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Air-drying kinetics affect yeast membrane organization and survival

  • Applied microbial and cell physiology
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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.

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References

  • Abe F, Hiraki T (2009) Mechanistic role of ergosterol in membrane rigidity and cycloheximide resistance in Saccharomyces cerevisiae. Biochim Biophys Acta 1788:743–752

    Article  CAS  Google Scholar 

  • Anand JC, Brown AD (1968) Growth rate patterns of the so-called osmophilic and non-osmophilic yeasts in solutions of polyethylene glycol. Microbiology 52:205

    CAS  Google Scholar 

  • Beker M, Rapoport A (1987) Conservation of yeasts by dehydration. Adv Biochem Eng Biotechnol 35:127–171

    Google Scholar 

  • Brown A (1990) Microbial water stress physiology. Principles and perspectives. Wiley, New York

    Google Scholar 

  • Chirife J, Fontan CF (1980) A study of the water activity lowering behavior of polyethylene glycols in the intermediate moisture range. J Food Sci 45:1717–1719

    Article  CAS  Google Scholar 

  • Crowe JH, Crowe LM, Chapman D (1984) Preservation of membranes in anhydrobiotic organisms: the role of trehalose. Science 223:701–703

    Article  CAS  Google Scholar 

  • 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 86:520

    Article  CAS  Google Scholar 

  • Crowe J, Hoekstra F, Crowe L (1992) Anhydrobiosis. Annu Rev Physiol 54:579–599

    Article  CAS  Google Scholar 

  • 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 1798:975–985

    Article  CAS  Google Scholar 

  • Dupont S, Beney L, Ferreira T, Gervais P (2011) Nature of sterols affects plasma membrane behavior and yeast survival during dehydration. Biochim Biophys Acta 1808:1520–1528

    Article  CAS  Google Scholar 

  • Estruch F (2000) Stress controlled transcription factors, stress induced genes and stress tolerance in budding yeast. FEMS Microbiol Rev 24:469–486

    Article  CAS  Google Scholar 

  • França MB, Panek AD, Eleutherio ECA (2007) Oxidative stress and its effects during dehydration. Comp Biochem Physiol A 146:621–631

    Article  Google Scholar 

  • 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 136:295–303

    Article  CAS  Google Scholar 

  • Gorbushina AA (2007) Life on the rocks. Environ Microbiol 9:1613–1631

    Google Scholar 

  • 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 63:431–450

    Article  CAS  Google Scholar 

  • Greenspan L (1977) Humidity fixed points of binary saturated aqueous solutions. J Res Natl Bur Stand 81a:89–96

    Google Scholar 

  • 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 26:1–8

    Article  CAS  Google Scholar 

  • Gunde Cimerman N, Zalar P, Hoog S, Plemenitaš A (2000) Hypersaline waters in salterns–natural ecological niches for halophilic black yeasts. FEMS Microbiol Ecol 32:235–240

    CAS  Google Scholar 

  • Herdeiro R, Pereira M, Panek A, Eleutherio E (2006) Trehalose protects Saccharomyces cerevisiae from lipid peroxidation during oxidative stress. Biochim Biophys Acta 1760:340–346

    Article  CAS  Google Scholar 

  • Ito H, Fukuda Y, Murata K, Kimura A (1983) Transformation of intact yeast cells treated with alkali cations. J Bacteriol 153:163–168

    CAS  Google Scholar 

  • Klipp E, Nordlander B, Krüger R, Gennemark P, Hohmann S (2005) Integrative model of the response of yeast to osmotic shock. Nat Biotechnol 23:975–982

    Article  CAS  Google Scholar 

  • 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 141:229–235

    Article  CAS  Google Scholar 

  • Landry CR, Townsend JP, Hartl DL, Cavalieri D (2006) Ecological and evolutionary genomics of Saccharomyces cerevisiae. Mol Ecol 15:575–591

    Article  CAS  Google Scholar 

  • 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 117:6031–6041

    Article  CAS  Google Scholar 

  • Meng XC, Stanton C, Fitzgerald GF, Daly C, Ross RP (2008) Anhydrobiotics: the challenges of drying probiotic cultures. Food Chem 106:1406–1416

    Google Scholar 

  • Milhaud J (2004) New insights into water–phospholipid model membrane interactions. Biochim Biophys Acta 1663:19–51

    Article  CAS  Google Scholar 

  • Mille Y, Beney L, Gervais P (2002) Viability of Escherichia coli after combined osmotic and thermal treatment: a plasma membrane implication. Biochim Biophys Acta 1567:41–48

    Article  CAS  Google Scholar 

  • Norrish RS (1966) An equation for the activity coefficients and equilibrium relative humidities of water in confectionery syrups. Int J Food Sci Technol 1:25–39

    Article  CAS  Google Scholar 

  • Pereira E, Panek AD, Eleutherio ECA (2003) Protection against oxidation during dehydration of yeast. Cell Stress Chaperones 8:120–124

    Article  Google Scholar 

  • Petrovic U (2006) Role of oxidative stress in the extremely salt-tolerant yeast Hortaea werneckii. FEMS Yeast Res 6:816–822

    Article  CAS  Google Scholar 

  • Piette J (1991) New trends in photobiology: biological consequences associated with DNA oxidation mediated by singlet oxygen. J Photochem Photobiol B Biol 11:241–260

    Article  CAS  Google Scholar 

  • Quispel A (1998) Lourens GM Baas Becking (1895–1963). Inspirator for many (micro) biologists. Int Microbiol 1:69–72

    CAS  Google Scholar 

  • 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 1778:2283–2290

    Article  CAS  Google Scholar 

  • 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 7:139–149

    Article  CAS  Google Scholar 

  • 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 126:116–122

    Article  CAS  Google Scholar 

  • 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 73:110–116

    Article  CAS  Google Scholar 

  • Santos H, Da Costa MS (2002) Compatible solutes of organisms that live in hot saline environments. Environ Microbiol 4:501–509

    Article  CAS  Google Scholar 

  • Scherber C, Schottel J, Aksan A (2009) Membrane phase behavior of Escherichia coli during desiccation, rehydration, and growth recovery. Biochim Biophys Acta 1788:2427–2435

    Article  CAS  Google Scholar 

  • 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 1768:1600–1610

    Article  CAS  Google Scholar 

  • Teixeira P, Castro H, Kirby R (1996) Evidence of membrane lipid oxidation of spray-dried Lactobacillus bulgaricus during storage. Lett Appl Microbiol 22:34–38

    Article  CAS  Google Scholar 

  • Tunnacliffe A, Lapinski J (2003) Resurrecting Van Leeuwenhoek’s rotifers: a reappraisal of the role of disaccharides in anhydrobiosis. Phil Trans R Soc Lond 358:1755–1771

    Google Scholar 

  • 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 7:550–557

    Article  CAS  Google Scholar 

  • 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 93:63–74

    Article  Google Scholar 

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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).

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Authors and Affiliations

  1. Université de Bourgogne/AGROSUP Dijon, UMR Procédés Alimentaires et Microbiologiques, 1 Esplanade Erasme, Dijon, France

    Guillaume Lemetais, Sébastien Dupont, Laurent Beney & Patrick Gervais

  2. Merck Medication Familiale, 18C boulevard Winston Churchill, Dijon, France

    Guillaume Lemetais

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  1. Guillaume Lemetais
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  2. Sébastien Dupont
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  3. Laurent Beney
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  4. Patrick Gervais
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Correspondence to Laurent Beney.

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Lemetais, G., Dupont, S., Beney, L. et al. Air-drying kinetics affect yeast membrane organization and survival. Appl Microbiol Biotechnol 96, 471–480 (2012). https://doi.org/10.1007/s00253-012-4014-3

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  • DOI: https://doi.org/10.1007/s00253-012-4014-3

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