Applied Microbiology and Biotechnology

, Volume 96, Issue 2, pp 471–480 | Cite as

Air-drying kinetics affect yeast membrane organization and survival

  • Guillaume Lemetais
  • Sébastien Dupont
  • Laurent Beney
  • Patrick Gervais
Applied microbial and cell physiology

Abstract

The plasma membrane (PM) is a key structure for the survival of cells during dehydration. In this study, we focused on the concomitant changes in survival and in the lateral organization of the PM in yeast strains during desiccation, a natural or technological environmental perturbation that involves transition from a liquid to a solid medium. To evaluate the role of the PM in survival during air-drying, a wild-type yeast strain and an osmotically fragile mutant (erg6Δ) were used. The lateral organization of the PM (microdomain distribution) was observed using a fluorescent marker related to a specific green fluorescent protein-labeled membrane protein (Sur7-GFP) after progressive or rapid desiccation. We also evaluated yeast behavior during a model dehydration experiment performed in liquid medium (osmotic stress). For both strains, we observed similar behavior after osmotic and desiccation stresses. In particular, the same lethal magnitude of dehydration and the same lethal kinetic effect were found for both dehydration methods. Thus, yeast survival after progressive air-drying was related to PM reorganization, suggesting the positive contribution of passive lateral rearrangements of the membrane components. This study also showed that the use of glycerol solutions is an efficient means to simulate air-drying desiccation.

Keywords

Desiccation Osmotic dehydration Cell survival Plasma membrane Yeast 

Notes

Acknowledgments

We are grateful to W. Tanner and G. Grossmann (University of Regensburg, Cell Biology and Plant Physiology, Regensburg, Germany) for providing the plasmid YIp211SUR7GFP. We thank the personnel of the Plateau Technique “Imagerie Spectroscopique” IFR 92 (Université de Bourgogne, Dijon, France). This work was supported by French Ministry of Research, the Regional Council of Burgundy, Merck MF (Dijon, France), and the “FUI Probiotique” program supported by Vitagora (Dijon, France).

References

  1. Abe F, Hiraki T (2009) Mechanistic role of ergosterol in membrane rigidity and cycloheximide resistance in Saccharomyces cerevisiae. Biochim Biophys Acta 1788:743–752CrossRefGoogle Scholar
  2. Anand JC, Brown AD (1968) Growth rate patterns of the so-called osmophilic and non-osmophilic yeasts in solutions of polyethylene glycol. Microbiology 52:205Google Scholar
  3. Beker M, Rapoport A (1987) Conservation of yeasts by dehydration. Adv Biochem Eng Biotechnol 35:127–171Google Scholar
  4. Brown A (1990) Microbial water stress physiology. Principles and perspectives. Wiley, New YorkGoogle Scholar
  5. Chirife J, Fontan CF (1980) A study of the water activity lowering behavior of polyethylene glycols in the intermediate moisture range. J Food Sci 45:1717–1719CrossRefGoogle Scholar
  6. Crowe JH, Crowe LM, Chapman D (1984) Preservation of membranes in anhydrobiotic organisms: the role of trehalose. Science 223:701–703CrossRefGoogle Scholar
  7. Crowe J, Hoekstra F, Crowe L (1989) Membrane phase transitions are responsible for imbibitional damage in dry pollen. Proc Natl Acad Sci U S A 86:520CrossRefGoogle Scholar
  8. Crowe J, Hoekstra F, Crowe L (1992) Anhydrobiosis. Annu Rev Physiol 54:579–599CrossRefGoogle Scholar
  9. Dupont S, Beney L, Ritt JF, Lherminier J, Gervais P (2010) Lateral reorganization of plasma membrane is involved in the yeast resistance to severe dehydration. Biochim Biophys Acta 1798:975–985CrossRefGoogle Scholar
  10. Dupont S, Beney L, Ferreira T, Gervais P (2011) Nature of sterols affects plasma membrane behavior and yeast survival during dehydration. Biochim Biophys Acta 1808:1520–1528CrossRefGoogle Scholar
  11. Estruch F (2000) Stress controlled transcription factors, stress induced genes and stress tolerance in budding yeast. FEMS Microbiol Rev 24:469–486CrossRefGoogle Scholar
  12. França MB, Panek AD, Eleutherio ECA (2007) Oxidative stress and its effects during dehydration. Comp Biochem Physiol A 146:621–631CrossRefGoogle Scholar
  13. Garre E, Raginel F, Palacios A, Julien A, Matallana E (2010) Oxidative stress responses and lipid peroxidation damage are induced during dehydration in the production of dry active wine yeasts. Int J Food Microbiol 136:295–303CrossRefGoogle Scholar
  14. Gorbushina AA (2007) Life on the rocks. Environ Microbiol 9:1613–1631Google Scholar
  15. Gorbushina AA, Broughton WJ (2009) Microbiology of the atmosphere–rock interface: how biological interactions and physical stresses modulate a sophisticated microbial ecosystem. Annu Rev Microbiol 63:431–450CrossRefGoogle Scholar
  16. Greenspan L (1977) Humidity fixed points of binary saturated aqueous solutions. J Res Natl Bur Stand 81a:89–96Google Scholar
  17. Grossmann G, Opekarová M, Malinsky J, Weig-Meckl I, Tanner W (2007) Membrane potential governs lateral segregation of plasma membrane proteins and lipids in yeast. EMBO J 26:1–8CrossRefGoogle Scholar
  18. Gunde Cimerman N, Zalar P, Hoog S, Plemenitaš A (2000) Hypersaline waters in salterns–natural ecological niches for halophilic black yeasts. FEMS Microbiol Ecol 32:235–240Google Scholar
  19. Herdeiro R, Pereira M, Panek A, Eleutherio E (2006) Trehalose protects Saccharomyces cerevisiae from lipid peroxidation during oxidative stress. Biochim Biophys Acta 1760:340–346CrossRefGoogle Scholar
  20. Ito H, Fukuda Y, Murata K, Kimura A (1983) Transformation of intact yeast cells treated with alkali cations. J Bacteriol 153:163–168Google Scholar
  21. Klipp E, Nordlander B, Krüger R, Gennemark P, Hohmann S (2005) Integrative model of the response of yeast to osmotic shock. Nat Biotechnol 23:975–982CrossRefGoogle Scholar
  22. Landolfo S, Zara G, Zara S, Budroni M, Ciani M, Mannazzu I (2010) Oleic acid and ergosterol supplementation mitigates oxidative stress in wine strains of Saccharomyces cerevisiae. Int J Food Microbiol 141:229–235CrossRefGoogle Scholar
  23. Landry CR, Townsend JP, Hartl DL, Cavalieri D (2006) Ecological and evolutionary genomics of Saccharomyces cerevisiae. Mol Ecol 15:575–591CrossRefGoogle Scholar
  24. Malinska K, Malinsky J, Opekarova M, Tanner W (2004) Distribution of Can1p into stable domains reflects lateral protein segregation within the plasma membrane of living S. cerevisiae cells. J Cell Sci 117:6031–6041CrossRefGoogle Scholar
  25. Meng XC, Stanton C, Fitzgerald GF, Daly C, Ross RP (2008) Anhydrobiotics: the challenges of drying probiotic cultures. Food Chem 106:1406–1416Google Scholar
  26. Milhaud J (2004) New insights into water–phospholipid model membrane interactions. Biochim Biophys Acta 1663:19–51CrossRefGoogle Scholar
  27. Mille Y, Beney L, Gervais P (2002) Viability of Escherichia coli after combined osmotic and thermal treatment: a plasma membrane implication. Biochim Biophys Acta 1567:41–48CrossRefGoogle Scholar
  28. Norrish RS (1966) An equation for the activity coefficients and equilibrium relative humidities of water in confectionery syrups. Int J Food Sci Technol 1:25–39CrossRefGoogle Scholar
  29. Pereira E, Panek AD, Eleutherio ECA (2003) Protection against oxidation during dehydration of yeast. Cell Stress Chaperones 8:120–124CrossRefGoogle Scholar
  30. Petrovic U (2006) Role of oxidative stress in the extremely salt-tolerant yeast Hortaea werneckii. FEMS Yeast Res 6:816–822CrossRefGoogle Scholar
  31. Piette J (1991) New trends in photobiology: biological consequences associated with DNA oxidation mediated by singlet oxygen. J Photochem Photobiol B Biol 11:241–260CrossRefGoogle Scholar
  32. Quispel A (1998) Lourens GM Baas Becking (1895–1963). Inspirator for many (micro) biologists. Int Microbiol 1:69–72Google Scholar
  33. Ragoonanan V, Malsam J, Bond DR, Aksan A (2008) Roles of membrane structure and phase transition on the hyperosmotic stress survival of Geobacter sulfurreducens. Biochim Biophys Acta 1778:2283–2290CrossRefGoogle Scholar
  34. Ratnakumar S, Hesketh A, Gkargkas K, Wilson M, Rash BM, Hayes A, Tunnacliffe A, Oliver SG (2011) Phenomic and transcriptomic analyses reveal that autophagy plays a major role in desiccation tolerance in Saccharomyces cerevisiae. Mol Biosyst 7:139–149CrossRefGoogle Scholar
  35. Rodriguez-Porrata B, Novo M, Guillamón J, Rozes N, Mas A, Otero RC (2008) Vitality enhancement of the rehydrated active dry wine yeast. Int J Food Microbiol 126:116–122CrossRefGoogle Scholar
  36. Rodriguez-Vargas S, Sanchez-Garcia A, Martinez-Rivas J, Prieto J, Randez-Gil F (2007) Fluidization of membrane lipids enhances the tolerance of Saccharomyces cerevisiae to freezing and salt stress. Appl Environ Microbiol 73:110–116CrossRefGoogle Scholar
  37. Santos H, Da Costa MS (2002) Compatible solutes of organisms that live in hot saline environments. Environ Microbiol 4:501–509CrossRefGoogle Scholar
  38. Scherber C, Schottel J, Aksan A (2009) Membrane phase behavior of Escherichia coli during desiccation, rehydration, and growth recovery. Biochim Biophys Acta 1788:2427–2435CrossRefGoogle Scholar
  39. Simonin H, Beney L, Gervais P (2007) Sequence of occurring damages in yeast plasma membrane during dehydration and rehydration: mechanisms of cell death. Biochim Biophys Acta 1768:1600–1610CrossRefGoogle Scholar
  40. Teixeira P, Castro H, Kirby R (1996) Evidence of membrane lipid oxidation of spray-dried Lactobacillus bulgaricus during storage. Lett Appl Microbiol 22:34–38CrossRefGoogle Scholar
  41. Tunnacliffe A, Lapinski J (2003) Resurrecting Van Leeuwenhoek’s rotifers: a reappraisal of the role of disaccharides in anhydrobiosis. Phil Trans R Soc Lond 358:1755–1771Google Scholar
  42. Turk M, Abramovi Z, Plemenitaš A, Gunde Cimerman N (2007) Salt stress and plasma membrane fluidity in selected extremophilic yeasts and yeast like fungi. FEMS Yeast Res 7:550–557CrossRefGoogle Scholar
  43. Wolfe J, Dowgert MF, Steponkus PL (1986) Mechanical study of the deformation and rupture of the plasma membranes of protoplasts during osmotic expansions. J Membr Biol 93:63–74CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • Guillaume Lemetais
    • 1
    • 2
  • Sébastien Dupont
    • 1
  • Laurent Beney
    • 1
  • Patrick Gervais
    • 1
  1. 1.Université de Bourgogne/AGROSUP Dijon, UMR Procédés Alimentaires et MicrobiologiquesDijonFrance
  2. 2.Merck Medication FamilialeDijonFrance

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