stricto complex. Int J Food Microbiol 122:188–195CrossRefPubMedGoogle Scholar
  5. Borovikova D, Herynkova P, Rapoport A, Sychrova H (2014) Potassium uptake system Trk2 is crucial for yeast cell viability during anhydrobiosis. FEMS Microbiol Lett 350:28–33CrossRefPubMedGoogle Scholar
  6. Bubnova M, Zemancikova J, Sychrova H (2014) Osmotolerant yeast species differ in basic physiological parameters and in tolerance of non-osmotic stresses. Yeast 31:309–321CrossRefPubMedGoogle Scholar
  7. Cadek R, Chladkova K, Sigler K, Gaskova D (2004) Impact of the growth phase on the activity of multidrug resistance pumps and membrane potential of S. cerevisiae: effect of pump overproduction and carbon source. Biochim Biophys Acta 1665:111–117CrossRefPubMedGoogle Scholar
  8. Denksteinova B, Gaskova D, Herman P, Vecer J, Malinsky J, Plasek J, Sigler K (1997) Monitoring of membrane potential changes in Saccharomyces cerevisiae by diS-C3(3) fluorescence. Folia Microbiol (Praha) 42:221–224CrossRefGoogle Scholar
  9. Dupont S, Rapoport A, Gervais P, Beney L (2014) Survival kit of Saccharomyces Cerevisiae for anhydrobiosis. Appl Microbiol Biot 98:8821–8834CrossRefGoogle Scholar
  10. Duskova M, Ferreira C, Lucas C, Sychrova H (2015) Two glycerol uptake systems contribute to the high osmotolerance of Zygosaccharomyces rouxii. Mol Microbiol 97:541–559.  https://doi.org/10.1111/mmi.13048 CrossRefPubMedGoogle Scholar
  11. Eleutherio E, Panek A, De Mesquita JF, Trevisol E, Magalhaes R (2015) Revisiting yeast trehalose metabolism. Curr Genet 61:263–274CrossRefPubMedGoogle Scholar
  12. Espindola AD, Gomes DS, Panek AD, Eleutherio ECA (2003) The role of glutathione in yeast dehydration tolerance. Cryobiology 47:236–241CrossRefGoogle Scholar
  13. Felcmanova K, Neveceralova P, Sychrova H, Zimmermannova OP (2017) Yeast Kch1 and Kch2 membrane proteins play apleiotropic role in membrane potential establishmentand monovalent cation homeostasis regulation FEMS. Yeast Res 17:fox053CrossRefGoogle Scholar
  14. Gamero A, Tronchoni J, Querol A, Belloch C (2013) Production of aroma compounds by cryotolerant Saccharomyces species and hybrids at low and moderate fermentation temperatures. J Appl Microbiol 114:1405–1414.  https://doi.org/10.1111/jam.12126 CrossRefPubMedGoogle Scholar
  15. Garciadeblas B, Rubio F, Quintero FJ, Banuelos MA, Haro R, Rodriguez-Navarro A (1993) Differential expression of two genes encoding isoforms of the ATPase involved in sodium efflux in Saccharomyces Cerevisiae. Mol Gen Genet 236:363–368CrossRefPubMedGoogle Scholar
  16. Gaskova D et al (1998) Fluorescent probing of membrane potential in walled cells: diS-C-3(3) assay in Saccharomyces Cerevisiae. Yeast 14:1189–1197CrossRefPubMedGoogle Scholar
  17. Hendrych T, Kodedova M, Sigler K, Gakova D (2009) Characterization of the kinetics and mechanisms of inhibition of drugs interacting with the S. cerevisiae multidrug resistance pumps Pdr5p and Snq2p. Biochim Biophys Acta 1788:717–723CrossRefPubMedGoogle Scholar
  18. Hohmann S (2002) Osmotic stress signaling and osmoadaptation in yeasts. Microbiol Mol Biol Rev 66:300–372CrossRefPubMedPubMedCentralGoogle Scholar
  19. Jordan P, Choe JY, Boles E, Oreb M (2016) Hxt13, Hxt15, Hxt16 and Hxt17 from Saccharomyces cerevisiae represent a novel type of polyol transporters. Sci Rep 6:23502.  https://doi.org/10.1038/srep23502srep23502 CrossRefPubMedPubMedCentralGoogle Scholar
  20. Kodedova M, Sychrova H (2015) Changes in the sterol composition of the plasma membrane affect membrane potential, salt tolerance and the activity of multidrug resistance pumps in Saccharomyces cerevisiae. PLoS One 10:e0139306.  https://doi.org/10.1371/journal.pone.0139306PONE-D-15-28879 CrossRefPubMedPubMedCentralGoogle Scholar
  21. Kurtzman CP, Fell JW, Boekhout T (2010) The yeasts, a taxonomic study, 5th Edition edn. Elsevier, AmsterdamGoogle Scholar
  22. Llopis-Torregrosa V, Husekova B, Sychrova H (2016) Potassium uptake mediated by Trk1 is crucial for Candida glabrata growth and fitness. Plos One 11:DOI: https://doi.org/10.1371/journal.pone.0153374
  23. Malac J, Urbankova E, Sigler K, Gaskova D (2005) Activity of yeast multidrug resistance pumps during growth is controlled by carbon source and the composition of growth-depleted medium: DiS-C-3(3) fluorescence assay. Int J Biochem Cell Biol 37:2536–2543CrossRefPubMedGoogle Scholar
  24. Maresova L, Sychrova H (2007) Applications of a microplate reader in yeast physiology research. BioTechniques 43:667–672CrossRefPubMedGoogle Scholar
  25. Maresova L, Hoskova B, Urbankova E, Chaloupka R, Sychrova H (2010) New applications of pHluorin-measuring intracellular pH of prototrophic yeasts and determining changes in the buffering capacity of strains with affected potassium homeostasis. Yeast 27:317–325PubMedGoogle Scholar
  26. Miesenbock G, De Angelis DA, Rothman JE (1998) Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins. Nature 394:192–195CrossRefPubMedGoogle Scholar
  27. Navarette C et al (2010) Lack of main K+ uptake systems in Saccharomyces cerevisiae cells affects yeast performance both in potassium sufficient and limiting conditions. FEMS Yeast Res 10:508–517Google Scholar
  28. Oliveira BM, Barrio E, Querol A, Perez-Torrado R (2014) Enhanced enzymatic activity of glycerol-3-phosphate dehydrogenase from the cryophilic Saccharomyces kudriavzevii. PLoS One 9:doi. https://doi.org/10.1371/journal.pone.0087290
  29. Orij R, Postmus J, Ter Beek A, Brul S, Smits GJ (2009) In vivo measurement of cytosolic and mitochondrial pH using a pH-sensitive GFP derivative in Saccharomyces cerevisiae reveals a relation between intracellular pH and growth. Microbiology-(UK) 155:268–278CrossRefGoogle Scholar
  30. Orij R, Brul S, Smits GJ (2011) Intracellular pH is a tightly controlled signal in yeast. Biochim Biophys Acta 1810:933–944CrossRefPubMedGoogle Scholar
  31. Perez-Torrado R, Oliveira BM, Zemancikova J, Sychrova H, Querol A (2016) Alternative glycerol balance strategies among Saccharomyces species in response to winemaking stress. Front Microbiol 7:DOI:  https://doi.org/10.3389/fmicb.2016.00435
  32. Petrezselyova S, Kinclova-Zimmermannova O, Sychrova H (2013) Vhc1, a novel transporter belonging to the family of electroneutral cation-Cl(-) cotransporters, participates in the regulation of cation content and morphology of Saccharomyces cerevisiae vacuoles. Biochim Biophys Acta 1828:623–631CrossRefPubMedGoogle Scholar
  33. Pribylova L, Farkas V, Slaninova I, de Montigny J, Sychrova H (2007) Differences in osmotolerant and cell-wall properties of two Zygosaccharomyces rouxii strains. Folia Microbiol (Praha) 52:241–245CrossRefGoogle Scholar
  34. Ramos J, Arino J, Sychrova H (2011) Alkali-metal-cation influx and efflux systems in nonconventional yeast species. FEMS Microbiol Lett 317:1–8CrossRefPubMedGoogle Scholar
  35. Rapoport A (2017) Anhydrobiosis and dehydration of yeasts. In: Sibyrny A (ed) Biotechnology of Yeasts and Filamentous Fungi. Springer international Publishing, Basel, pp 87–116CrossRefGoogle Scholar
  36. Ruiz A, Arino J (2007) Function and regulation of the Saccharomyces cerevisiae ENA sodium ATPase system Eukaryot. Cell 6:2175–2183Google Scholar
  37. Serrano R, Kielland-Brandt MC, Fink GR (1986) Yeast plasma membrane ATPase is essential for growth and has homology with (Na+ + K+), K+- and Ca2+-ATPases. Nature 319:689–693CrossRefPubMedGoogle Scholar
  38. Stribny J, Kinclova-Zimmermannova O, Sychrova H (2012) Potassium supply and homeostasis in the osmotolerant non-conventional yeasts Zygosaccharomyces rouxii differ from Saccharomyces cerevisiae. Curr Genet 58:255–264.  https://doi.org/10.1007/s00294-012-0381-7 CrossRefPubMedGoogle Scholar
  39. Stribny J, Gamero A, Perez-Torrado R, Querol A (2015) Saccharomyces kudriavzevii and Saccharomyces uvarum differ from Saccharomyces cerevisiae during the production of aroma-active higher alcohols and acetate esters using their amino acidic precursors. Int J Food Microbiol 205:41–46.  https://doi.org/10.1016/j.ijfoodmicro.2015.04.003S0168-1605(15)00184-1 CrossRefPubMedGoogle Scholar
  40. Stribny J, Querol A, Perez-Torrado R (2016) Differences in enzymatic properties of theSaccharomyces kudriavzevii and Saccharomyces uvarum alcohol acetyltransferases and their impact on aroma-active compounds production. Front Microbiol 7:897.  https://doi.org/10.3389/fmicb.2016.00897 CrossRefPubMedPubMedCentralGoogle Scholar
  41. Sychrová H, Kotyk A (1985) Conditions of activation of yeast plasma membrane ATPase. FEBS Lett 183:21–24CrossRefPubMedGoogle Scholar
  42. Takagi H (2008) Proline as a stress protectant in yeast: physiological functions, metabolic regulations, and biotechnological applications. Appl Microbiol Biot 81:211–223CrossRefGoogle Scholar
  43. Wieland J, Nitsche AM, Strayle J, Steiner H, Rudolph HK (1995) The PMR2 gene cluster encodes functionally distinct isoforms of a putative Na+ pump in the yeast plasma membrane. EMBO J 14:3870–3882PubMedPubMedCentralGoogle Scholar

Copyright information

© Institute of Microbiology, Academy of Sciences of the Czech Republic, v.v.i. 2017

Authors and Affiliations

  1. 1.Department of Membrane TransportInstitute of Physiology CASPrague 4Czech Republic

Personalised recommendations