Abstract
2-Phenylethanol (2-PE) is a kind of advanced aromatic alcohol with rose fragrance, which is wildly used for the deployment of flavors and fragrances. Microbial transformation is the most feasible method for the production of natural 2-PE. But a bottleneck problem is the toxicity of 2-PE on the cells. The molecular mechanisms of the toxic effect of 2-PE to Saccharomyces cerevisiae are not well studied. In this study, we analyzed the transcriptomes of S. cerevisiae in the media with and without 2-PE, respectively, using Illumina RNA-Seq technology. We identified 580 differentially expressed genes between S. cerevisiae in two different treatments. GO and KEGG enrichment analyses of these genes suggested that most genes encoding mitochondrial proteins, cytoplasmic, and plasma membrane proteins were significantly up-regulated, whereas the enzymes related to amino acid metabolism were down-regulated. These results indicated that 2-PE suppressed the synthesis of plasma membrane proteins, which suppressed the transport of nutrients required for growth. The findings in this study will provide insight into the inhibitory mechanism of 2-PE to yeast and other microbes.
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Albertazzi E, Cardillo R, Servi S, Zucchi G (1994) Biogeneration of 2-phenylethanol and 2-phenylethylacetate important aroma components. Biotechnol Lett 16:491–496
Bauer MF, Hofmann S, Neupert W, Brunner M (2000) Protein translocation into mitochondria: the role of TIM complexes. Trends Cell Biol 10:25–31
Boer VM, Tai SL, Vuralhan Z, Arifin Y, Walsh MC, Piper MD, de Winde JH, Pronk JT, Daran JM (2007) Transcriptional responses of Saccharomyces cerevisiae to preferred and nonpreferred nitrogen sources in glucose-limited chemostat cultures. FEMS Yeast Res 7:604–620
Brush GS, Najor NA, Dombkowski AA, Cukovic D, Sawarynski KE (2012) Yeast IME2 functions early in meiosis upstream of cell cycle-regulated SBF and MBF targets. PLoS ONE 7:e31575
Chung HJ, Lee SL, Chou CC (2000) Production and molar yield of 2-phenylethanol by Pichia fermentans L-5 as affected by some medium components. J Biosci Bioeng 90:142–147
Desai N, Brown A, Amunts A, Ramakrishnan V (2017) The structure of the yeast mitochondrial ribosome. Science 355:528–531
Eshkol N, Sendovski M, Bahalul M, Katz-Ezov T, Kashi Y, Fishman A (2009) Production of 2-phenylethanol from L-phenylalanine by a stress tolerant Saccharomyces cerevisiae strain. J Appl Microbiol 106:534–542
Florea L, Song L, Salzberg SL (2013) Thousands of exon skipping events differentiate among splicing patterns in sixteen human tissues. F1000Research 2:188
Godard P, Urrestarazu A, Vissers S, Kontos K, Bontempi G, van Helden J, Andre B (2007) Effect of 21 different nitrogen sources on global gene expression in the yeast Saccharomyces cerevisiae. Mol Cell Biol 27:3065–3086
Hazelwood LA, Daran JM, van Maris AJ, Pronk JT, Dickinson JR (2008) The Ehrlich pathway for fusel alcohol production: a century of research on Saccharomyces cerevisiae metabolism. Appl Environ Microbiol 74:2259–2266
Herrmann JM, Woellhaf MW, Bonnefoy N (2013) Control of protein synthesis in yeast mitochondria: the concept of translational activators. Biochim Biophys Acta 1833:286–294
Hirschberg J, Simchen G (1977) Commitment to the mitotic cell cycle in yeast in relation to meiosis. Exp Cell Res 105:245–252
Honigberg SM, Purnapatre K (2003) Signal pathway integration in the switch from the mitotic cell cycle to meiosis in yeast. J Cell Sci 11:2137–2147
Hurtado S, Kim GK, Sontheimer EJ (2014) SPO24 is a transcriptionally dynamic, small ORF-encoding locus required for efficient sporulation in Saccharomyces cerevisiae. PLoS ONE 9:e105058
Iraqui I, Vissers S, Andre B, Urrestarazu A (1999) Transcriptional induction by aromatic amino acids in Saccharomyces cerevisiae. Mol Cell Biol 19:3360–3371
Jambhekar A, Amon A (2008) Control of meiosis by respiration. Curr Biol 18:969–975
Kim B, Cho BR, Hahn JS (2014) Metabolic engineering of Saccharomyces cerevisiae for the production of 2-phenylethanol via Ehrlich pathway. Biotechnol Bioeng 111:115–124
Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg SL (2013) TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol 14:R36
Kuszak AJ, Jacobs D, Gurnev PA, Shiota T, Louis JM, Lithgow T, Bezrukov SM, Rostovtseva TK, Buchanan SK (2015) Evidence of distinct channel conformations and substrate binding affinities for the mitochondrial outer membrane protein translocase pore Tom40. J Biol Chem 290:26204–26217
Liu P, Cheng Y, Yang M, Liu Y, Chen K, Long CA, Deng X (2014) Mechanisms of action for 2-phenylethanol isolated from Kloeckera apiculata in control of Penicillium molds of citrus fruits. BMC Microbiol 14:242
Magasanik B (2003) Ammonia assimilation by Saccharomyces cerevisiae. Eukaryot Cell 2:827–829
Marini AM, Vissers S, Urrestarazu A, Andre B (1994) Cloning and expression of the MEP1 gene encoding an ammonium transporter in Saccharomyces cerevisiae. EMBO J 13:3456–3463
Neupert W (1997) Protein import into mitochondria. Annu Rev Biochem 66:863–917
Piekarska I, Rytka J, Rempola B (2010) Regulation of sporulation in the yeast Saccharomyces cerevisiae. Acta Biochim Pol 57:241–250
Pierce M, Benjamin KR, Montano SP, Georgiadis MM, Winter E, Vershon AK (2003) Sum1 and Ndt80 proteins compete for binding to middle sporulation element sequences that control meiotic gene expression. Mol Cell Biol 23:4814–4825
Popa CV, Dumitru I, Ruta LL, Danet AF, Farcasanu IC (2010) Exogenous oxidative stress induces Ca2+ release in the yeast Saccharomyces cerevisiae. FEBS J 277:4027–4038
Reichert AS, Neupert W (2002) Contact sites between the outer and inner membrane of mitochondria-role in protein transport. Biochim Biophys Acta 1592:41–49
Roy M, Reddy PH, Iijima M, Sesaki H (2015) Mitochondrial division and fusion in metabolism. Curr Opin Cell Biol 33:111–118
Schuller HJ (2003) Transcriptional control of nonfermentative metabolism in the yeast Saccharomyces cerevisiae. Curr Genet 43:139–160
Sendovski M, Nir N, Fishman A (2010) Bioproduction of 2-phenylethanol in a biphasic ionic liquid aqueous system. J Agric Food Chem 58:2260–2265
Serp D, von Stockar U, Marison IW (2003) Enhancement of 2-phenylethanol productivity by Saccharomyces cerevisiae in two-phase fed-batch fermentations using solvent immobilization. Biotechnol Bioeng 82:103–110
Smith HE, Driscoll SE, Sia RA, Yuan HE, Mitchell AP (1993) Genetic evidence for transcriptional activation by the yeast IME1 gene product. Genetics 133:775–784
Sokol AM, Sztolsztener ME, Wasilewski M, Heinz E, Chacinska A (2014) Mitochondrial protein translocases for survival and wellbeing. FEBS Lett 588:2484–2495
Stark D, Munch T, Sonnleitner B, Marison IW, von Stockar U (2002) Extractive bioconversion of 2-phenylethanol from L-phenylalanine by Saccharomyces cerevisiae. Biotechnol Prog 18:514–523
Stark D, Zala D, Münch T, Sonnleitner B, Marison IW, Stockar U (2003) Inhibition aspects of the bioconversion of L-phenylalanine to 2-phenylethanol by Saccharomyces cerevisiae. Enzyme Microb Technol 32:113–212
Van der Rest ME, Kamminga AH, Nakano A, Anraku Y, Poolman B, Konings WN (1995) The plasma membrane of Saccharomyces cerevisiae: structure, function, and biogenesis. Microbiol Rev 59:304–322
Walther K, Schuller HJ (2001) Adr1 and Cat8 synergistically activate the glucose-regulated alcohol dehydrogenase gene ADH2 of the yeast Saccharomyces cerevisiae. Microbiology 147:2037–2044
Wang Z, Bai X, Guo X, He X (2017) Regulation of crucial enzymes and transcription factors on 2-phenylethanol biosynthesis via Ehrlich pathway in Saccharomyces cerevisiae. J Ind Microbiol Biotechnol 44:129–139
Acknowledgements
This study was supported by the Science and Technology Project of Jiangxi Academy of Sciences (2017-YZD2-05, 2014-YYB-09, 2014-XTPH1-09).
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Jin, D., Gu, B., Xiong, D. et al. A Transcriptomic Analysis of Saccharomyces cerevisiae Under the Stress of 2-Phenylethanol. Curr Microbiol 75, 1068–1076 (2018). https://doi.org/10.1007/s00284-018-1488-y
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DOI: https://doi.org/10.1007/s00284-018-1488-y