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Directed Evolution of Pyruvate Decarboxylase-Negative Saccharomyces cerevisiae , Yielding a C 2 -Independent, Glucose-Tolerant, and Pyruvate-Hyperproducing Yeast
Open accessAbstract
The absence of alcoholic fermentation makes pyruvate decarboxylase-negative (Pdc − ) strains of Saccharomyces cerevisiae an interesting platform for further metabolic engineering of central metabolism. However, Pdc − S. cerevisiae strains have two growth defects: (i) growth on synthetic medium in glucose-limited chemostat cultures requires the addition of small amounts of ethanol or acetate and (ii) even in the presence of a C 2 compound, these strains cannot grow in batch cultures on synthetic medium with glucose. We used two subsequent phenotypic selection strategies to obtain a Pdc − strain without these growth defects. An acetate-independent Pdc − mutant was obtained via (otherwise) glucose-limited chemostat cultivation by progressively lowering the acetate content in the feed. Transcriptome analysis did not reveal the mechanisms behind the C 2 independence. Further selection for glucose tolerance in shake flasks resulted in a Pdc − S. cerevisiae mutant (TAM) that could grow in batch cultures (μ max = 0.20 h −1 ) on synthetic medium, with glucose as the sole carbon source. Although the exact molecular mechanisms underlying the glucose-tolerant phenotype were not resolved, transcriptome analysis of the TAM strain revealed increased transcript levels of many glucose-repressible genes relative to the isogenic wild type in nitrogen-limited chemostat cultures with excess glucose. In pH-controlled aerobic batch cultures, the TAM strain produced large amounts of pyruvate. By repeated glucose feeding, a pyruvate concentration of 135 g liter −1 was obtained, with a specific pyruvate production rate of 6 to 7 mmol g of biomass −1 h −1 during the exponential-growth phase and an overall yield of 0.54 g of pyruvate g of glucose −1 .
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“Adaptive changes towards ethanol tolerance were linked to the up-regulation of oxyR and nrdR, indicating major changes in the cellular respiratory system but also changes in amino acid metabolism [85].”
From Adaptive laboratory evolution—Principles and applications for biotechnology (2013) · cites this paper as [85]
In the citing paper
“Furthermore, changes in enterobactin biosynthetic processes (ent genes) were also observed in independent studies [84,85,91].”
From Adaptive laboratory evolution—Principles and applications for biotechnology (2013) · cites this paper as [85]
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InfluentialYeast biomass, an optimised product with myriad applications in the food industry
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“Furthermore, its industrial production costs can be greatly reduced by increasing the titer and yield, whereby 135g/L pyruvate was accumulated from glucose by PDC-negative Saccharomyces cerevisiae [62].”
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Gambacorta, F. V., Dietrich, J. J., Yan, Q., & Pfleger, B. F. (2020) · Current Opinion in Chemical Biology · doi:10.1016/j.cbpa.2020.08.005 · Cited by 64
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BackgroundInfluentialComparative analysis of the chemical and biochemical synthesis of keto acids
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“In the other direction, through directed evolution of the Pdc− strains, the mutant strain TAM obtained tolerance of glucose, and the highest titer of pyruvate in S. cerevisiae reached 135 g/L (van Maris et al. 2004).”
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DIRECTED EVOLUTION: SELECTION OF THE HOST ORGANISM
Pourmir, A., & Johannes, T. W. (2012) · Computational and Structural Biotechnology Journal · doi:10.5936/csbj.201209012 · Cited by 57
Geertman, J.-M. A., van Maris, A. J. A., van Dijken, J. P., & Pronk, J. T. (2006) · Metabolic Engineering · doi:10.1016/j.ymben.2006.06.004 · Cited by 61
Self-citationMazzoleni, S., Landi, C., Cartenì, F., de Alteriis, E., Giannino, F., Paciello, L., & Parascandola, P. (2015) · Microbial Cell Factories · doi:10.1186/s12934-015-0295-4 · Cited by 51
Hubmann, G., Mathé, L., Foulquié-Moreno, M. R., Duitama, J., Nevoigt, E., & Thevelein, J. M. (2013) · Biotechnology for Biofuels · doi:10.1186/1754-6834-6-87 · Cited by 50
“Introduction Rational genetic modification of industrial microorganisms using targeted deletion and/or overexpression of structural or regulatory genes very often results in undesirable side effects on other essential functions [1-8].”
BackgroundKlein, M., Carrillo, M., Xiberras, J., Islam, Z.-U., Swinnen, S., & Nevoigt, E. (2016) · Metabolic Engineering · doi:10.1016/j.ymben.2016.10.008 · Cited by 47
Zhang, B., Zhu, Y., Zhang, J., Wang, D., Sun, L., & Hong, J. (2016) · Bioresource Technology · doi:10.1016/j.biortech.2016.11.110 · Cited by 47
Choi, B.-H., Rangel, A. E. T., Kerkhoven, E. J., & Nygård, Y. (2024) · Metabolic Engineering · doi:10.1016/j.ymben.2024.05.003 · Cited by 46
Zhang, Y., Liu, G., Engqvist, M. K. M., Krivoruchko, A., Hallström, B. M., Chen, Y., Siewers, V., & Nielsen, J. (2015) · Microbial Cell Factories · doi:10.1186/s12934-015-0305-6 · Cited by 42
2,3-Butanediol production from cellobiose by engineered Saccharomyces cerevisiae
Nan, H., Seo, S.-O., Oh, E. J., Seo, J., Cate, J. H. D., & Jin, Y. (2014) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-014-5683-x · Cited by 43
“While lack of acetyl-CoA may be the main reason why PDC mutants cannot grow on glucose, redox imbalance from the mutants' inability to regenerate NAD + may also contribute to lack of growth on glucose (van Maris et al., 2004).”
BackgroundEngineering Saccharomyces cerevisiae for Succinic Acid Production From Glycerol and Carbon Dioxide
Xiberras, J., Klein, M., de Hulster, E. A. F., Mans, R., & Nevoigt, E. (2020) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2020.00566 · Cited by 43
Ho, P.-W., Swinnen, S., Duitama, J., & Nevoigt, E. (2017) · Biotechnology for Biofuels · doi:10.1186/s13068-016-0696-6 · Cited by 42
“PK strains have been applied in numerous metabolic and evolutionary engineering studies, such as for the production of lactate and pyruvate [8, 9], isoprenoids [10, 11], C4-dicarboxylic acids [12], ornithine [13], n-butanol [14], and 3-hydroxypropionic acid [15], and for the fermentation of pentose sugars [16–18].”
MethodIshii, J., Morita, K., Ida, K., Kato, H., Kinoshita, S., Hataya, S., Shimizu, H., Kondo, A., & Matsuda, F. (2018) · Biotechnology for Biofuels · doi:10.1186/s13068-018-1176-y · Cited by 42
Yan, Y. L., Chen, H., Sun, L., Zhang, W., Lü, X., Li, Z., Xu, J., & Ren, Q. (2022) · PLoS ONE · doi:10.1371/journal.pone.0262353 · Cited by 42
“The principally well-known pyruvate bioproduction microorganisms are fungus like Torulopsis glabrata [92, 93] and Saccharomyces cerevisiae [94], with less research on bacterium.”
BackgroundLactic acid production from cellobiose and xylose by engineered Saccharomyces cerevisiae
Turner, T. L., Zhang, G., Oh, E. J., Subramaniam, V., Adiputra, A., Subramaniam, V., Skory, C. D., Jang, J. Y., Yu, B. J., Park, I., et al. (2015) · Biotechnology and Bioengineering · doi:10.1002/bit.25875 · Cited by 41
Wang, Z., Gao, C., Wang, Q., Liang, Q., & Qi, Q. (2012) · Biochemical Engineering Journal · doi:10.1016/j.bej.2012.06.006 · Cited by 39
Enhanced glutathione production by evolutionary engineering of Saccharomyces cerevisiae strains
Patzschke, A., Steiger, M. G., Holz, C., Lang, C., Mattanovich, D., & Sauer, M. (2015) · Biotechnology Journal · doi:10.1002/biot.201400809 · Cited by 38
“[18], who observed a two-fold increase in pyruvate production and from Cakar et al.”
BackgroundKamzolova, S. V., & Morgunov, I. G. (2018) · Bioresource Technology · doi:10.1016/j.biortech.2018.06.071 · Cited by 37
CO2 to succinic acid – Estimating the potential of biocatalytic routes
Liebal, U. W., Blank, L. M., & Ebert, B. E. (2018) · Metabolic Engineering Communications · doi:10.1016/j.mec.2018.e00075 · Cited by 38
Milne, N., Wahl, A., van Maris, A. J. A., Pronk, J. T., & Daran, J.-M. G. (2016) · Metabolic Engineering Communications · doi:10.1016/j.meteno.2016.01.002 · Cited by 37
“Consistent with an earlier report (van Maris et al., 2004a) the Pdc strain IMZ500 converted a large fraction of the consumed glucose to pyruvate (0.28970.071 mol/mol glucose).”
BackgroundInfluentialSelf-citationMETABOLIC ENGINEERING OF BIOCATALYSTS FOR CARBOXYLIC ACIDS PRODUCTION
Liu, P., & Jarboe, L. R. (2012) · Computational and Structural Biotechnology Journal · doi:10.5936/csbj.201210011 · Cited by 36
Bridging the Gap between Fluxomics and Industrial Biotechnology
Feng, X., Page, L., Rubens, J. R., Chircus, L. M., Colletti, P. F., Pakrasi, H. B., & Tang, Y. (2010) · BioMed Research International · doi:10.1155/2010/460717 · Cited by 36
Zhang, Y., Su, M., Wang, Z., Nielsen, J., & Liu, Z. (2022) · Synthetic and Systems Biotechnology · doi:10.1016/j.synbio.2022.06.004 · Cited by 35
“pdc deletion strains by limiting the glycolysis flux by reducing its degradation [15,16,21], indicating the possibility to regulate glucose uptake rates by manipulating MTH1 expression levels.”
BackgroundSelective recovery of pyruvic acid from two and three acid aqueous solutions by reactive extraction
Martı, M. E., & Gürkan, T. (2015) · Separation and Purification Technology · doi:10.1016/j.seppur.2015.09.067 · Cited by 35
Production of pyruvic acid from glycerol by Yarrowia lipolytica
Cybulski, K., Tomaszewska-Hetman, L., Rakicka, M., Juszczyk, P., & Rywińska, A. (2019) · Folia Microbiologica · doi:10.1007/s12223-019-00695-2 · Cited by 35
Schorsch, C., Köhler, T., & Boles, E. (2009) · Current Genetics · doi:10.1007/s00294-009-0252-z · Cited by 35
“Moreover, the deletion of genes has been shown to be a powerful means to redirect metabolic Xuxes or to engineer S. cerevisiae for the production of valuable chemicals (Boles et al. 1993; van Maris et al. 2004 ).”
Background
Metadata
- Authors
- van Maris, A. J. A., Geertman, J.-M. A., Vermeulen, A., Groothuizen, M. K., Winkler, A. A., Piper, M. D. W., van Dijken, J. P., & Pronk, J. T.
- Affiliations
- Department of Biotechnology, Delft University of Technology, NL-2628 BC Delft
- Delft University of Technology (NL)
- BIRD Engineering B.V., NL-3044 CK Rotterdam, The Netherlands
- Corresponding author
- Pronk, Jack T.
- Venue
- Applied and Environmental Microbiology
- Publisher
- American Society for Microbiology
- Published
- 2004-01
- Volume
- 70
- Issue
- 1
- Pages
- 159-166
- ISSN
- 0099-2240 (ISSN-L)
- 1098-5336
- PMC
- PMC321313
- OpenAlex
- W2119059442
- Cited by
- 227
- References
- 51
- Citations by year
- 2026: 3 · 2025: 5 · 2024: 10 · 2023: 5 · 2022: 15 · 2021: 25 · 2020: 19 · 2019: 5 · 2018: 16 · 2017: 16 · 2016: 15 · 2015: 16 · 2014: 14 · 2013: 10 · 2012: 16
- FWCI
- 1.42
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Locations
- Applied and Environmental Microbiology (publishedVersion, public-domain)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- UCL Discovery (University College London) (submittedVersion)
- Research Repository (Delft University of Technology) (submittedVersion)
- Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Microbial Metabolic Engineering and Bioproduction
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
- Physical Sciences › Engineering › Biomedical Engineering › Biofuel production and bioconversion
- Keywords
- Saccharomyces cerevisiae, glucose tolerance, phenotypic selection, glucose repression, glucose-limited chemostat, batch culture, yeast metabolic engineering
- MeSH terms
- Culture Media, Glucose, Mutation, Pyruvate Decarboxylase, Saccharomyces cerevisiae, Transcription, Genetic, Gene Expression Regulation, Fungal, Directed Molecular Evolution, Pyruvic Acid, Proteome, Saccharomyces cerevisiae Proteins
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