全部 标题 作者
关键词 摘要

OALib Journal期刊
ISSN: 2333-9721
费用:99美元

查看量下载量

相关文章

更多...
PLOS ONE  2013 

Lipidomic Profiling of Saccharomyces cerevisiae and Zygosaccharomyces bailii Reveals Critical Changes in Lipid Composition in Response to Acetic Acid Stress

DOI: 10.1371/journal.pone.0073936

Full-Text   Cite this paper   Add to My Lib

Abstract:

When using microorganisms as cell factories in the production of bio-based fuels or chemicals from lignocellulosic hydrolysate, inhibitory concentrations of acetic acid, released from the biomass, reduce the production rate. The undissociated form of acetic acid enters the cell by passive diffusion across the lipid bilayer, mediating toxic effects inside the cell. In order to elucidate a possible link between lipid composition and acetic acid stress, the present study presents detailed lipidomic profiling of the major lipid species found in the plasma membrane, including glycerophospholipids, sphingolipids and sterols, in Saccharomyces cerevisiae (CEN.PK 113_7D) and Zygosaccharomyces bailii (CBS7555) cultured with acetic acid. Detailed physiological characterization of the response of the two yeasts to acetic acid has also been performed in aerobic batch cultivations using bioreactors. Physiological characterization revealed, as expected, that Z. bailii is more tolerant to acetic acid than S. cerevisiae. Z. bailii grew at acetic acid concentrations above 24 g L?1, while limited growth of S. cerevisiae was observed after 11 h when cultured with only 12 g L?1 acetic acid. Detailed lipidomic profiling using electrospray ionization, multiple-reaction-monitoring mass spectrometry (ESI-MRM-MS) showed remarkable changes in the glycerophospholipid composition of Z. bailii, including an increase in saturated glycerophospholipids and considerable increases in complex sphingolipids in both S. cerevisiae (IPC 6.2×, MIPC 9.1×, M(IP)2C 2.2×) and Z. bailii (IPC 4.9×, MIPC 2.7×, M(IP)2C 2.7×), when cultured with acetic acid. In addition, the basal level of complex sphingolipids was significantly higher in Z. bailii than in S. cerevisiae, further emphasizing the proposed link between lipid saturation, high sphingolipid levels and acetic acid tolerance. The results also suggest that acetic acid tolerance is associated with the ability of a given strain to generate large rearrangements in its lipid profile.

References

[1]  Laluce C, Schenberg ACG, Gallardo JCM, Coradello LFC, Pombeiro-Sponchiado SR (2012) Advances and developments in strategies to improve strains of Saccharomyces cerevisiae and processes to obtain the lignocellulosic ethanol - A review. Applied Biochemistry and Biotechnology 166: 1908–1926.
[2]  Palmqvist E, Hahn-H?gerdal B (2000) Fermentation of lignocellulosic hydrolysates. II: Inhibitors and mechanisms of inhibition. Bioresource Technology 74: 25–33.
[3]  Zhu JY, Gleisner R, Scott CT, Luo XL, Tian S (2011) High titer ethanol production from simultaneous enzymatic saccharification and fermentation of aspen at high solids: A comparison between SPORL and dilute acid pretreatments. Bioresource Technology 102: 8921–8929.
[4]  Monavari S, Galbe M, Zacchi G (2011) Influence of impregnation with lactic acid on sugar yields from steam pretreatment of sugarcane bagasse and spruce, for bioethanol production. Biomass and Bioenergy 35: 3115–3122.
[5]  Ullah A, Orij R, Brul S, Smits GJ (2012) Quantitative analysis of the modes of growth inhibition by weak organic acids in Saccharomyces cerevisiae. Applied and Environmental Microbiology 78: 8377–8387.
[6]  Pampulha ME, Loureiro-Dias MC (1990) Activity of glycolytic enzymes of Saccharomyces cerevisiae in the presence of acetic acid. Applied Microbiology and Biotechnology 34: 375–380.
[7]  Zhao J, Wang Z, Wang M, He Q, Zhang H (2008) The inhibition of Saccharomyces cerevisiae cells by acetic acid quantified by electrochemistry and fluorescence. Bioelectrochemistry 72: 117–121.
[8]  Russell JB (1992) Another explanation for the toxicity of fermentation acids at low pH: Anion accumulation versus uncoupling. Journal of Applied Bacteriology 73: 363–370.
[9]  Ludovico P, Sousa MJ, Silva MT, Le?o C, C?rte-Real M (2001) Saccharomyces cerevisiae commits to a programmed cell death process in response to acetic acid. Microbiology 147: 2409–2415.
[10]  Verduyn C, Postma E, Scheffers WA, Van Dijken JP (1992) Effect of benzoic acid on metabolic fluxes in yeasts: A continuous-culture study on the regulation of respiration and alcoholic fermentation. Yeast. 501–517.
[11]  Mollapour M, Piper PW (2007) Hog1 mitogen-activated protein kinase phosphorylation targets the yeast Fps1 aquaglyceroporin for endocytosis, thereby rendering cells resistant to acetic acid. Molecular and Cellular Biology 27: 6446–6456.
[12]  Mollapour M, Shepherd A, Piper PW (2008) Novel stress responses facilitate Saccharomyces cerevisiae growth in the monocarboxylate preservatives. Yeast 25: 169–177.
[13]  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+-ATPase. Nature 319: 689–693.
[14]  Piper P, Mahé Y, Thompson S, Pandjaitan R, Holyoak C, et al. (1998) The Pdr12 ABC transporter is required for the development of weak organic acid resistance in yeast. EMBO Journal 17: 4257–4265.
[15]  Souza CM, Schwabe TME, Pichler H, Ploier B, Leitner E, et al. (2011) A stable yeast strain efficiently producing cholesterol instead of ergosterol is functional for tryptophan uptake, but not weak organic acid resistance. Metabolic Engineering 13: 555–569.
[16]  Zheng DQ, Liu TZ, Chen J, Zhang K, Li O, et al. (2013) Comparative functional genomics to reveal the molecular basis of phenotypic diversities and guide the genetic breeding of industrial yeast strains. Applied Microbiology and Biotechnology 97: 2067–2076.
[17]  Zheng DQ, Wu XC, Wang PM, Chi XQ, Tao XL, et al. (2011) Drug resistance marker-aided genome shuffling to improve acetic acid tolerance in Saccharomyces cerevisiae. Journal of Industrial Microbiology and Biotechnology 38: 415–422.
[18]  Lu Y, Cheng YF, He XP, Guo XN, Zhang BR (2012) Improvement of robustness and ethanol production of ethanologenic Saccharomyces cerevisiae under co-stress of heat and inhibitors. Journal of Industrial Microbiology and Biotechnology 39: 73–80.
[19]  Wright J, Bellissimi E, de Hulster E, Wagner A, Pronk JT, et al. (2011) Batch and continuous culture-based selection strategies for acetic acid tolerance in xylose-fermenting Saccharomyces cerevisiae. FEMS Yeast Research 11: 299–306.
[20]  Gilbert A, Sangurdekar DP, Srienc F (2009) Rapid strain improvement through optimized evolution in the cytostat. Biotechnology and Bioengineering 103: 500–512.
[21]  Pe?a PV, Glasker S, Srienc F (2013) Genome-wide overexpression screen for sodium acetate resistance in Saccharomyces cerevisiae. Journal of Biotechnology 164(1): 26–33.
[22]  Fleet G (1992) Spoilage yeasts. Critical reviews in biotechnology 12: 1–44.
[23]  Zuehlke JM, Petrova B, Edwards CG (2013) Advances in the control of wine spoilage by Zygosaccharomyces and Dekkera/Brettanomyces. Annual Review of Food Science and Technology 4: 57–78.
[24]  Branduardi P, Valli M, Brambilla L, Sauer M, Alberghina L, et al. (2004) The yeast Zygosaccharomyces bailii: A new host for heterologous protein production, secretion and for metabolic engineering applications. FEMS Yeast Research 4: 493–504.
[25]  Dato L, Branduardi P, Passolunghi S, Cattaneo D, Riboldi L, et al. (2010) Advances in molecular tools for the use of Zygosaccharomyces bailii as host for biotechnological productions and construction of the first auxotrophic mutant. FEMS Yeast Research 10: 894–908.
[26]  Sousa MJ, Miranda L, C?rte-Real M, Le?o C (1996) Transport of acetic acid in Zygosaccharomyces bailii: Effects of ethanol and their implications on the resistance of the yeast to acidic environments. Applied and Environmental Microbiology 62: 3152–3157.
[27]  Rodrigues F, Sousa MJ, Ludovico P, Santos H, C?rte-Real M, et al.. (2012) The Fate of Acetic Acid during Glucose Co-Metabolism by the Spoilage Yeast Zygosaccharomyces bailii. PLoS ONE 7.
[28]  Arneborg N, Jespersen L, Jakobsen M (2000) Individual cells of Saccharomyces cerevisiae and Zygosaccharomyces bailii exhibit different short-term intracellular pH responses to acetic acid. Archives of Microbiology 174: 125–128.
[29]  Prudêncio C, Sansonetty F, C?rte-Real M (1998) Flow cytometric assessment of cell structural and functional changes induced by acetic acid in the yeasts Zygosaccharomyces bailii and Saccharomyces cerevisiae. Cytometry 31: 307–313.
[30]  Klose C, Surma MA, Gerl MJ, Meyenhofer F, Shevchenko A, et al.. (2012) Flexibility of a eukaryotic lipidome - insights from yeast lipidomics. PLoS ONE 7.
[31]  Guan XL, Wenk MR (2006) Mass spectrometry-based profiling of phospholipids and sphingolipids in extracts from Saccharomyces cerevisiae. Yeast 23: 465–477.
[32]  Pilkington BJ, Rose AH (1989) Accumulation of sulphite by Saccharomyces cerevisiae and Zygosaccharomyces bailii as affected by phospholipid fatty-acyl unsaturation and chain length. Journal of General Microbiology 135: 2423–2428.
[33]  Patton JL, Lester RL (1991) The phosphoinositol sphingolipids of Saccharomyces cerevisiae are highly localized in the plasma membrane. Journal of Bacteriology 173: 3101–3108.
[34]  Van der Rest ME, Kamminga AH, Nakano A, Anraku Y, Poolman B, et al. (1995) The plasma membrane of Saccharomyces cerevisiae: Structure, function, and biogenesis. Microbiological Reviews 59: 304–322.
[35]  Ejsing CS, Sampaio JL, Surendranath V, Duchoslav E, Ekroos K, et al. (2009) Global analysis of the yeast lipidome by quantitative shotgun mass spectrometry. Proceedings of the National Academy of Sciences of the United States of America 106: 2136–2141.
[36]  Navas-Iglesias N, Carrasco-Pancorbo A, Cuadros-Rodríguez L (2009) From lipids analysis towards lipidomics, a new challenge for the analytical chemistry of the 21st century. Part II: Analytical lipidomics. TrAC - Trends in Analytical Chemistry 28: 393–403.
[37]  Sonntag D (1990) Important new values of the physical constants of 1986, vapor pressure formulations based on ITS-90 and phychrometer formulae. Zeitschrift für Meteorologie 40: 340–344.
[38]  Villadsen J, Nielsen J, Lidén G (2011) Bioreaction Engineering Principles. Third Edition. Springer Science+Business Media: 74.
[39]  Guan XL, Riezman I, Wenk MR, Riezman H (2010) Yeast lipid analysis and quantification by mass spectrometry. 369–391.
[40]  Vilela-Moura A, Schuller D, Mendes-Faia A, C?rte-Real M (2008) Reduction of volatile acidity of wines by selected yeast strains. Applied Microbiology and Biotechnology 80: 881–890.
[41]  Dos Santos MM, Gombert AK, Christensen B, Olsson L, Nielsen J (2003) Identification of in vivo enzyme activities in the cometabolism of glucose and acetate by Saccharomyces cerevisiae by using 13C-labeled substrates. Eukaryotic Cell 2: 599–608.
[42]  Fernandas L, C?rte-Real M, Loureiro V, Loureiro-Dias MC, Le?o C (1997) Glucose respiration and fermentation in Zygosaccharomyces bailii and Saccharomyces cerevisiae express different sensitivity patterns to ethanol and acetic acid. Letters in Applied Microbiology 25: 249–253.
[43]  Sousa MJ, Rodrigues F, C?rte-Real M, Leaˇo C (1998) Mechanisms underlying the transport and intracellular metabolism of acetic acid in the presence of glucose in the yeast Zygosaccharomyces bailii. Microbiology 144: 665–670.
[44]  Merico A, Capitanio D, Vigentini I, Ranzi BM, Compagno C (2003) Aerobic sugar metabolism in the spoilage yeast Zygosaccharomyces bailii. FEMS Yeast Research 4: 277–283.
[45]  Van Meer G, Voelker DR, Feigenson GW (2008) Membrane lipids: Where they are and how they behave. Nature Reviews Molecular Cell Biology 9: 112–124.
[46]  Martin CE, Oh CS, Jiang Y (2007) Regulation of long chain unsaturated fatty acid synthesis in yeast. Biochimica et Biophysica Acta - Molecular and Cell Biology of Lipids 1771: 271–285.
[47]  Simons K, Sampaio JL (2011) Membrane organization and lipid rafts. Cold Spring Harbor Perspectives in Biology 3: 1–17.
[48]  Russell NJ (1995) Membranes as a target for stress adaptation. International Journal of Food Microbiology 28: 255–261.
[49]  Liu J, Zhu Y, Du G, Zhou J, Chen J (2013) Exogenous ergosterol protects Saccharomyces cerevisiae from d-limonene stress. Journal of Applied Microbiology 114: 482–491.
[50]  Turk M, Méjanelle L, ?entjurc M, Grimalt JO, Gunde-Cimerman N, et al. (2004) Salt-induced changes in lipid composition and membrane fluidity of halophilic yeast-like melanized fungi. Extremophiles 8: 53–61.
[51]  Mannazzu I, Angelozzi D, Belviso S, Budroni M, Farris GA, et al. (2008) Behaviour of Saccharomyces cerevisiae wine strains during adaptation to unfavourable conditions of fermentation on synthetic medium: Cell lipid composition, membrane integrity, viability and fermentative activity. International Journal of Food Microbiology 121: 84–91.
[52]  Mira NP, Palma M, Guerreiro JF, Sá-Correia I (2010) Genome-wide identification of Saccharomyces cerevisiae genes required for tolerance to acetic acid. Microbial Cell Factories 9.
[53]  Kawahata M, Masaki K, Fujii T, Iefuji H (2006) Yeast genes involved in response to lactic acid and acetic acid: Acidic conditions caused by the organic acids in Saccharomyces cerevisiae cultures induce expression of intracellular metal metabolism genes regulated by Aft1p. FEMS Yeast Research 6: 924–936.
[54]  Narendranath NV, Thomas KC, Ingledew WM (2001) Acetic acid and lactic acid inhibition of growth of Saccharomyces cerevisiae by different mechanisms. Journal of the American Society of Brewing Chemists 59: 187–194.
[55]  Xia JM, Yuan YJ (2009) Comparative lipidomics of four strains of Saccharomyces cerevisiae reveals different responses to furfural, phenol, and acetic acid. Journal of Agricultural and Food Chemistry 57: 99–108.
[56]  Yang J, Ding MZ, Li BZ, Liu ZL, Wang X, et al. (2012) Integrated phospholipidomics and transcriptomics analysis of Saccharomyces cerevisiae with enhanced tolerance to a mixture of acetic acid, furfural, and phenol. OMICS A Journal of Integrative Biology 16: 374–386.
[57]  Nezil FA, Bloom M (1992) Combined influence of cholesterol and synthetic amphiphillic peptides upon bilayer thickness in model membranes. Biophysical Journal 61: 1176–1183.
[58]  Alexandre H, Rousseaux I, Charpentier C (1994) Relationship between ethanol tolerance, lipid composition and plasma membrane fluidity in Saccharomyces cerevisiae and Kloeckera apiculata. FEMS Microbiology Letters 124: 17–22.
[59]  Dupont S, Beney L, Ferreira T, Gervais P (2011) Nature of sterols affects plasma membrane behavior and yeast survival during dehydration. Biochimica et Biophysica Acta - Biomembranes 1808: 1520–1528.
[60]  Guan XL, Souza CM, Pichler H, Dewhurst G, Schaad O, et al. (2009) Functional interactions between sphingolipids and sterols in biological membranes regulating cell physiology. Molecular Biology of the Cell 20: 2083–2095.
[61]  Levine TP, Wiggins CAR, Munro S (2000) Inositol phosphorylceramide synthase is located in the Golgi apparatus of Saccharomyces cerevisiae. Molecular Biology of the Cell 11: 2267–2281.
[62]  Simons K, Ikonen E (1997) Functional rafts in cell membranes. Nature 387: 569–572.
[63]  Patton JL, Lester RL (1992) Phosphatidylinositol phosphate, phosphatidylinositol bisphosphate, and the phosphoinositol sphingolipids are found in the plasma membrane and stimulate the plasma membrane H+-ATPase of Saccharomyces cerevisiae. Archives of Biochemistry and Biophysics 292: 70–76.
[64]  Wang Q, Chang A (2002) Sphingoid base synthesis is required for oligomerization and cell surface stability of the yeast plasma membrane ATPase, Pma1. Proceedings of the National Academy of Sciences of the United States of America 99: 12853–12858.
[65]  Lee AG (2011) Biological membranes: The importance of molecular detail. Trends in Biochemical Sciences 36: 493–500.

Full-Text

Contact Us

service@oalib.com

QQ:3279437679

WhatsApp +8615387084133