Turbidostat culture of Saccharomyces cerevisiae W303-1A under selective pressure elicited by ethanol selects for mutations in SSD1 and UTH1
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We investigated the genetic causes of ethanol tolerance by characterizing mutations selected in Saccharomyces cerevisiae W303-1A under the selective pressure of ethanol. W303-1A was subjected to three rounds of turbidostat, in a medium supplemented with increasing amounts of ethanol. By the end of selection, the growth rate of the culture has increased from 0.029 to 0.32 h(-1) . Unlike the progenitor strain, all yeast cells isolated from this population were able to form colonies on medium supplemented with 7% ethanol within 6 days, our definition of ethanol tolerance. Several clones selected from all three stages of selection were able to form dense colonies within 2 days on solid medium supplemented with 9% ethanol. We sequenced the whole genomes of six clones and identified mutations responsible for ethanol tolerance. Thirteen additional clones were tested for the presence of similar mutations. In 15 of 19 tolerant clones, the stop codon in ssd1-d was replaced with an amino acid-encoding codon. Three other clones contained one of two mutations in UTH1, and one clone did not contain mutations in either SSD1 or UTH1. We showed that the mutations in SSD1 and UTH1 increased tolerance of the cell wall to zymolyase and conclude that stability of the cell wall is a major factor in increased tolerance to ethanol.
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Selection for improved galactose utilization could be achieved by serial transfer with a 24% increase of μmax within 62 days, and galactose uptake rates and ethanol production were increased.
“For other carbon sources, it was shown that selection for improved galactose utilization could be achieved by serial transfer with a 24% increase of μmax within 62 days. Galactose uptake rates and ethanol production were increased.”
From Adaptive laboratory evolution—Principles and applications for biotechnology (2013) · cites this paper as [106]
Transcript analysis in galactose-evolved S. cerevisiae showed up-regulation of trehalose and glycogen metabolism, no mutations in galactose or storage carbohydrate related genes, and mutations in RAS/PKA signaling as a source for increased fitness on galactose medium.
“Transcript analysis showed up-regulation of trehalose and glycogen metabolism, whereas no mutations were identified in galactose or storage carbohydrate related genes. Interestingly, the authors rather identified mutations in RAS/PKA signaling as a source for increased fitness on galactose medium [106].”
From Adaptive laboratory evolution—Principles and applications for biotechnology (2013) · cites this paper as [106]
Yeast cells that were evolved for efficient galactose utilization subsequently showed trade-offs when grown on glucose as carbon source; this effect was due to antagonistic pleiotropy based on mutations of the regulatory protein RAS2.
“Yeast cells that were evolved for efficient galactose utilization [106] subsequently showed trade-offs when grown on glucose as carbon source. This effect was due to antagonistic pleiotropy that was based on mutations of the regulatory protein RAS2[162].”
From Adaptive laboratory evolution—Principles and applications for biotechnology (2013) · cites this paper as [106]
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Cites
The Sequence Alignment/Map format and SAMtools
Li, H., Handsaker, B., Wysoker, A., Fennell, T., Ruan, J., Homer, N., Marth, G., Abecasis, G., Durbin, R., & 1000 Genome Project Data Processing Subgroup (2009) · Bioinformatics · doi:10.1093/bioinformatics/btp352 · Cited by 62,041 · see citing works
Fast and accurate short read alignment with Burrows-Wheeler transform
Li, H., & Durbin, R. (2009) · Bioinformatics · doi:10.1093/bioinformatics/btp324 · Cited by 58,607 · see citing works
Sikorski, R. S., & Hieter, P. (1989) · Genetics · doi:10.1093/genetics/122.1.19 · Cited by 8,685 · see citing works
Current protocols in molecular biology
(1988) · Trends in Biochemical Sciences · doi:10.1016/0968-0004(88)90131-4 · Cited by 4,234 · see citing works
Brachmann, C. B., Davies, A., Cost, G. J., Caputo, E. M., Li, J., Hieter, P., & Boeke, J. D. (1998) · Yeast · doi:10.1002/(sici)1097-0061(19980130)14:2 · Cited by 3,411 · see citing works
Trends in biotechnological production of fuel ethanol from different feedstocks
Sánchez, Ó. J., & Cardona, C. A. (2008) · Bioresource Technology · doi:10.1016/j.biortech.2007.11.013 · Cited by 1,826 · see citing works
Ethanol fermentation from biomass resources: current state and prospects
Lin, Y., & Tanaka, S. (2005) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-005-0229-x · Cited by 1,622 · see citing works
Cell Wall Integrity Signaling in <i>Saccharomyces cerevisiae</i>
Levin, D. E. (2005) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.69.2.262-291.2005 · Cited by 1,136 · see citing works
Martínez‐Pastor, M. T., Marchler, G. H., Schüller, C., Marchler‐Bauer, A., Ruis, H., & Estruch, F. (1996) · The EMBO Journal · doi:10.1002/j.1460-2075.1996.tb00576.x · Cited by 1,077 · see citing works
Engineering Yeast Transcription Machinery for Improved Ethanol Tolerance and Production
Alper, H., Moxley, J., Nevoigt, E., Fink, G. R., & Stephanopoulos, G. (2006) · Science · doi:10.1126/science.1131969 · Cited by 823 · see citing works
Hogan, D. J., Riordan, D. P., Gerber, A. P., Herschlag, D., & Brown, P. O. (2008) · PLoS Biology · doi:10.1371/journal.pbio.0060255 · Cited by 609 · see citing works
Mutation in the silencing gene S/R4 can delay aging in S. cerevisiae
Kennedy, B. K., Austriaco, N. P. G., Zhang, J., & Guarente, L. (1995) · Cell · doi:10.1016/0092-8674(95)90499-9 · Cited by 499 · see citing works
Quick and easy yeast transformation using the LiAc/SS carrier DNA/PEG method
Gietz, R. D., & Schiestl, R. H. (2007) · Nature Protocols · doi:10.1038/nprot.2007.14 · Cited by 448 · see citing works
Uth1p Is Involved in the Autophagic Degradation of Mitochondria
Bhatia‐Kiššová, I., Deffieu, M. S., Manon, S., & Camougrand, N. M. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m406960200 · Cited by 418 · see citing works
Piper, P. W. (1995) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.1995.tb07925.x · Cited by 389 · see citing works
Global gene expression during short‐term ethanol stress in Saccharomyces cerevisiae
Alexandre, H., Galéote, V., Dequin, S., & Blondin, B. (2001) · FEBS Letters · doi:10.1016/s0014-5793(01)02503-0 · Cited by 369 · see citing works
Estimating the Per-Base-Pair Mutation Rate in the Yeast <i>Saccharomyces cerevisiae</i>
Lang, G. I., & Murray, A. W. (2008) · Genetics · doi:10.1534/genetics.107.071506 · Cited by 344 · see citing works
The SIT4 protein phosphatase functions in late G1 for progression into S phase.
Sutton, A., Immanuel, D., & Arndt, K. T. (1991) · Molecular and Cellular Biology · doi:10.1128/mcb.11.4.2133 · Cited by 337 · see citing works
Kao, K. C., & Sherlock, G. J. (2008) · Nature Genetics · doi:10.1038/ng.280 · Cited by 314 · see citing works
Self-citationMechanisms of ethanol tolerance in Saccharomyces cerevisiae
Ma, M., & Liu, Z. L. (2010) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-010-2594-3 · Cited by 309 · see citing works
Tolerance and stress response to ethanol in the yeast Saccharomyces cerevisiae
Ding, J., Huang, X., Zhang, L., Zhao, N., Yang, D., & Zhang, K. (2009) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-009-2223-1 · Cited by 309 · see citing works
[2] Micromanipulation and dissection of asci
Sherman, F., & Hicks, J. (1991) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/0076-6879(91)94005-w · Cited by 305 · see citing works
Reinke, A. W., Anderson, S., McCaffery, J. M., Yates, J. R., Aronova, S., Chu, S., Fairclough, S. R., Iverson, C., Wedaman, K. P., & Powers, T. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m313062200 · Cited by 257 · see citing works
Mechanisms of yeast stress tolerance and its manipulation for efficient fuel ethanol production
Zhao, X., & Bai, F. (2009) · Journal of Biotechnology · doi:10.1016/j.jbiotec.2009.05.001 · Cited by 244 · see citing works
Yoshikawa, K., Tanaka, T., Furusawa, C., Nagahisa, K., Hirasawa, T., & Shimizu, H. (2008) · FEMS Yeast Research · doi:10.1111/j.1567-1364.2008.00456.x · Cited by 230 · see citing works
Hirasawa, T., Yoshikawa, K., Nakakura, Y., et al. (2007) · Journal of Biotechnology · doi:10.1016/j.jbiotec.2007.05.010 · Cited by 211 · see citing works
Microbial Selection in Continuous Culture
Harder, W., Kuenen, J. G., & Matin, A. (1977) · Journal of Applied Bacteriology · doi:10.1111/j.1365-2672.1977.tb00717.x · Cited by 181 · see citing works
Fujita, K., Matsuyama, A., Kobayashi, Y., et al. (2006) · FEMS Yeast Research · doi:10.1111/j.1567-1364.2006.00040.x · Cited by 165 · see citing works
KUBOTA, S., TAKEO, I., Kume, K., et al. (2004) · Bioscience Biotechnology and Biochemistry · doi:10.1271/bbb.68.968 · Cited by 164 · see citing works
Whole-Genome Sequencing of Sake Yeast Saccharomyces cerevisiae Kyokai no. 7
Akao, T., Yashiro, I., Hosoyama, A., Kitagaki, H., Horikawa, H., Watanabe, D., Akada, R., Ando, Y., Harashima, S., Inoue, T., et al. (2011) · DNA Research · doi:10.1093/dnares/dsr029 · Cited by 157 · see citing works
van Voorst, F., Houghton‐Larsen, J., Jønson, L., Kielland‐Brandt, M. C., & Brandt, A. (2006) · Yeast · doi:10.1002/yea.1359 · Cited by 156 · see citing works
Transcriptional profiling on all open reading frames ofSaccharomyces cerevisiae
Hauser, N. C., Vingron, M., Scheideler, M., Krems, B., Hellmuth, K., Entian, K.-D., & Hoheisel, J. D. (1998) · Yeast · doi:10.1002/(sici)1097-0061(19980930)14:13 · Cited by 131 · see citing works
Saccharomyces cerevisiae MPT5 and SSD1 Function in Parallel Pathways to Promote Cell Wall Integrity
Kaeberlein, M. R., & Guarente, L. (2002) · Genetics · doi:10.1093/genetics/160.1.83 · Cited by 124 · see citing works
Tolerance Mechanism of the Ethanol-Tolerant Mutant of Sake Yeast.
Ogawa, Y., Nitta, A., Uchiyama, H., Imamura, T., Shimoi, H., & Ito, K. (2000) · Journal of Bioscience and Bioengineering · doi:10.1016/s1389-1723(00)80087-0 · Cited by 120 · see citing works
Kim, J., Alizadeh, P., Harding, T., et al. (1996) · Applied and Environmental Microbiology · doi:10.1128/aem.62.5.1563-1569.1996 · Cited by 120 · see citing works
The Yeast Ras/Cyclic AMP Pathway Induces Invasive Growth by Suppressing the Cellular Stress Response
Stanhill, A., Schick, N., & Engelberg, D. (1999) · Molecular and Cellular Biology · doi:10.1128/mcb.19.11.7529 · Cited by 116 · see citing works
Self-citationCbk1 Regulation of the RNA-Binding Protein Ssd1 Integrates Cell Fate with Translational Control
Jansen, J. M., Wanless, A. G., Seidel, C. W., & Weiss, E. L. (2009) · Current Biology · doi:10.1016/j.cub.2009.10.071 · Cited by 110 · see citing works
High-Resolution Genetic Mapping With Ordered Arrays of Saccharomyces cerevisiae Deletion Mutants
Jorgensen, P., Nelson, B., Robinson, M. D., Chen, Y., Andrews, B., Tyers, M., & Boone, C. M. (2002) · Genetics · doi:10.1093/genetics/162.3.1091 · Cited by 106 · see citing works
Generation and characterisation of stable ethanol-tolerant mutants of Saccharomyces cerevisiae
Stanley, D., Fraser, S., Chambers, P. J., Rogers, P. L., & Stanley, G. A. (2009) · Journal of Industrial Microbiology & Biotechnology · doi:10.1007/s10295-009-0655-3 · Cited by 105 · see citing works
Isolation of ethanol-tolerant mutants of yeast by continuous selection
Brown, S., & Oliver, S. G. (1982) · Applied Microbiology and Biotechnology · doi:10.1007/bf00500738 · Cited by 102 · see citing works
A Saccharomyces cerevisiae mutant with increased virulence
Wheeler, R. T., Kupiec, M., Magnelli, P. E., Abeijón, C., & Fink, G. R. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0437995100 · Cited by 99 · see citing works
Takahashi, T., Shimoi, H., & Ito, K. (2001) · Molecular Genetics and Genomics · doi:10.1007/s004380100510 · Cited by 93 · see citing works
Camougrand, N. M., Grelaud, A., Marza, E., Priault, M., Bessoule, J., & Manon, S. (2003) · Molecular Microbiology · doi:10.1046/j.1365-2958.2003.03311.x · Cited by 81 · see citing works
A possible role of trehalose in osmotolerance and ethanol tolerance in Saccharomyces cerevisiae
Sharma, S. C. (2006) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.1997.tb10402.x · Cited by 80 · see citing works
Kopp, M., & Hermisson, J. (2009) · Genetics · doi:10.1534/genetics.109.106195 · Cited by 78 · see citing works
Jo, W. J., Loguinov, A. V., Chang, M., Henri Wintz, A., Nislow, C., Arkin, A. P., Giaever, G. N., & Vulpe, C. D. (2007) · Toxicological Sciences · doi:10.1093/toxsci/kfm226 · Cited by 76 · see citing works
Involvement of the Saccharomyces cerevisiae UTH1 gene in the oxidative-stress response
Bandara, P., Flattery-O'Brien, J. A., Grant, C. M., & Dawes, I. W. (1998) · Current Genetics · doi:10.1007/s002940050395 · Cited by 59 · see citing works
The SUN41 and SUN42 genes are essential for cell separation in Candida albicans
Firon, A., Aubert, S., Iraqui, I., Guadagnini, S., Goyard, S., Prévost, M., Janbon, G., & d’Enfert, C. (2007) · Molecular Microbiology · doi:10.1111/j.1365-2958.2007.06011.x · Cited by 56 · see citing works
Yazawa, H., Iwahashi, H., & Uemura, H. (2007) · Yeast · doi:10.1002/yea.1492 · Cited by 54 · see citing works
Saccharomyces cerevisiae SSD1-V Confers Longevity by a Sir2p-Independent Mechanism
Kaeberlein, M. R. (2004) · Genetics · doi:10.1534/genetics.166.4.1661 · Cited by 54 · see citing works
Jung, W. H., Warn, P. A., Ragni, E., Popolo, L., Nunn, C. D., Turner, M., & Stateva, L. I. (2005) · Yeast · doi:10.1002/yea.1199 · Cited by 50 · see citing works
Camougrand, N. M., Mouassite, M., Velours, G., et al. (2000) · Archives of Biochemistry and Biophysics · doi:10.1006/abbi.1999.1655 · Cited by 45 · see citing works
The Saccharomyces SUN gene, UTH1 , is involved in cell wall biogenesis
Ritch, J. J., Davidson, S. M., Sheehan, J., & Austriaco, N. P. G. (2009) · FEMS Yeast Research · doi:10.1111/j.1567-1364.2009.00601.x · Cited by 39 · see citing works
Selection of Ethanol-Tolerant Yeast Hybrids in pH-Regulated Continuous Culture
Jiménez, J., & Benı́tez, T. (1988) · Applied and Environmental Microbiology · doi:10.1128/aem.54.4.917-922.1988 · Cited by 38 · see citing works
Bloom, F. R., & McFall, E. (1975) · Journal of Bacteriology · doi:10.1128/jb.121.3.1078-1084.1975 · Cited by 34 · see citing works
Genome-Wide Expression Profile of Sake Brewing Yeast under Shaking and Static Conditions
Shobayashi, M., Ukena, E., Fujii, T., & Iefuji, H. (2007) · Bioscience Biotechnology and Biochemistry · doi:10.1271/bbb.60190 · Cited by 31 · see citing works
Bennett, W. N., & Boraas, M. E. (1988) · Aquaculture · doi:10.1016/0044-8486(88)90038-5 · Cited by 24 · see citing works
Baerends, R. J. S., Qiu, J., Rasmussen, S., Nielsen, H. B., & Brandt, A. (2009) · Applied and Environmental Microbiology · doi:10.1128/aem.00989-09 · Cited by 21 · see citing works
The present status and future prospects of the turbidostat
Watson, T. G. (1972) · Journal of Applied Chemistry and Biotechnology · doi:10.1002/jctb.5020220206 · Cited by 21 · see citing works
The present status and future prospects of the turbidostat
Watson, T. G. (1972) · Journal of Applied Chemistry and Biotechnology · doi:10.1002/jctb.2720220206 · Cited by 20 · see citing works
Omi, K., Sonoda, H., Nagata, K., et al. (1999) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.1999.1209 · Cited by 19 · see citing works
Influence of Ras function on ethanol stress response of sake yeast
Yamaji, K., Hara, S., & Mizoguchi, H. (2003) · Journal of Bioscience and Bioengineering · doi:10.1016/s1389-1723(03)70134-0 · Cited by 9 · see citing works
The susceptibility of membrane vesicles to interaction with ethanol
Chen, C., & Engel, S. G. (1990) · Chemistry and Physics of Lipids · doi:10.1016/0009-3084(90)90113-6 · Cited by 8 · see citing works
Jo, W. J., Loguinov, A. V., Chang, M., et al. (2008) · Toxicological Sciences · doi:10.1093/toxsci/kfm307 · Cited by 6 · see citing works
Molecular Mechanism of Sporulation Defect in Sake Yeast, Kyokai No.7
Nakazawa, N., Harashima, S., & Oshima, Y. (1993) · JOURNAL OF THE BREWING SOCIETY OF JAPAN · doi:10.6013/jbrewsocjapan1988.88.354 · Cited by 3 · see citing works
Possible regulatory function of the Saccharomyces cerevisiae Ty1 retrotransposon core protein
Roth, J., Kingsman, S., Kingsman, A., & Martin-Rendon, E. (2000) · Yeast · doi:10.1002/1097-0061(200007)16:10
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- Jimenez J Benitez T 1988 Selection of Ethanol-Tolerant Yeast Hybrids in pH-Regulated Continuous Culture Appl Environ Microbiol 54 917 922 16347613 PMC202573
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- Authors
- Avrahami-Moyal, L., Engelberg, D., Wenger, J. W., Sherlock, G., & Braun, S.
- Affiliations
- Department of Biological Chemistry; Institute of Life Sciences; The Hebrew University of Jerusalem; Jerusalem; Israel
- Hebrew University of Jerusalem (IL)
- Stanford Medicine (US)
- Corresponding author
- Braun, Sergei
- Venue
- FEMS Yeast Research
- Publisher
- Oxford University Press (OUP)
- Published
- 2012-04-23
- Volume
- 12
- Issue
- 5
- Pages
- 521-533
- ISSN
- 1567-1356 (ISSN-L)
- PMC
- PMC3393845
- OpenAlex
- W2098597173
- Cited by
- 43
- References
- 66
- Citations by year
- 2026: 1 · 2025: 5 · 2024: 4 · 2023: 2 · 2022: 3 · 2021: 4 · 2020: 2 · 2019: 5 · 2018: 1 · 2017: 3 · 2016: 3 · 2015: 4 · 2014: 4 · 2013: 1 · 2012: 1
- FWCI
- 1.28
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Locations
- FEMS Yeast Research (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Hebrew University of Jerusalem
- National Institute of General Medical Sciences (T32GM007790, GM007790)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Microbial Metabolic Engineering and Bioproduction
- Keywords
- ethanol tolerance, Saccharomyces cerevisiae, Ssd1, selection pressure, cell wall stability, zymolyase, growth rate, yeast cell wall
- MeSH terms
- Ethanol, Cell Wall, Culture Media, DNA Mutational Analysis, Glucan Endo-1,3-beta-D-Glucosidase, Heat-Shock Proteins, Membrane Proteins, Saccharomyces cerevisiae, Selection, Genetic, Genome, Fungal, Sequence Analysis, DNA, Mutation, Missense, Mitochondrial Proteins, Saccharomyces cerevisiae Proteins
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