Proteomic Analysis of Erythritol-Producing Yarrowia lipolytica from Glycerol in Response to Osmotic Pressure

Li-Bo  Yang; Xiao-Meng  Dai; Zhi-Yong  Zheng; Li  Zhu; Xiao-Bei  Zhan; Chi-Chung  Lin

doi:10.4014/jmb.1412.12026

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Research article

Biocatalysis and Fermentation Technology

Proteomic Analysis of Erythritol-Producing Yarrowia lipolytica from Glycerol in Response to Osmotic Pressure

Li-Bo Yang ¹, Xiao-Meng Dai ¹, Zhi-Yong Zheng ¹, Li Zhu ², Xiao-Bei Zhan ^1* and Chi-Chung Lin ¹

¹Key Laboratory of Carbohydrate Chemistry and Biotechnology of Ministry of Education, School of Biotechnology, Jiangnan University, Wuxi, Jiangsu 214122, P.R. China, ²Jiangsu Rayguang Biotechnology Co., Ltd., Wuxi, Jiangsu 214125, P.R. China

Received: December 10, 2014; Accepted: March 1, 2015

J. Microbiol. Biotechnol. 2015; 25(7): 1056-1069

Published July 28, 2015 https://doi.org/10.4014/jmb.1412.12026

Abstract

Osmotic pressure is a critical factor for erythritol production with osmophilic yeast. Protein expression patterns of an erythritol-producing yeast, Yarrowia lipolytica, were analyzed to identify differentially-expressed proteins in response to osmotic pressure. In order to analyze intracellular protein levels quantitatively, two-dimensional gel electrophoresis was performed to separate and visualize the differential expression of the intracellular proteins extracted from Y. lipolytica cultured under low (3.17 osmol/kg) and high (4.21 osmol/kg) osmotic pressures. Proteomic analyses allowed identification of 54 differentially-expressed proteins among the proteins distributed in the range of pI 3-10 and 14.4-97.4 kDa molecular mass between the osmotic stress conditions. Remarkably, the main proteins were involved in the pathway of energy, metabolism, cell rescue, and stress response. The expression of such enzymes related to protein and nucleotide biosynthesis was inhibited drastically, reflecting the growth arrest of Y. lipolytica under hyperosmotic stress. The improvement of erythritol production under high osmotic stress was due to the significant induction of a range of crucial enzymes related to polyols biosynthesis, such as transketolase and triosephosphate isomerase, and the osmotic stress responsive proteins like pyridoxine-4-dehydrogenase and the AKRs family. The polyols biosynthesis was really related to an osmotic response and a protection mechanism against hyperosmotic stress in Y. lipolytica. Additionally, the high osmotic stress could also induce other cell stress responses as with heat shock and oxidation stress responses, and these responsive proteins, such as the HSPs family, catalase T, and superoxide dismutase, also had drastically increased expression levels under hyperosmotic pressure.

Keywords

Yarrowia lipolytica, Osmotic stress response, Proteomics, Erythritol

References

Auesukaree C, Damnernsawad A, Kruatrachue M, Pokethitiyook P, B oonchird C, K aneko Y , Harashim a S. 2 009. G enom ewide identification of genes involved in tolerance to various environmental stresses in Saccharomyces cerevisiae. J. Appl. Genet. 50: 301-310.
Blom N, Sicheritz-Ponten T, Gupta R, Gammeltoft S, Brunak S. 2004. Prediction of post-translational glycosylation and phosphorylation of proteins from the amino acid sequence. Proteomics 4: 1633-1649.
Blomberg A, Adler L. 1992. Physiology of osmotolerance in fungi. Adv. Microb. Physiol. 33: 145.
Boubekeur S, Bunoust O, Camougrand N, Castroviejo M, Rigoulet M, Guerin B. 1999. A mitochondrial pyruvate dehydrogenase bypass in the yeast Saccharomyces cerevisiae. J. Biol. Chem. 274: 21044-21048.
Bukau B, Weissman J, Horwich A. 2006. Molecular chaperones and protein quality control. Cell 125: 443-451.
Candiano G, Bruschi M, Musante L, Santucci L, Ghiggeri GM, Carnemolla B, et al. 2004. Blue silver: a very sensitive colloidal Coomassie G-250 staining for proteome analysis. Electrophoresis 25: 1327-1333.
Chang Q, Griest TA, Harter TM, Petrash JM. 2007. Functional studies of aldo-keto reductases in Saccharomyces cerevisiae. BBA Mol. Cell Res. 1773: 321-329.
Chang Q, Petrash JM. 2008. Disruption of aldo-keto reductase genes leads to elevated markers of oxidative stress and inositol auxotrophy in Saccharomyces cerevisiae. BBA Mol. Cell Res. 1783: 237-245.
Cohen R, Holland JP, Yokoi T, Holland MJ. 1986. Identification of a regulatory region that mediates glucosedependent induction of the Saccharomyces cerevisiae enolase gene ENO2. Mol. Cell. Biol. 6: 2287-2297.
Compagno C, Boschi F, Ranzi BM. 1996. Glycerol production in a triose phosphate isomerase-deficient mutant of Saccharomyces cerevisiae. Biotechnol. Progr. 12: 591-595.
Cossins EA. 1980. One-carbon metabolism, pp. 365-418. The Biochemistry of Plants, Vol II. Academic Press, New York.
Craig EA, Kramer J, Kosic-Smithers J. 1987. SSC1, a member of the 70-kDa heat shock protein multigene family of Saccharomyces cerevisiae, is essential for growth. Proc. Natl. Acad. Sci. USA 84: 4156-4160.
De Nobel H, Lawrie L, Brul S, Klis F, Davis M, Alloush H, Coote P. 2001. Parallel and comparative analysis of the proteome and transcriptome of sorbic acid-stressed Saccharomyces cerevisiae. Yeast 18: 1413-1428.
Dickson RC, Sumanasekera C, Lester RL. 2006. Functions and metabolism of sphingolipids in Saccharomyces cerevisiae. Prog. Lipid Res. 45: 447-465.
Dihazi H, Asif AR, Agarwal NK, Doncheva Y, Müller GA. 2005. Proteomic analysis of cellular response to osmotic stress in thick ascending limb of Henle’s loop (TALH) cells. Mol. Cell. Proteomics 4: 1445-1458.
Dragosits M, Stadlmann J, Graf A, Gasser B, Maurer M, Sauer M, et al. 2010. The response to unfolded protein is involved in osmotolerance of Pichia pastoris. BMC Genomics 11: 207.
Ellis EM. 2002. Microbial aldo-keto reductases. FEMS Microbiol. Lett. 216: 123-131.
Fazius F, Shelest E, Gebhardt P, Brock M. 2012. The fungal α-aminoadipate pathway for lysine biosynthesis requires two enzymes of the aconitase family for the isomerization of homocitrate to homoisocitrate. Mol. Microbiol. 86: 1508-1530.
Garay-Arroyo A, Covarrubias AA. 1999. Three genes whose expression is induced by stress in Saccharomyces cerevisiae. Yeast 15: 879-892.
Hernandez R, Nombela C, Diez-Orejas R, Gil C. 2004. Twodimensional reference map of Candida albicans hyphal forms. Proteomics 4: 374-382.
Hilt W, Wolf DH. 1992. Stress-induced proteolysis in yeast. Mol. Microbiol. 6: 2437-2442.22. Hirasawa T, Yamada K, Nagahisa K, Dinh TN, Furusawa C, Katakura Y, et al. 2009. Proteomic analysis of responses to osmotic stress in laboratory and sake-brewing strains of Saccharomyces cerevisiae. Process. Biochem. 44: 647-653.
Hohmann S. 2002. Osmotic stress signaling and osmoadaptation in yeasts. Microbiol. Mol. Biol. Rev. 66: 300-372.
Hourton-Cabassa C, Ambard-Bretteville F, Moreau F, de Virville JD, Remy R, des Francs-Small CC. 1998. Stress induction of mitochondrial formate dehydrogenase in potato leaves. Plant Physiol. 116: 627-635.
Jin Z, Mu Y-W, Sun J-Y, Li X-M, Gao X-L, Lu J. 2012. Proteome analysis of metabolic proteins (pI 4-7) in barley (Hordeum vulgare) malts and initial application in malt quality discrimination. J. Agric. Food Chem. 61: 402-409.
Kim HJ, Lee H-R, Kim CS, Jin Y-S, Seo J-H. 2013. Investigation of protein expression profiles of erythritolproducing Candida magnoliae in response to glucose perturbation. Enzyme Microb. Technol. 53: 174-180.
Kim SI, Choi HK, Kim JH, Lee HS, Hong SS. 2001. Effect of osmotic pressure on paclitaxel production in suspension cell cultures of Taxus chinensis. Enzyme Microb. Technol. 28: 202-209.
Krantz M, Nordlander B, Valadi H, Johansson M, Gustafsson L, Hohmann S. 2004. Anaerobicity prepares Saccharomyces cerevisiae cells for faster adaptation to osmotic shock. Eukaryot. Cell 3: 1381-1390.
Lahav R, Nejidat A, Abeliovich A. 2004. Alterations in protein synthesis and levels of heat shock 70 proteins in response to salt stress of the halotolerant yeast Rhodotorula mucilaginosa. Antonie Van Leeuwenhoek 85: 259-269.
Larsson C, Gustafsson L. 1987. Glycerol production in relation to the ATP pool and heat production rate of the yeasts Debaryomyces hansenii and Saccharomyces cerevisiae during salt stress. Arch. Microbiol. 147: 358-363.
Li Z, Li Z. 2012. Glucose regulated protein 78: a critical link between tumor microenvironment and cancer hallmarks. BBA Rev. Cancer 1826: 13-22.
Mager WH, de Boer AH, Siderius MH, Voss H-P. 2000. Cellular responses to oxidative and osmotic stress. Cell Stress Chaperones 5: 73.
Mann M, Jensen ON. 2003. Proteomic analysis of posttranslational modifications. Nat. Biotechnol. 21: 255-261.
Mansour S, Bailly J, Delettre J, Bonnarme P. 2009. A proteomic and transcriptomic view of amino acids catabolism in the yeast Yarrowia lipolytica. Proteomics 9: 4714-4725.
Masselot M, de Robichon-Szulmajster H. 1975. Methionine biosynthesis in Saccharomyces cerevisiae. Mol. Gen. Genet. 139:121-132.
Miyagi H, Kawai S, Murata K. 2009. Two sources of mitochondrial NADPH in the yeast Saccharomyces cerevisiae. J. Biol. Chem. 284: 7553-7560.
Moon HJ, Jeya M, Kim IW, Lee JK. 2010. Biotechnological production of erythritol and its applications. Appl. Microbiol. Biotechnol. 86: 1017-1025.
Morano KA, Grant CM, Moye-Rowley WS. 2012. The response to heat shock and oxidative stress in Saccharomyces cerevisiae. Genetics 190: 1157-1195.
Morin M, Monteoliva L, Insenser M, Gil C, Dominguez A. 2007. Proteomic analysis reveals metabolic changes during yeast to hypha transition in Yarrowia lipolytica. J. Mass Spectrom. 42: 1453-1462.
Moriyama T, Garcia-Perez A, Burg M. 1989. Osmotic regulation of aldose reductase protein synthesis in renal medullary cells. J. Biol. Chem. 264: 16810-16814.
Norregaard Jensen O. 2004. Modification-specific proteomics:characterization of post-translational modifications by mass spectrometry. Curr. Opin. Chem. Biol. 8: 33-41.
Nicolet CM, Craig EA. 1989. Isolation and characterization of STI1, a stress-inducible gene from Saccharomyces cerevisiae. Mol. Cell. Biol. 9: 3638-3646.
Norbeck J, Blomberg A. 1997. Metabolic and regulatory changes associated with growth of Saccharomyces cerevisiae in 1.4 M NaCl - Evidence for osmotic induction of glycerol dissimilation via the dihydroxyacetone pathway. J. Biol. Chem. 272: 5544-5554.
Perez-Torrado R, Bruno-Barcena JM, Matallana E. 2005. Monitoring stress-related genes during the process of biomass propagation of Saccharomyces cerevisiae strains used for wine making. Appl. Environ. Microbiol. 71: 6831-6837.
Rep M , Krantz M , Thevelein J M, H ohm ann S. 2 000. T he transcriptional response of Saccharomyces cerevisiae to osmotic shock. Hot1p and Msn2p/Msn4p are required for the induction of subsets of high osmolarity glycerol pathwaydependent genes. J. Biol. Chem. 275: 8290-8300.
Rose MD, Misra LM, Vogel JP. 1989. KAR2, a karyogamy gene, is the yeast homolog of the mammalian BiP/GRP78 gene. Cell 57: 1211-1221.
Rymowicz W, Rywinska A, Marcinkiewicz M. 2009. Highyield production of erythritol from raw glycerol in fed-batch cultures of Yarrowia lipolytica. Biotechnol. Lett. 31: 377-380.
Rywinska A, Juszczyk P, Wojtatowicz M, Robak M, Lazar Z, Tomaszewska L, Rymowicz W. 2013. Glycerol as a promising substrate for Yarrowia lipolytica biotechnological applications. Biomass Bioenerg. 48: 148-166.
Sawada K, Taki A, Yamakawa T, Seki M. 2009. Key role for transketolase activity in erythritol production by Trichosporonoides megachiliensis SN-G42. J. Biosci. Bioeng. 108: 385-390.
Schneider R, Brors B, Burger F, Camrath S, Weiss H. 1997. Two genes of the putative mitochondrial fatty acid synthase in the genome of Saccharomyces cerevisiae. Curr. Genet. 32:384-388.
Teichert U, Mechler B, Müller H, Wolf D. 1989. Lysosomal (vacuolar) proteinases of yeast are essential catalysts for protein degradation, differentiation, and cell survival. J. Biol. Chem. 264: 16037-16045.
Tomaszewska L, Rywinska A, Gladkowski W. 2012. Production of erythritol and mannitol by Yarrowia lipolyticayeast in media containing glycerol. J. Ind. Microbiol. Biotechnol. 39: 1333-1343.
Varela J, Praekelt UM, Meacock PA, Planta RJ, Mager WH. 1995. The Saccharomyces cerevisiae HSP12 gene is activated by the high-osmolarity glycerol pathway and negatively regulated by protein kinase A. Mol. Cell. Biol. 15: 6232-6245.
Weber A, Kogl SA, Jung K. 2006. Time-dependent proteome alterations under osmotic stress during aerobic and anaerobic growth in Escherichia coli. J. Bacteriol. 188: 7165-7175.
Wong C-M, Siu K-L, Jin D-Y. 2004. Peroxiredoxin-null yeast cells are hypersensitive to oxidative stress and are genomically unstable. J. Biol. Chem. 279: 23207-23213.
Wucherpfennig T, Hestler T, Krull R. 2011. Morphology engineering - osmolality and its effect on Aspergillus niger morphology and productivity. Microb. Cell Fact. 10: 58.
Xu S, Zhou J, Liu L, Chen J. 2011. Arginine: a novel compatible solute to protect Candida glabrata against hyperosmotic stress. Process Biochem. 46: 1230-1235.
Yan S, Tang Z, Su W, Sun W. 2005. Proteomic analysis of salt stress-responsive proteins in rice root. Proteomics 5: 235-244.
Yancey PH. 2005. Organic osmolytes as compatible, metabolic and counteracting cytoprotectants in high osmolarity and other stresses. J. Exp. Biol. 208: 2819-2830.
Yang L-B, Zhan X-B, Zheng Z-Y, Wu J-R, Gao M-J, Lin C-C. 2014. A novel osmotic pressure control fed-batch fermentation strategy for improvement of erythritol production by Yarrowia lipolytica from glycerol. Bioresour. Technol. 151: 120-127.
Zhang X, Lester RL, Dickson RC. 2004. Pil1p and Lsp1p negatively regulate the 3-phosphoinositide-dependent protein kinase-like kinase Pkh1p and downstream signaling pathways Pkc1p and Ypk1p. J. Biol. Chem. 279: 22030-22038.

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Article

Research article

J. Microbiol. Biotechnol. 2015; 25(7): 1056-1069

Published online July 28, 2015 https://doi.org/10.4014/jmb.1412.12026

Proteomic Analysis of Erythritol-Producing Yarrowia lipolytica from Glycerol in Response to Osmotic Pressure

Li-Bo Yang ¹, Xiao-Meng Dai ¹, Zhi-Yong Zheng ¹, Li Zhu ², Xiao-Bei Zhan ^1* and Chi-Chung Lin ¹

¹Key Laboratory of Carbohydrate Chemistry and Biotechnology of Ministry of Education, School of Biotechnology, Jiangnan University, Wuxi, Jiangsu 214122, P.R. China, ²Jiangsu Rayguang Biotechnology Co., Ltd., Wuxi, Jiangsu 214125, P.R. China

Received: December 10, 2014; Accepted: March 1, 2015

Abstract

Osmotic pressure is a critical factor for erythritol production with osmophilic yeast. Protein
expression patterns of an erythritol-producing yeast, Yarrowia lipolytica, were analyzed to
identify differentially-expressed proteins in response to osmotic pressure. In order to analyze
intracellular protein levels quantitatively, two-dimensional gel electrophoresis was performed
to separate and visualize the differential expression of the intracellular proteins extracted from
Y. lipolytica cultured under low (3.17 osmol/kg) and high (4.21 osmol/kg) osmotic pressures.
Proteomic analyses allowed identification of 54 differentially-expressed proteins among the
proteins distributed in the range of pI 3-10 and 14.4-97.4 kDa molecular mass between the
osmotic stress conditions. Remarkably, the main proteins were involved in the pathway of
energy, metabolism, cell rescue, and stress response. The expression of such enzymes related
to protein and nucleotide biosynthesis was inhibited drastically, reflecting the growth arrest of
Y. lipolytica under hyperosmotic stress. The improvement of erythritol production under high
osmotic stress was due to the significant induction of a range of crucial enzymes related to
polyols biosynthesis, such as transketolase and triosephosphate isomerase, and the osmotic
stress responsive proteins like pyridoxine-4-dehydrogenase and the AKRs family. The polyols
biosynthesis was really related to an osmotic response and a protection mechanism against
hyperosmotic stress in Y. lipolytica. Additionally, the high osmotic stress could also induce
other cell stress responses as with heat shock and oxidation stress responses, and these
responsive proteins, such as the HSPs family, catalase T, and superoxide dismutase, also had
drastically increased expression levels under hyperosmotic pressure.

Keywords: Yarrowia lipolytica, Osmotic stress response, Proteomics, Erythritol

Abstract

References

Auesukaree C, Damnernsawad A, Kruatrachue M, Pokethitiyook P, B oonchird C, K aneko Y , Harashim a S. 2 009. G enom ewide identification of genes involved in tolerance to various environmental stresses in Saccharomyces cerevisiae. J. Appl. Genet. 50: 301-310.
Blom N, Sicheritz-Ponten T, Gupta R, Gammeltoft S, Brunak S. 2004. Prediction of post-translational glycosylation and phosphorylation of proteins from the amino acid sequence. Proteomics 4: 1633-1649.
Blomberg A, Adler L. 1992. Physiology of osmotolerance in fungi. Adv. Microb. Physiol. 33: 145.
Boubekeur S, Bunoust O, Camougrand N, Castroviejo M, Rigoulet M, Guerin B. 1999. A mitochondrial pyruvate dehydrogenase bypass in the yeast Saccharomyces cerevisiae. J. Biol. Chem. 274: 21044-21048.
Bukau B, Weissman J, Horwich A. 2006. Molecular chaperones and protein quality control. Cell 125: 443-451.
Candiano G, Bruschi M, Musante L, Santucci L, Ghiggeri GM, Carnemolla B, et al. 2004. Blue silver: a very sensitive colloidal Coomassie G-250 staining for proteome analysis. Electrophoresis 25: 1327-1333.
Chang Q, Griest TA, Harter TM, Petrash JM. 2007. Functional studies of aldo-keto reductases in Saccharomyces cerevisiae. BBA Mol. Cell Res. 1773: 321-329.
Chang Q, Petrash JM. 2008. Disruption of aldo-keto reductase genes leads to elevated markers of oxidative stress and inositol auxotrophy in Saccharomyces cerevisiae. BBA Mol. Cell Res. 1783: 237-245.
Cohen R, Holland JP, Yokoi T, Holland MJ. 1986. Identification of a regulatory region that mediates glucosedependent induction of the Saccharomyces cerevisiae enolase gene ENO2. Mol. Cell. Biol. 6: 2287-2297.
Compagno C, Boschi F, Ranzi BM. 1996. Glycerol production in a triose phosphate isomerase-deficient mutant of Saccharomyces cerevisiae. Biotechnol. Progr. 12: 591-595.
Cossins EA. 1980. One-carbon metabolism, pp. 365-418. The Biochemistry of Plants, Vol II. Academic Press, New York.
Craig EA, Kramer J, Kosic-Smithers J. 1987. SSC1, a member of the 70-kDa heat shock protein multigene family of Saccharomyces cerevisiae, is essential for growth. Proc. Natl. Acad. Sci. USA 84: 4156-4160.
De Nobel H, Lawrie L, Brul S, Klis F, Davis M, Alloush H, Coote P. 2001. Parallel and comparative analysis of the proteome and transcriptome of sorbic acid-stressed Saccharomyces cerevisiae. Yeast 18: 1413-1428.
Dickson RC, Sumanasekera C, Lester RL. 2006. Functions and metabolism of sphingolipids in Saccharomyces cerevisiae. Prog. Lipid Res. 45: 447-465.
Dihazi H, Asif AR, Agarwal NK, Doncheva Y, Müller GA. 2005. Proteomic analysis of cellular response to osmotic stress in thick ascending limb of Henle’s loop (TALH) cells. Mol. Cell. Proteomics 4: 1445-1458.
Dragosits M, Stadlmann J, Graf A, Gasser B, Maurer M, Sauer M, et al. 2010. The response to unfolded protein is involved in osmotolerance of Pichia pastoris. BMC Genomics 11: 207.
Ellis EM. 2002. Microbial aldo-keto reductases. FEMS Microbiol. Lett. 216: 123-131.
Fazius F, Shelest E, Gebhardt P, Brock M. 2012. The fungal α-aminoadipate pathway for lysine biosynthesis requires two enzymes of the aconitase family for the isomerization of homocitrate to homoisocitrate. Mol. Microbiol. 86: 1508-1530.
Garay-Arroyo A, Covarrubias AA. 1999. Three genes whose expression is induced by stress in Saccharomyces cerevisiae. Yeast 15: 879-892.
Hernandez R, Nombela C, Diez-Orejas R, Gil C. 2004. Twodimensional reference map of Candida albicans hyphal forms. Proteomics 4: 374-382.
Hilt W, Wolf DH. 1992. Stress-induced proteolysis in yeast. Mol. Microbiol. 6: 2437-2442.22. Hirasawa T, Yamada K, Nagahisa K, Dinh TN, Furusawa C, Katakura Y, et al. 2009. Proteomic analysis of responses to osmotic stress in laboratory and sake-brewing strains of Saccharomyces cerevisiae. Process. Biochem. 44: 647-653.
Hohmann S. 2002. Osmotic stress signaling and osmoadaptation in yeasts. Microbiol. Mol. Biol. Rev. 66: 300-372.
Hourton-Cabassa C, Ambard-Bretteville F, Moreau F, de Virville JD, Remy R, des Francs-Small CC. 1998. Stress induction of mitochondrial formate dehydrogenase in potato leaves. Plant Physiol. 116: 627-635.
Jin Z, Mu Y-W, Sun J-Y, Li X-M, Gao X-L, Lu J. 2012. Proteome analysis of metabolic proteins (pI 4-7) in barley (Hordeum vulgare) malts and initial application in malt quality discrimination. J. Agric. Food Chem. 61: 402-409.
Kim HJ, Lee H-R, Kim CS, Jin Y-S, Seo J-H. 2013. Investigation of protein expression profiles of erythritolproducing Candida magnoliae in response to glucose perturbation. Enzyme Microb. Technol. 53: 174-180.
Kim SI, Choi HK, Kim JH, Lee HS, Hong SS. 2001. Effect of osmotic pressure on paclitaxel production in suspension cell cultures of Taxus chinensis. Enzyme Microb. Technol. 28: 202-209.
Krantz M, Nordlander B, Valadi H, Johansson M, Gustafsson L, Hohmann S. 2004. Anaerobicity prepares Saccharomyces cerevisiae cells for faster adaptation to osmotic shock. Eukaryot. Cell 3: 1381-1390.
Lahav R, Nejidat A, Abeliovich A. 2004. Alterations in protein synthesis and levels of heat shock 70 proteins in response to salt stress of the halotolerant yeast Rhodotorula mucilaginosa. Antonie Van Leeuwenhoek 85: 259-269.
Larsson C, Gustafsson L. 1987. Glycerol production in relation to the ATP pool and heat production rate of the yeasts Debaryomyces hansenii and Saccharomyces cerevisiae during salt stress. Arch. Microbiol. 147: 358-363.
Li Z, Li Z. 2012. Glucose regulated protein 78: a critical link between tumor microenvironment and cancer hallmarks. BBA Rev. Cancer 1826: 13-22.
Mager WH, de Boer AH, Siderius MH, Voss H-P. 2000. Cellular responses to oxidative and osmotic stress. Cell Stress Chaperones 5: 73.
Mann M, Jensen ON. 2003. Proteomic analysis of posttranslational modifications. Nat. Biotechnol. 21: 255-261.
Mansour S, Bailly J, Delettre J, Bonnarme P. 2009. A proteomic and transcriptomic view of amino acids catabolism in the yeast Yarrowia lipolytica. Proteomics 9: 4714-4725.
Masselot M, de Robichon-Szulmajster H. 1975. Methionine biosynthesis in Saccharomyces cerevisiae. Mol. Gen. Genet. 139:121-132.
Miyagi H, Kawai S, Murata K. 2009. Two sources of mitochondrial NADPH in the yeast Saccharomyces cerevisiae. J. Biol. Chem. 284: 7553-7560.
Moon HJ, Jeya M, Kim IW, Lee JK. 2010. Biotechnological production of erythritol and its applications. Appl. Microbiol. Biotechnol. 86: 1017-1025.
Morano KA, Grant CM, Moye-Rowley WS. 2012. The response to heat shock and oxidative stress in Saccharomyces cerevisiae. Genetics 190: 1157-1195.
Morin M, Monteoliva L, Insenser M, Gil C, Dominguez A. 2007. Proteomic analysis reveals metabolic changes during yeast to hypha transition in Yarrowia lipolytica. J. Mass Spectrom. 42: 1453-1462.
Moriyama T, Garcia-Perez A, Burg M. 1989. Osmotic regulation of aldose reductase protein synthesis in renal medullary cells. J. Biol. Chem. 264: 16810-16814.
Norregaard Jensen O. 2004. Modification-specific proteomics:characterization of post-translational modifications by mass spectrometry. Curr. Opin. Chem. Biol. 8: 33-41.
Nicolet CM, Craig EA. 1989. Isolation and characterization of STI1, a stress-inducible gene from Saccharomyces cerevisiae. Mol. Cell. Biol. 9: 3638-3646.
Norbeck J, Blomberg A. 1997. Metabolic and regulatory changes associated with growth of Saccharomyces cerevisiae in 1.4 M NaCl - Evidence for osmotic induction of glycerol dissimilation via the dihydroxyacetone pathway. J. Biol. Chem. 272: 5544-5554.
Perez-Torrado R, Bruno-Barcena JM, Matallana E. 2005. Monitoring stress-related genes during the process of biomass propagation of Saccharomyces cerevisiae strains used for wine making. Appl. Environ. Microbiol. 71: 6831-6837.
Rep M , Krantz M , Thevelein J M, H ohm ann S. 2 000. T he transcriptional response of Saccharomyces cerevisiae to osmotic shock. Hot1p and Msn2p/Msn4p are required for the induction of subsets of high osmolarity glycerol pathwaydependent genes. J. Biol. Chem. 275: 8290-8300.
Rose MD, Misra LM, Vogel JP. 1989. KAR2, a karyogamy gene, is the yeast homolog of the mammalian BiP/GRP78 gene. Cell 57: 1211-1221.
Rymowicz W, Rywinska A, Marcinkiewicz M. 2009. Highyield production of erythritol from raw glycerol in fed-batch cultures of Yarrowia lipolytica. Biotechnol. Lett. 31: 377-380.
Rywinska A, Juszczyk P, Wojtatowicz M, Robak M, Lazar Z, Tomaszewska L, Rymowicz W. 2013. Glycerol as a promising substrate for Yarrowia lipolytica biotechnological applications. Biomass Bioenerg. 48: 148-166.
Sawada K, Taki A, Yamakawa T, Seki M. 2009. Key role for transketolase activity in erythritol production by Trichosporonoides megachiliensis SN-G42. J. Biosci. Bioeng. 108: 385-390.
Schneider R, Brors B, Burger F, Camrath S, Weiss H. 1997. Two genes of the putative mitochondrial fatty acid synthase in the genome of Saccharomyces cerevisiae. Curr. Genet. 32:384-388.
Teichert U, Mechler B, Müller H, Wolf D. 1989. Lysosomal (vacuolar) proteinases of yeast are essential catalysts for protein degradation, differentiation, and cell survival. J. Biol. Chem. 264: 16037-16045.
Tomaszewska L, Rywinska A, Gladkowski W. 2012. Production of erythritol and mannitol by Yarrowia lipolyticayeast in media containing glycerol. J. Ind. Microbiol. Biotechnol. 39: 1333-1343.
Varela J, Praekelt UM, Meacock PA, Planta RJ, Mager WH. 1995. The Saccharomyces cerevisiae HSP12 gene is activated by the high-osmolarity glycerol pathway and negatively regulated by protein kinase A. Mol. Cell. Biol. 15: 6232-6245.
Weber A, Kogl SA, Jung K. 2006. Time-dependent proteome alterations under osmotic stress during aerobic and anaerobic growth in Escherichia coli. J. Bacteriol. 188: 7165-7175.
Wong C-M, Siu K-L, Jin D-Y. 2004. Peroxiredoxin-null yeast cells are hypersensitive to oxidative stress and are genomically unstable. J. Biol. Chem. 279: 23207-23213.
Wucherpfennig T, Hestler T, Krull R. 2011. Morphology engineering - osmolality and its effect on Aspergillus niger morphology and productivity. Microb. Cell Fact. 10: 58.
Xu S, Zhou J, Liu L, Chen J. 2011. Arginine: a novel compatible solute to protect Candida glabrata against hyperosmotic stress. Process Biochem. 46: 1230-1235.
Yan S, Tang Z, Su W, Sun W. 2005. Proteomic analysis of salt stress-responsive proteins in rice root. Proteomics 5: 235-244.
Yancey PH. 2005. Organic osmolytes as compatible, metabolic and counteracting cytoprotectants in high osmolarity and other stresses. J. Exp. Biol. 208: 2819-2830.
Yang L-B, Zhan X-B, Zheng Z-Y, Wu J-R, Gao M-J, Lin C-C. 2014. A novel osmotic pressure control fed-batch fermentation strategy for improvement of erythritol production by Yarrowia lipolytica from glycerol. Bioresour. Technol. 151: 120-127.
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