Genome-Wide Screening of Saccharomyces cerevisiae Genes Regulated by Vanillin

Eun-Hee  Park  and Myoung-Dong  Kim

doi:10.4014/jmb.1409.09064

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Research article

Biocatalysis and Fermentation Technology

Genome-Wide Screening of Saccharomyces cerevisiae Genes Regulated by Vanillin

Eun-Hee Park ¹ and Myoung-Dong Kim ^1*

Department of Food Science and Biotechnology, Kangwon National University, Chuncheon 200-701, Republic of Korea

Received: September 22, 2014; Accepted: September 29, 2014

J. Microbiol. Biotechnol. 2015; 25(1): 50-56

Published January 28, 2015 https://doi.org/10.4014/jmb.1409.09064

Abstract

During pretreatment of lignocellulosic biomass, a variety of fermentation inhibitors, including acetic acid and vanillin, are released. Using DNA microarray analysis, this study explored genes of the budding yeast Saccharomyces cerevisiae that respond to vanillin-induced stress. The expression of 273 genes was upregulated and that of 205 genes was downregulated under vanillin stress. Significantly induced genes included MCH2, SNG1, GPH1, and TMA10, whereas NOP2, UTP18, FUR1, and SPR1 were down regulated. Sequence analysis of the 5’-flanking region of upregulated genes suggested that vanillin might regulate gene expression in a stress response element (STRE)-dependent manner, in addition to a pathway that involved the transcription factor Yap1p. Retardation in the cell growth of mutant strains indicated that MCH2, SNG1, and GPH1 are intimately involved in vanillin stress response. Deletion of the genes whose expression levels were decreased under vanillin stress did not result in a notable change in S. cerevisiae growth under vanillin stress. This study will provide the basis for a better understanding of the stress response of the yeast S. cerevisiae to fermentation inhibitors.

Keywords

Saccharomyces cerevisiae, DNA microarray, Vanillin, Stress response

References

Almeida JRM, Modig T, Petersson A, Hägerdal BH, Lidén G, Grauslund MFG. 2007. Increased tolerance and conversion of inhibitors in lignocellulosic hydrolysates by Saccharomyces cerevisiae. J. Chem. Technol. Biotechnol. 82: 340-349.
Amoros M, Estruch F. 2001. Hsf1p and Msn2/4p cooperate in the expression of Saccharomyces cerevisiae genes HSP26 and HSP104 in a gene- and stress type-dependent manner. Mol. Microbiol. 39: 1523-1532.
Brachmann CB, Davies A, Cost GJ, Caputo E, Li J, Hieter P, Boeke JD. 1998. Designer deletion strains derived from Saccharomyces cerevisiae S288C: a useful set of strains and plasmids for PCR-mediated gene disruption and other applications. Yeast 14: 115-132.
Cerrutti P, Alzamora SM. 1996. Inhibitory effects of vanillin on some food spoilage yeasts in laboratory media and fruit purees. Int. J. Food Microbiol. 29: 379-386.
Cerrutti P, Alzamora SM, Vidales SL. 1997. Vanillin as an antimicrobial for producing shelf-stable strawberry puree. J. Food Sci. 62: 608-610.
Cortez D V, R oberto IC. 2 010. I ndividual a nd interaction effects of vanillin and syringaldehyde on the xylitol formation by Candida guilliermondii. Bioresour. Technol. 101: 1858-1865.
Dunlop AP. 1948. Furfural formation and behavior. Ind. Eng. Chem. 40: 204-209.
Endo A, Nakamura T, Ando A, Tokuyasu K, Shima J. 2008. Genome-wide screening of the genes required for tolerance to vanillin, which is a potential inhibitor of bioethanol fermentation, in Saccharomyces cerevisiae. Biotechnol. Biofuels 1: 3.
Endo A, Nakamura T, Shima J. 2009. Involvement of ergosterol in tolerance to vanillin, a potential inhibitor of bioethanol fermentation, in Saccharomyces cerevisiae. FEMS Microbiol. Lett. 299: 95-99.
Fleischer TC, Weaver CM, McAfee KJ, Jennings JL, Link AJ. 2006. Systematic identification and functional screens of uncharacterized proteins associated with eukaryotic ribosomal complexes. Genes Dev. 20: 1294-1307.
Galbe M, Zacchi G. 2002. A review of the production of ethanol from softwood. Appl. Microbiol. Biotechnol. 59: 618-628.
García-López MC, Mirón-García MC, Garrido-Godino AI, Mingorance C, Navarro F. 2010. Overexpression of SNG1 causes 6-azauracil resistance in Saccharomyces cerevisiae. Curr. Genet. 56: 251-263.
Grey M, Pich CT, Haase E, Brendel M. 1995. SNG1 - a new gene involved in nitrosoguanidine resistance in Saccharomyces cerevisiae. Mutat. Res. 346: 207-214.
Hansen EH, Moller BL, Kock GR, Bunner CM, Kristensen C, Jensen OR, et al. 2009. De novo biosynthesis of vanillin in fission yeast (Schizosaccharomyces pombe) and baker’s yeast (Saccharomyces cerevisiae). Appl. Environ. Microbiol. 75: 2765-2774.
Haslbeck M, Braun N, Stromer T, Richter B, Model N, Weinkauf S, Buchner J. 2004. Hsp42 is the general small heat shock protein in the cytosol of Saccharomyces cerevisiae. EMBO J. 23: 638-649.
Hong B, Wu K, Brockenbrough JS, Wu P, Aris JP. 2001. Temperature sensitive nop2 alleles defective in synthesis of 25S rRNA and large ribosomal subunits in Saccharomyces cerevisiae. Nucleic Acids Res. 29: 2927-2937.
Hubbell E, Liu WM, Mei R. 2002. Robust estimators for expression analysis. Bioinformatics 18: 1585-1592.
Irizarry RA, Bolstad BM, Collin F, Cope LM, Hobbs B, Speed TP. 2003. Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res. 31: 15.
Iwaki A, Ohnuki S, Suga Y, Izawa S, Ohya Y. 2013. Vanillin inhibits translation and induces messenger ribonucleoprotein (mRNP) granule formation in Saccharomyces cerevisiae:application and validation of high-content, image-based profiling. PLoS One 8: e61748.
Klinke HB, Thomsen AB, Ahring BK. 2004. Inhibition of ethanol-producing yeast and bacteria by degradation products produced during pre-treatment of biomass. Appl. Microbiol. Biotechnol. 66: 10-26.
Klionsky DJ, Cregg JM, Dunn WA Jr, Emr SD, Sakai Y, Sandoval IV, et al. 2003. A unified nomenclature for yeast autophagy-related genes. Dev. Cell 5: 539-545.
Kobayashi N, McEntee K. 1993. Identification of cis and trans components of a novel heat shock stress regulatory pathway in Saccharomyces cerevisiae. Mol. Cell Biol. 13: 248-256.
Lin T, Tanaka S. 2006. Ethanol fermentation from biomass resources: current state and prospects. Appl. Microbiol. Biotechnol. 69: 627-642.
López-Malo A, Alzamora SM, Argaiz A. 1995. Effect of natural vanillin on germination time and radial growth of moulds in fruit-based agar systems. Food Microbiol. 12: 213-219.
Mahmud SA, Hirasawa T, Furusawa C, Yoshikawa K, Shimizu H. 2012. Understanding the mechanism of heat stress tolerance caused by high trehalose accumulation in Saccharomyces cerevisiae using DNA microarray. J. Biosci. Bioeng. 113: 526-528.
Makuc J, Paiva S, Schauen M, Krämer R, André B, Casal M, et al. 2001. The putative monocarboxylate permeases of the yeast Saccharomyces cerevisiae do not transport monocarboxylic acids across the plasma membrane. Yeast 18: 1131-1143.
Minique H, Faaij A, vanden Broek R, Berndes G, Gielen D, Turkenburg W. 2003. Exploration of the ranges of the global potential of biomass for energy. Biomass Bioenergy 25: 119-133.
Modig T, Liden G, Taherzadeh MJ. 2002. Inhibition effects of furfural on alcohol dehydrogenase, aldehyde dehydrogenase and pyruvate dehydrogenase. Biochem. J. 363: 769-776.
Mulford KE, Fassler JS. 2011. Association of the Skn7 and Yap1 transcription factors in the Saccharomyces cerevisiae oxidative stress response. Eukaryot. Cell 10: 761-769.
Nguyen TTM, Iwaki A, Ohya Y, Izawa S. 2014. Vanillin cause the activation of Yap1 and mitocondrial fragmentation in Saccharomyces cerevisiae. J. Biosci. Bioeng. 117: 33-38.
Park EH, Lee HY, Ryu YW, Seo JH, Kim MD. 2011. Role of osmotic and salt stress in the expression of erythrose reductase in Candida magnoliae. J. Microbiol. Biotechnol. 21: 1064-1068.
Rivera-Carriles K, Argaiz A, Palou E, Lopez-Malo A. 2005. Synergistic inhibitory effect of citral with selected phenolics against Zygosaccharomyces bailii. J. Food Prot. 68: 602-606.
Srokol Z, Bouche AG, van Estrik A, Strik RC, Maschmeyer T, Peters JA. 2004. Hydrothermal upgrading of biomass to biofuel; studies on some monosaccharide model compounds. Carbohydr. Res. 339: 1717-1726.
Sunnarborg SW, Miller SP, Unnikrishnan I, LaPorte DC. 2001. Expression of the yeast glycogen phosphorylase gene is regulated by stress-response elements and by the HOG MAP kinase pathway. Yeast 18: 1505-1514.
Treger JM, Schmitt AP, Simon JR, McEntee K. 1998. Transcriptional factor mutations reveal regulatory complexities of heat shock and newly identified stress genes in Saccharomyces cerevisiae. J. Biol. Chem. 273: 26875-26879.
Trotter EW, Kao CM, Berenfeld L, Botstein D, Petsko GA, Gray JV. 2002. Misfolded proteins are competent to mediate a subset of the responses to heat shock in Saccharomyces cerevisiae. J. Biol. Chem. 277: 44817-44825.

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Article

Research article

J. Microbiol. Biotechnol. 2015; 25(1): 50-56

Published online January 28, 2015 https://doi.org/10.4014/jmb.1409.09064

Genome-Wide Screening of Saccharomyces cerevisiae Genes Regulated by Vanillin

Eun-Hee Park ¹ and Myoung-Dong Kim ^1*

Department of Food Science and Biotechnology, Kangwon National University, Chuncheon 200-701, Republic of Korea

Received: September 22, 2014; Accepted: September 29, 2014

Abstract

During pretreatment of lignocellulosic biomass, a variety of fermentation inhibitors, including
acetic acid and vanillin, are released. Using DNA microarray analysis, this study explored
genes of the budding yeast Saccharomyces cerevisiae that respond to vanillin-induced stress. The
expression of 273 genes was upregulated and that of 205 genes was downregulated under
vanillin stress. Significantly induced genes included MCH2, SNG1, GPH1, and TMA10, whereas
NOP2, UTP18, FUR1, and SPR1 were down regulated. Sequence analysis of the 5’-flanking
region of upregulated genes suggested that vanillin might regulate gene expression in a stress
response element (STRE)-dependent manner, in addition to a pathway that involved the
transcription factor Yap1p. Retardation in the cell growth of mutant strains indicated that
MCH2, SNG1, and GPH1 are intimately involved in vanillin stress response. Deletion of the
genes whose expression levels were decreased under vanillin stress did not result in a notable
change in S. cerevisiae growth under vanillin stress. This study will provide the basis for a
better understanding of the stress response of the yeast S. cerevisiae to fermentation inhibitors.

Keywords: Saccharomyces cerevisiae, DNA microarray, Vanillin, Stress response

Abstract

References

Almeida JRM, Modig T, Petersson A, Hägerdal BH, Lidén G, Grauslund MFG. 2007. Increased tolerance and conversion of inhibitors in lignocellulosic hydrolysates by Saccharomyces cerevisiae. J. Chem. Technol. Biotechnol. 82: 340-349.
Amoros M, Estruch F. 2001. Hsf1p and Msn2/4p cooperate in the expression of Saccharomyces cerevisiae genes HSP26 and HSP104 in a gene- and stress type-dependent manner. Mol. Microbiol. 39: 1523-1532.
Brachmann CB, Davies A, Cost GJ, Caputo E, Li J, Hieter P, Boeke JD. 1998. Designer deletion strains derived from Saccharomyces cerevisiae S288C: a useful set of strains and plasmids for PCR-mediated gene disruption and other applications. Yeast 14: 115-132.
Cerrutti P, Alzamora SM. 1996. Inhibitory effects of vanillin on some food spoilage yeasts in laboratory media and fruit purees. Int. J. Food Microbiol. 29: 379-386.
Cerrutti P, Alzamora SM, Vidales SL. 1997. Vanillin as an antimicrobial for producing shelf-stable strawberry puree. J. Food Sci. 62: 608-610.
Cortez D V, R oberto IC. 2 010. I ndividual a nd interaction effects of vanillin and syringaldehyde on the xylitol formation by Candida guilliermondii. Bioresour. Technol. 101: 1858-1865.
Dunlop AP. 1948. Furfural formation and behavior. Ind. Eng. Chem. 40: 204-209.
Endo A, Nakamura T, Ando A, Tokuyasu K, Shima J. 2008. Genome-wide screening of the genes required for tolerance to vanillin, which is a potential inhibitor of bioethanol fermentation, in Saccharomyces cerevisiae. Biotechnol. Biofuels 1: 3.
Endo A, Nakamura T, Shima J. 2009. Involvement of ergosterol in tolerance to vanillin, a potential inhibitor of bioethanol fermentation, in Saccharomyces cerevisiae. FEMS Microbiol. Lett. 299: 95-99.
Fleischer TC, Weaver CM, McAfee KJ, Jennings JL, Link AJ. 2006. Systematic identification and functional screens of uncharacterized proteins associated with eukaryotic ribosomal complexes. Genes Dev. 20: 1294-1307.
Galbe M, Zacchi G. 2002. A review of the production of ethanol from softwood. Appl. Microbiol. Biotechnol. 59: 618-628.
García-López MC, Mirón-García MC, Garrido-Godino AI, Mingorance C, Navarro F. 2010. Overexpression of SNG1 causes 6-azauracil resistance in Saccharomyces cerevisiae. Curr. Genet. 56: 251-263.
Grey M, Pich CT, Haase E, Brendel M. 1995. SNG1 - a new gene involved in nitrosoguanidine resistance in Saccharomyces cerevisiae. Mutat. Res. 346: 207-214.
Hansen EH, Moller BL, Kock GR, Bunner CM, Kristensen C, Jensen OR, et al. 2009. De novo biosynthesis of vanillin in fission yeast (Schizosaccharomyces pombe) and baker’s yeast (Saccharomyces cerevisiae). Appl. Environ. Microbiol. 75: 2765-2774.
Haslbeck M, Braun N, Stromer T, Richter B, Model N, Weinkauf S, Buchner J. 2004. Hsp42 is the general small heat shock protein in the cytosol of Saccharomyces cerevisiae. EMBO J. 23: 638-649.
Hong B, Wu K, Brockenbrough JS, Wu P, Aris JP. 2001. Temperature sensitive nop2 alleles defective in synthesis of 25S rRNA and large ribosomal subunits in Saccharomyces cerevisiae. Nucleic Acids Res. 29: 2927-2937.
Hubbell E, Liu WM, Mei R. 2002. Robust estimators for expression analysis. Bioinformatics 18: 1585-1592.
Irizarry RA, Bolstad BM, Collin F, Cope LM, Hobbs B, Speed TP. 2003. Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res. 31: 15.
Iwaki A, Ohnuki S, Suga Y, Izawa S, Ohya Y. 2013. Vanillin inhibits translation and induces messenger ribonucleoprotein (mRNP) granule formation in Saccharomyces cerevisiae:application and validation of high-content, image-based profiling. PLoS One 8: e61748.
Klinke HB, Thomsen AB, Ahring BK. 2004. Inhibition of ethanol-producing yeast and bacteria by degradation products produced during pre-treatment of biomass. Appl. Microbiol. Biotechnol. 66: 10-26.
Klionsky DJ, Cregg JM, Dunn WA Jr, Emr SD, Sakai Y, Sandoval IV, et al. 2003. A unified nomenclature for yeast autophagy-related genes. Dev. Cell 5: 539-545.
Kobayashi N, McEntee K. 1993. Identification of cis and trans components of a novel heat shock stress regulatory pathway in Saccharomyces cerevisiae. Mol. Cell Biol. 13: 248-256.
Lin T, Tanaka S. 2006. Ethanol fermentation from biomass resources: current state and prospects. Appl. Microbiol. Biotechnol. 69: 627-642.
López-Malo A, Alzamora SM, Argaiz A. 1995. Effect of natural vanillin on germination time and radial growth of moulds in fruit-based agar systems. Food Microbiol. 12: 213-219.
Mahmud SA, Hirasawa T, Furusawa C, Yoshikawa K, Shimizu H. 2012. Understanding the mechanism of heat stress tolerance caused by high trehalose accumulation in Saccharomyces cerevisiae using DNA microarray. J. Biosci. Bioeng. 113: 526-528.
Makuc J, Paiva S, Schauen M, Krämer R, André B, Casal M, et al. 2001. The putative monocarboxylate permeases of the yeast Saccharomyces cerevisiae do not transport monocarboxylic acids across the plasma membrane. Yeast 18: 1131-1143.
Minique H, Faaij A, vanden Broek R, Berndes G, Gielen D, Turkenburg W. 2003. Exploration of the ranges of the global potential of biomass for energy. Biomass Bioenergy 25: 119-133.
Modig T, Liden G, Taherzadeh MJ. 2002. Inhibition effects of furfural on alcohol dehydrogenase, aldehyde dehydrogenase and pyruvate dehydrogenase. Biochem. J. 363: 769-776.
Mulford KE, Fassler JS. 2011. Association of the Skn7 and Yap1 transcription factors in the Saccharomyces cerevisiae oxidative stress response. Eukaryot. Cell 10: 761-769.
Nguyen TTM, Iwaki A, Ohya Y, Izawa S. 2014. Vanillin cause the activation of Yap1 and mitocondrial fragmentation in Saccharomyces cerevisiae. J. Biosci. Bioeng. 117: 33-38.
Park EH, Lee HY, Ryu YW, Seo JH, Kim MD. 2011. Role of osmotic and salt stress in the expression of erythrose reductase in Candida magnoliae. J. Microbiol. Biotechnol. 21: 1064-1068.
Rivera-Carriles K, Argaiz A, Palou E, Lopez-Malo A. 2005. Synergistic inhibitory effect of citral with selected phenolics against Zygosaccharomyces bailii. J. Food Prot. 68: 602-606.
Srokol Z, Bouche AG, van Estrik A, Strik RC, Maschmeyer T, Peters JA. 2004. Hydrothermal upgrading of biomass to biofuel; studies on some monosaccharide model compounds. Carbohydr. Res. 339: 1717-1726.
Sunnarborg SW, Miller SP, Unnikrishnan I, LaPorte DC. 2001. Expression of the yeast glycogen phosphorylase gene is regulated by stress-response elements and by the HOG MAP kinase pathway. Yeast 18: 1505-1514.
Treger JM, Schmitt AP, Simon JR, McEntee K. 1998. Transcriptional factor mutations reveal regulatory complexities of heat shock and newly identified stress genes in Saccharomyces cerevisiae. J. Biol. Chem. 273: 26875-26879.
Trotter EW, Kao CM, Berenfeld L, Botstein D, Petsko GA, Gray JV. 2002. Misfolded proteins are competent to mediate a subset of the responses to heat shock in Saccharomyces cerevisiae. J. Biol. Chem. 277: 44817-44825.