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Changes in Lipids Composition and Fluidity of Yeast Plasma Membrane as Response to Cold

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Cold-adapted Yeasts

Abstract

In order to function properly, plasma membranes have to preserve a suitable dynamic state of the bilayer even in changing environments, which alters their fluidity. This is achieved by active restructuring of membrane lipids composition. Perturbations in membrane structure determined by environment may result in significant disruption of its physiological function. Accordingly, its composition is modified as response to environmental changes. Because the fluid state of plasma membrane is mandatory for proper functioning, organisms exposed to changes in the environmental conditions alter their membrane lipid composition, to maintain membrane lipids in a lamellar liquid crystalline phase, and avoid the formation of a lamellar gel phase. One of the main adaptative mechanisms to overcome the negative effect of cold is the ability to finely adjust phospholipid composition and physical properties of their plasma membranes. The minimum growth temperature of a given organism is reached when the degree of fluidity of its plasma membrane becomes too low for allowing the trans-membrane-nutrient transport. Yeasts have long served as an attractive model of a eukaryotic system for studying the regulation of lipid biosynthesis and thermal adaptation of the plasma membrane: the ability of psychrophilic, psychrotolerant and mesophilic yeasts to change the composition of phospholipids may suggest that the extent of such changes may be an important controlling factor, which determines the yeast growth temperature limits and limits for their distribution in the environment. In this chapter, some essential aspects of the changes in lipids composition and fluidity of yeast plasma membrane as response to cold are reported.

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References

  • AI-Fageeh MB, Smales CM (2006) Control and regulation of the cellular responses to cold shock: the responses in yeast and mammalian systems. Biochem J 397:247–259

    Article  Google Scholar 

  • Arthur H, Watson K (1976) Thermal adaptation in yeast: growth temperatures, membrane lipid, and cytochrome composition of psychrophilic, mesophilic, and thermophilic yeasts. J Bacteriol 128:56–68

    CAS  PubMed  Google Scholar 

  • Becker GW, Lester RL (1977) Changes in phospholipids of Saccharomyces cerevisiae associated with inositol-less death. J Biol Chem 252:8684–8691

    CAS  PubMed  Google Scholar 

  • Beney L, Gervais P (2001) Influence of the fluidity of the membrane on the response of microorganisms to environmental stresses. Appl Microbiol Biotechnol 57:34–42

    Article  CAS  PubMed  Google Scholar 

  • Blusztajn JK (1998) Choline, a vital amine. Science 281:794–795

    Article  CAS  PubMed  Google Scholar 

  • Carman GM, Han GS (2006) Roles of phosphatidate phosphatase enzymes in lipid metabolism. Trends Biochem Sci 31:694–699

    Article  CAS  PubMed  Google Scholar 

  • Carman GM, Han GS (2007) Regulation of phospholipid synthesis in Saccharomyces cerevisiae by zinc depletion. Biochim Biophys Acta 1771:322–330

    Article  CAS  PubMed  Google Scholar 

  • Carman GM, Han GS (2011) Regulation of phospholipid synthesis in the yeast Saccharomyces cerevisiae. Annu Rev Biochem 80:859–883

    Article  CAS  PubMed  Google Scholar 

  • Carman GM, Henry SA (1989) Phospholipid biosynthesis in yeast. Annu Rev Biochem 58:635–669

    Article  CAS  PubMed  Google Scholar 

  • Carman GM, Henry SA (1999) Phospholipid biosynthesis in the yeast Saccharomyces cerevisiae and interrelationship with other metabolic processes. Prog Lipid Res 38:361–399

    Article  CAS  PubMed  Google Scholar 

  • Carman GM, Henry SA (2007) Phosphatidic acid plays a central role in the transcriptional regulation of glycerophospholipid synthesis in Saccharomyces cerevisiae. J Biol Chem 282:37293–37297

    Article  CAS  PubMed  Google Scholar 

  • Carman GM, Kersting MC (2004) Phospholipid synthesis in yeast: regulation by phosphorylation. Biochem Cell Biol 82:62–70

    Article  CAS  PubMed  Google Scholar 

  • Carman GM, Zeimetz GM (1996) Regulation of phospholipid biosynthesis in the yeast Saccharomyces cerevisiae. J Biol Chem 271:13293–13296

    Article  CAS  PubMed  Google Scholar 

  • Chang YF, Carman GM (2008) CTP synthetase and its role in phospholipid synthesis in the yeast Saccharomyces cerevisiae. Prog Lipid Res 47:333–339

    Article  CAS  PubMed  Google Scholar 

  • Chen M, Hancock LC, Lopes JM (2007) Transcriptional regulation of yeast phospholipid biosynthetic genes. Biochim Biophys Acta 1771:310–321

    Article  CAS  PubMed  Google Scholar 

  • Chintalapati S, Kiran MD, Shivaji S (2004) Role of membrane lipid fatty acids in cold adaptation. Cell Mol Biol 50:631–642

    CAS  PubMed  Google Scholar 

  • Clancey CJ, Chang S, Dowhan W (1993) Cloning of a gene (PSD1) encoding phosphatidylserine decarboxylase from Saccharomyces cerevisiae by complementation of an Escherichia coli mutant. J Biol Chem 268:24580–24590

    CAS  PubMed  Google Scholar 

  • Coolbear KP, Berde CB, Keough KMW (1983) Gel to liquid-crystalline phase transitions of aqueous dispersions of polyunsaturated mixed-acid phosphatidylcholines. Biochemistry 22:1466–1473

    Article  CAS  PubMed  Google Scholar 

  • Cossins AR, Murray PA, Gracey AY, Logue J, Polley S, Caddick M, Brooks S, Pestle T, Maclean N (2002) The role of desaturases in cold induced lipid restructuring. Biochem Soc Trans 30:1082–1086

    Article  CAS  PubMed  Google Scholar 

  • Daum G, Lees ND, Bard M, Dickson R (1998) Biochemistry, cell biology and molecular biology of lipids of Saccharomyces cerevisiae. Yeast 14:1471–1510

    Article  CAS  PubMed  Google Scholar 

  • Daum G, Tuller, G Nemec T, Hrastnik C, Balliano G, Cattel L, Milla P, Rocco F, Conzelmann A, Vionnet C, Kelly DE, Kelly S, Schweizer E, Schüller HJ, Hojad U, Greiner E, Finger K (1999) Systematic analysis of yeast strains with possible defects in lipid metabolism. Yeast 15:601–614

    Google Scholar 

  • Davis PJ, Fleming BD, Coolbear KP, Keough KMW (1981) Gel to liquid-crystalline transition temperatures of water dispersions of two pairs of positional isomers of unsaturated mixed acid phosphatidyl cholines. Biochemistry 20:3633–3636

    Article  CAS  PubMed  Google Scholar 

  • Dickson RC (2008) New insights into sphingolipid metabolism and function in budding yeast. J Lipid Res 49:909–921

    Article  CAS  PubMed  Google Scholar 

  • Feller G (2007) Life at low temperatures: is disorder the driving force? Extremophiles 11:211–216

    Article  CAS  PubMed  Google Scholar 

  • Gaspar ML, Aregullin MA, Jesch SA, Nunez LR, Villa-Garcia M, Henry SA (2007) The emergence of yeast lipidomics. Biochim Biophys Acta 1771:241–254

    Article  CAS  PubMed  Google Scholar 

  • Gaspar ML, Jesch SA, Viswanatha R, Antosh AL, Brown WJ, Kohlwein SD, Henry SA (2008) A block in endoplasmic reticulum-to-Golgi trafficking inhibits phospholipid synthesis and induces neutral lipid accumulation. J Biol Chem 283:25735–25751

    Article  CAS  PubMed  Google Scholar 

  • Gerday C, Aittaleb M, Bentahir M, Chessa JP, Claverie P, Collins T, D’Amico S, Dumont J, Garsoux G, Georlette D, Hoyoux A, Lonhienne T, Meuwis MA, Feller G (2000) Cold-adapted enzymes: from fundamentals to biotechnology. Trend Biotechnol 18:103–107

    Article  CAS  Google Scholar 

  • Gostincar C, Turk M, Gunde–Cimerman N (2009) Environmental impacts on fatty acid composition of fungal mebranes. In: Misra Jk, Desmukh SK (eds) Fungi from different environments. Science Publishers, Enfield, pp 278–327

    Chapter  Google Scholar 

  • Guschina IA, Harwood JL (2006) Mechanisms of temperature adaptation in poikilotherms. FEBS Lett 580:5477–5483

    Article  CAS  PubMed  Google Scholar 

  • Hazel JR, Williams EE (1990) Therole of alterations in membrane lipid composition in enabling physiological adaptation of organisms to their physical environment. Progr Lipid Res 29:167–227

    Article  CAS  Google Scholar 

  • Henschke PA, Rose AH (1991) Plasma membranes. In: Rose AH, Harrison JS (eds) The yeasts, 2nd edn, vol 4, Yeast organelles. Academic Press, London, pp 297–435

    Google Scholar 

  • Höfer M (1997) Membranes. In: Spencer JFT, Spencer DM (eds) Yeasts in natural and artificial habitats. Springer, Berlin, pp 95–132

    Chapter  Google Scholar 

  • Hunter K, Rose AH (1972) Lipid composition of Saccharomyces cerevisiae as influenced by growth temperature. Biochim Biophys Acta 260:639–653

    Article  CAS  PubMed  Google Scholar 

  • Kates M, Baxter RM (1962) Lipid composition of mesophilic and psychrophilic yeasts (Candida species) as influenced by environmental temperatures. Can J Biochem Physiol 40:1213–1227

    Article  CAS  PubMed  Google Scholar 

  • Kates M, Pugh EL, Ferrante G (1984) Regulation of membrane fluidity by lipid desaturases. In: Kates M, Mason LA (eds) Membrane fluidity, vol 12., BiomembranesPlenum Press, New York, pp 379–395

    Chapter  Google Scholar 

  • Los DA, Murata N (2004) Membrane fluidity and its roles in the perception of environmental signals. Biochim Biophys Acta 1666:142–157

    Article  CAS  PubMed  Google Scholar 

  • Losel DM (1990) Lipids in the structure and function of fungal membranes. In: Kuhn PJ, Trinci APJ, Jung MJ, Goosey MW, Copping LG (eds) Biochemistry of the cell walls and membranes in fungi. Springer, Berlin, pp 119–133

    Chapter  Google Scholar 

  • Madigan MT, Martinko JM, Parker J (1997) Brock biology of microorganisms, 8th edn. Prentice Hall, Upper Saddle River

    Google Scholar 

  • Malanovic N, Streith I, Wolinski H, Rechberger G, Kohlwein SD, Tehlivets O (2008) S-adenosyl-L-homocysteine hydrolase, key enzyme of methylation metabolism, regulates phosphatidylcholine synthesis and triacylglycerol homeostasis in yeast: implications for homocysteine as a risk factor of atherosclerosis. J Biol Chem 283:23989–23999

    Article  CAS  PubMed  Google Scholar 

  • Mansilla MC, Cybulski LE, de Albanesi D, Mendoza D (2004) Control of membrane lipid fluidity by molecular thermosensors. J Bacteriol 186:6681–6688

    Article  CAS  PubMed  Google Scholar 

  • Martin CE, Oh CS, Jiang Y (2007) Regulation of long chain unsaturated fatty acid synthesis in yeast. Biochim Biophys Acta 1771:271–285

    Article  CAS  PubMed  Google Scholar 

  • McGraw P, Henry S (1989) Mutations in the Saccharomyces cerevisiae Opi3 gene: effects on phospholipid methylation, growth and cross-pathway regulation of inositol synthesis. Genetics 122:317–330

    CAS  PubMed  Google Scholar 

  • McMurrough I, Rose AH (1973) Effects of temperature variation on the fatty acid composition of a psychrophilic Candida species. J Bacteriol 114:451–452

    CAS  PubMed  Google Scholar 

  • Morgan-Kiss RM, Priscu JC, Pocock T, Gudynaite-Savitch L, Huner NP (2006) Adaptation and acclimation of photosynthetic microorganisms to permanently cold environments. Microbiol Mol Biol R 70:222–252

    Article  CAS  Google Scholar 

  • Nakagawa Y, Sakumoto N, Kaneko Y, Harashima S (2002) Mga2p is a putative sensor for low temperature and oxygen to induce OLE1 transcription in Saccharomyces cerevisiae. Biochem Bioph Res Co 291:707–713

    Article  CAS  Google Scholar 

  • Okuyama H, Saito M, Joshi VC, Gunsberg S, Wakil SJ (1979) Regulation by temperature of the chain length of fatty acids in yeast. J Biol Chem 254:12281–12284

    CAS  PubMed  Google Scholar 

  • Paltauf F, Kohlwein SD, Henry SA (1992) Regulation and compartmentalization of lipid synthesis in yeast. In: Jones EW, Pringle JR, Broach JR (eds) The molecular and cellular biology of the yeast Saccharomyces: gene expression. Cold Spring Harbor, New York, pp 415–500

    Google Scholar 

  • Panadero J, Pallotti C, Rodriguez-Vargas S, Randez-Cil F, Prieto JA (2006) A downshift in temperature activates the high osmolarity glycerol (HOG) pathway, which determines freeze tolerance in Saccharomyces cerevisiae. J Biol Chem 281:4638–4645

    Article  CAS  PubMed  Google Scholar 

  • Phadtare S (2004) Recent developments in bacterial cold-shock response. Curr Issues Mol Biol 6:125–136

    CAS  PubMed  Google Scholar 

  • Pugh EL, Kates M (1975) Characterization of a membrane-bound phospholipid desaturase system of Candida lipolytica. Biochim Biophys Acta 380:442–453

    Article  CAS  PubMed  Google Scholar 

  • Rajakumari S, Grillitsch K, Daum G (2008) Synthesis and turnover of non polar lipids in yeast. Prog Lipid Res 47:157–171

    Article  CAS  PubMed  Google Scholar 

  • Raspor P, Zupan J (2006) Yeasts in extreme environments. In: Rosa CA, Peter G (eds) Biodiversity and ecophysiology of yeasts. Springer, Berlin, pp 371–417

    Chapter  Google Scholar 

  • Rattray JB, Schibeci A, Kidby DK (1975) Lipids of yeast. Bacteriol Rev 39:197–231

    CAS  PubMed  Google Scholar 

  • Redón M, Borrull A, López M, Salvadó Z, Cordero R, Mas A, Guillamón JM, Rozès N (2012) Effect of low temperature upon vitality of Saccharomyces cerevisiae phospholipid mutants. Yeast 29:443–452

    Article  PubMed  Google Scholar 

  • Rilfors L, Lindblom G (2002) Regulation of lipid compositionin biological membranes-biophysical studies of lipids and lipid synthesizing enzymes. Colloids Surf, B 26:112–124

    Article  CAS  Google Scholar 

  • Rodrıguez-Vargas S, Sanchez-Garcıa A, Martınez-Rivas JM, Prieto JA, 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  PubMed  Google Scholar 

  • Rossi M, Buzzini P, Cordisco L, Amaretti A, Sala M, Raimondi S, Ponzoni C, Pagnoni UM, Matteuzzi D (2009) Growth, lipid accumulation and fatty acid composition in obligate psychrophilic, facultative psychrophilic, and mesophilic yeasts. FEMS Microbiol Ecol 69:363–372

    Article  CAS  PubMed  Google Scholar 

  • Russell NJ (1989) Structural and functional role of lipids. In: Ratledge C, Wilkinson SG (eds) Microbial lipids, vol 2. Academic Press, New York, pp 249–279

    Google Scholar 

  • Russell NJ (1997) Psychrophilic bacteria: molecular adaptations of membrane lipids. Comp Biochem Phys A 118:489–493

    Article  CAS  Google Scholar 

  • Russell NJ (2008) Membrane components and cold sensing. In: Margesin R, Schinner F, Marx JC, Gerday C (eds) Psychrophiles: from biodiversity to biotechnology. Springer, Berlin, pp 177–190

    Chapter  Google Scholar 

  • Russell NJ, Evans RI, ter Steeg PF, Hellemons J, Verheul A, Abee T (1995) Membranes as a target for stress adaptation. Int J Food Microbiol 28:255–261

    Article  CAS  PubMed  Google Scholar 

  • Schneiter K, Brugger B, Sandhoff K (1999) Electrospray ionization tandem mass spectrometry (ESI-MS/MS) analysis of the lipid molecular species composition of yeast subcellular membranes reveals acyl chain-based sorting/remodeling of distinct molecular species en route to the plasma membrane. J Cell Biol 146:741–754

    Article  CAS  PubMed  Google Scholar 

  • Selbmann L, de Hoog GS, Mazzaglia A, Friedmann EI, Onofri S (2005) Fungi at the edge of life: cryptoendolithic black fungi from Antarctic desert. Stud Mycol 51:1–32

    Google Scholar 

  • Shivaji S, Prasad GS (2009) Antarctic yeasts: biodiversity and potential applications. In: Satyanarayana T, Kunze G (eds) Yeast biotechnology: diversity and applications. Springer, Berlin, pp 3–16

    Chapter  Google Scholar 

  • Shivaji S, Kiran MD, Chintalapati S (2007) Perception and transduction of low temperature in bacteria. In: Gerday C, Glansdorff N (eds) Physiology and biochemistry of extremophiles. ASM Press, Washington DC, pp 194–207

    Google Scholar 

  • Simonin H, Beney L, Gervais P (2008) Controlling the membrane fluidity of yeasts during coupled thermal and osmotic treatments. Biotechnol Bioeng 100:325–333

    Article  CAS  PubMed  Google Scholar 

  • Simons K, Toomre D (2000) Lipid rafts and signal transduction. Nature Rev Mol Cell Biol 1:31–39

    Article  CAS  Google Scholar 

  • Stukey JE, McDonough VM, Martin CE (1989) Isolation and characterization of OLE1, a gene affecting fatty acid desaturation from Saccharomyces cerevisiae. J Biol Chem 264:16537–16544

    CAS  PubMed  Google Scholar 

  • Suutari M, Liukkonen K, Laakso S (1990) Temperature adaptation in yeasts: the role of fatty acids. J Gen Microbiol 136:1469–1474

    Article  CAS  PubMed  Google Scholar 

  • Suutari M, Rintamaki A, Laakso S (1997) Membrane phospholipids in temperature adaptation of Candida utilis: alterations in fatty acid chain length and unsaturation. J Lipid Res 38:790–794

    CAS  PubMed  Google Scholar 

  • Swan TM, Watson K (1997) Membrane fatty acid composition and membrane fluidity as parameters of stress tolerance in yeast. Can J Microbiol 43:70–77

    Article  CAS  PubMed  Google Scholar 

  • Thomas-Hall S, Watson K (2002) Cryptococcus nyarrowii sp. nov., a basidiomycetous yeast from Antarctica. Int J Syst Evol Microbiol 52:1033–1038

    Article  CAS  PubMed  Google Scholar 

  • Thomas-Hall S, Watson K, Scorzetti G (2002) Cryptococcus statzelliae sp. nov. and three novel strains of Cryptococcus victoriae, yeasts isolated from Antarctic soils. Int J Syst Evol Microbiol 52:2303–2308

    Article  CAS  PubMed  Google Scholar 

  • Trotter PJ, Pedretti J, Voelker DR (1993) Phosphatidylserine decarboxylase from Saccharomyces cerevisiae. Isolation of mutants, cloning of the gene, and creation of a null allele. J Biol Chem 268:21416–21424

    CAS  PubMed  Google Scholar 

  • Turk M, Mejanelle L, Šentjurc M, Grimalt JO, Gunde-Cimerman N, Plemenitaš A (2004) Salt-induced changes in lipid composition and membrane fluidity of halophilic yeast-like melanized fungi. Extremophiles 8:53–61

    Article  CAS  PubMed  Google Scholar 

  • Turk M, Montel V, Žigon D, Plemenitas A, Ramos J (2007) Plasma membrane composition of Debaryomyces hansenii adapts to changes in pH and external salinity. Microbiology (Soc Gen Microbiol) 153:3586–3592

    CAS  Google Scholar 

  • Turk M, Plemenitaš A, Gunde-Cimerman N (2011) Extremophilic yeasts: plasma-membrane fluidity as determinant of stress tolerance. Fungal Biol 115:950–958

    Article  CAS  PubMed  Google Scholar 

  • van der Rest ME, Kamminga AH, Nakanoi A, Anraku Y, Poolman B, Konings WN (1995) The plasma membrane of S. cerevisiae: structure, function and biogenesis. Microbiol Rev 59:304–322

    PubMed  Google Scholar 

  • Vishniac HS (2006) Yeast biodiversity in the Antarctic. In: Rosa CA, Peter G (eds) Biodiversity and ecophysiology of yeasts. Springer, Berlin, pp 420–440

    Google Scholar 

  • Vishniac HS, Kurtzman CP (1992) Cryptococcus antarcticus sp. nov, and Cryptococcus albidosimilis sp. nov., basidioblastomycetes from antarctic soils. Int J Syst Bacteriol 42:547–553

    Article  Google Scholar 

  • Walker GM (1998) Yeast physiology and biotechnology. Wiley, New York

    Google Scholar 

  • Watson K (1978) Thermal adaptation in yeasts: correlation of substrate transport with membrane lipid composition in psychrophilic and thermotolerant yeasts. Biochem Soc T 6:293–296

    CAS  Google Scholar 

  • Watson K (1987) Temperature relations. In: Rose AH, Harrison JS (eds) The yeasts. Academic Press, London, pp 41–71

    Google Scholar 

  • Watson K, Rose AH (1980) Fatty-acyl composition of the lipids of Saccharomyces cerevisiae grown aerobically or anaerobically in media containing different fatty acids. J Gen Microbiol 117:225–233

    CAS  Google Scholar 

  • Watson K, Arthur H, Shipton WA (1976) Leucosporidium yeasts: obligate psychrophiles which alter membrane-lipid and cytochrome composition with temperature. J Gen Microbiol 97:11–18

    Article  CAS  PubMed  Google Scholar 

  • Watson K, Morton H, Arthur H, Streamer M (1978) Membrane lipid composition: a determinant of anaerobic growth and petite formation in psychrophilic and psychrophobic yeasts. Biochem Soc T 6:380–381

    CAS  Google Scholar 

  • White PL, Wynn-Williams DD, Russell NJ (2000) Diversity of thermal responses of lipid composition in the membranes of the dominant culturable members of an Antarctic fell field soil bacterial community. Antarct Sci 12:386–393

    Article  Google Scholar 

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Gunde-Cimerman, N., Plemenitaš, A., Buzzini, P. (2014). Changes in Lipids Composition and Fluidity of Yeast Plasma Membrane as Response to Cold. In: Buzzini, P., Margesin, R. (eds) Cold-adapted Yeasts. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-39681-6_10

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