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 in E. coli were linked to the up-regulation of oxyR and nrdR, indicating major changes in the cellular respiratory system and changes in amino acid metabolism.
“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]
Changes in enterobactin biosynthetic processes (ent genes) were observed in independent E. coli studies.
“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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Huberts, D. H. E. W., Niebel, B., & Heinemann, M. (2011) · FEMS Yeast Research · doi:10.1111/j.1567-1364.2011.00767.x · Cited by 96 · see citing works
“The growth of this strain could be rescued using a directed evolution approach that yielded a strain with a reduced glucose uptake rate (72).”
BackgroundKim, J. W., Kim, J., Seo, S.-O., Kim, K. H., Jin, Y., & Seo, J. (2016) · Biotechnology for Biofuels · doi:10.1186/s13068-016-0677-9 · Cited by 94 · see citing works
Utilizing an endogenous pathway for 1-butanol production in Saccharomyces cerevisiae
Si, T., Luo, Y., Xiao, H., & Zhao, H. (2014) · Metabolic Engineering · doi:10.1016/j.ymben.2014.01.002 · Cited by 90 · see citing works
Wei, Z., Xu, Y., Xu, Q. C., Cao, W., Huang, H., & Liu, H. (2021) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2021.765685 · Cited by 90 · see citing works
Reconstruction of cytosolic fumaric acid biosynthetic pathways in Saccharomyces cerevisiae
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“cerevisiae, and it has been successfully manipulated to produce monocarboxylic acid pyruvate [8], lactate [9], dicarboxylic acid malate [10,11], and succinate [2].”
BackgroundMethodSystems metabolic engineering of microorganisms for food and cosmetics production
Choi, K. R., & Lee, S. Y. (2023) · Nature Reviews Bioengineering · doi:10.1038/s44222-023-00076-y · Cited by 87 · see citing works
Catalase Overexpression Reduces Lactic Acid-Induced Oxidative Stress in Saccharomyces cerevisiae
Abbott, D. A., Suir, E., Duong, G.-H., de Hulster, E. A. F., Pronk, J. T., & van Maris, A. J. A. (2009) · Applied and Environmental Microbiology · doi:10.1128/aem.00009-09 · Cited by 85 · see citing works
“In anaerobic, glucosegrown batch cultures, S. cerevisiae CEN.PK grows with a specific growth rate of 0.34 h1 (27), while the aerobic growth rate under identical conditions is slightly faster, at 0.37 h1 ( 43 ).”
BackgroundInfluentialSelf-citationAnaerobic Fermentation for Production of Carboxylic Acids as Bulk Chemicals from Renewable Biomass
Wang, J., Lin, M., Xu, M., & Yang, S. (2016) · Advances in biochemical engineering, biotechnology · doi:10.1007/10_2015_5009 · Cited by 86 · see citing works
Hu, Y., Zhu, Z., Nielsen, J., & Siewers, V. (2019) · Open Biology · doi:10.1098/rsob.190049 · Cited by 81 · see citing works
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“PK TAM strain (3) and listed in Table S1.”
Biotechnological production of alpha-keto acids: Current status and perspectives
Song, Y., Li, J., Shin, H., Liu, L., Du, G., & Chen, J. (2016) · Bioresource Technology · doi:10.1016/j.biortech.2016.08.015 · Cited by 77 · see citing works
Engineering rTCA pathway and C4-dicarboxylate transporter for l-malic acid production
Chen, X., Wang, Y., Dong, X., Hu, G., & Liu, L. (2017) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-017-8141-8 · Cited by 77 · see citing works
Pyruvate production inCandida glabrata: manipulation and optimization of physiological function
Li, S., Chen, X., Liu, L., & Chen, J. (2013) · Critical Reviews in Biotechnology · doi:10.3109/07388551.2013.811636 · Cited by 76 · see citing works
“…(Pdc ) S. cerevisiae mutant (TAM), which can produce 135 g L 1 pyruvate with a high productivity (1.35 g L 1 h 1) and a low yield on glucose (0.54 g g 1) using a repeated glucose feeding strategy, was a serious contender for industrial pyruvate production (van Maris et al., 2004).”
InfluentialYeast biomass, an optimised product with myriad applications in the food industry
Pérez‐Torrado, R., Gamero, E., Gómez‐Pastor, R., Garré, E., Aranda, A., & Matallana, E. (2015) · Trends in Food Science & Technology · doi:10.1016/j.tifs.2015.10.008 · Cited by 75 · see citing works
Recent Progress in the Microbial Production of Pyruvic Acid
Maleki, N., & Eiteman, M. A. (2017) · Fermentation · doi:10.3390/fermentation3010008 · Cited by 75 · see citing works
Chemostat-Based Micro-Array Analysis in Baker's Yeast
Daran-Lapujade, P. A. S., Daran, J.-M. G., van Maris, A. J. A., de Winde, J. H., & Pronk, J. T. (2008) · Advances in microbial physiology/Advances in Microbial Physiology · doi:10.1016/s0065-2911(08)00004-0 · Cited by 71 · see citing works
Self-citationSong, J.-Y., Park, J.-S., Kang, C. D., Cho, H.-Y., Yang, D., Lee, S., & Cho, K. M. (2015) · Metabolic Engineering · doi:10.1016/j.ymben.2015.09.006 · Cited by 71 · see citing works
Zhang, Y., Cortez, J. D., Hammer, S. K., Carrasco‐López, C., Echauri, S. A. G., Wiggins, J. B., Wang, W., & Avalos, J. L. (2022) · Nature Communications · doi:10.1038/s41467-021-27852-x · Cited by 71 · see citing works
Zelle, R. M., de Hulster, E. A. F., Kloezen, W., Pronk, J. T., & van Maris, A. J. A. (2009) · Applied and Environmental Microbiology · doi:10.1128/aem.02396-09 · Cited by 69 · see citing works
Self-citationKim, J.-W., Seo, S., Zhang, G.-C., Jin, Y., & Seo, J. (2015) · Bioresource Technology · doi:10.1016/j.biortech.2015.02.077 · Cited by 66 · see citing works
“Pdc-deficient S. cerevisiae strains have been constructed as platform strains for further metabolic engineering and production of pyruvate which can serve as an effective precursor for many chemicals (van Maris et al., 2004).”
BackgroundKok, S., Nijkamp, J. F., Oud, B., Roque, F. C., Ridder, D., Daran, J.-M., Pronk, J. T., & Maris, A. J. A. (2012) · FEMS Yeast Research · doi:10.1111/j.1567-1364.2011.00787.x · Cited by 65 · see citing works
Self-citationAdvances in biological production of acetoin: a comprehensive overview
Cui, Z., Wang, Z., Zheng, M., & Chen, T. (2021) · Critical Reviews in Biotechnology · doi:10.1080/07388551.2021.1995319 · Cited by 65 · see citing works
“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].”
BackgroundRewiring yeast metabolism to synthesize products beyond ethanol
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 · see citing works
“Summary of strategies for non-ethanol chemical production in S. cerevisiae Reference Pdc− phenotype Relieve Crabtree effect through ALE Alternate acetylCoA routes NAD+ regeneration Metabolic control of ethanol production Alternate carbon source Product(s) Yield (g/g carbon source) Titer (g/L) Conditions (carbon source…”
BackgroundInfluentialComparative analysis of the chemical and biochemical synthesis of keto acids
Luo, Z., Yu, S., Zeng, W., & Zhou, J. (2021) · Biotechnology Advances · doi:10.1016/j.biotechadv.2021.107706 · Cited by 64 · see citing works
The Production of Pyruvate in Biological Technology: A Critical Review
Yuan, W., Du, Y., Yu, K., Xu, S., Liu, M., Wang, S., Yang, Y., Zhang, Y., & Sun, J. (2022) · Microorganisms · doi:10.3390/microorganisms10122454 · Cited by 64 · see citing works
Metabolic engineering of Saccharomyces cerevisiae for 2,3-butanediol production
Kim, S.-J., Kim, J.-W., Lee, Y., Park, Y., & Seo, J. (2017) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-017-8172-1 · Cited by 63 · see citing works
“To overcome this defect and to relieve the glucose repression, some mutations in Pdc − S. cerevisiae were designed through evolutionary engineering or overexpression of the MTH1 gene encoding a transcriptional regulator (Lian et al. 2014; Oud et al. 2012; van Maris et al. 2004).”
BackgroundNutrient-Limited Operational Strategies for the Microbial Production of Biochemicals
Rajpurohit, H., & Eiteman, M. A. (2022) · Microorganisms · doi:10.3390/microorganisms10112226 · Cited by 62 · see citing works
“In fact, at a long time-scale, the chemostat is an invaluable tool to evolve strains with greater substrate affinity [31–34], with relieved auxotrophy [35] or with a gain of substrate utilization [36].”
BackgroundCurrent advance in biological production of short-chain organic acid
Sun, L., Gong, M., Lv, X., Huang, Z., Gu, Y. M., Li, J., Du, G., & Liu, L. (2020) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-020-10917-0 · Cited by 61 · see citing works
“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).”
BackgroundInfluentialExtractive Fermentation for the Production of Carboxylic Acids
Yang, S., Huang, H., Tay, A., Qin, W., Guzman, L. D., & Nicolas, E. C. S. (2007) · Elsevier eBooks · doi:10.1016/b978-044452114-9/50017-7 · Cited by 61 · see citing works
Metabolic engineering of strains: from industrial-scale to lab-scale chemical production
Sun, J., & Alper, H. S. (2014) · Journal of Industrial Microbiology & Biotechnology · doi:10.1007/s10295-014-1539-8 · Cited by 60 · see citing works
“cerevisiae at titers of 90 g/L [175] and 135 g/L [139], respectively.”
Kim, S.-J., Sim, H.-J., Kim, J.-W., Lee, Y., Park, Y., & Seo, J. (2017) · Bioresource Technology · doi:10.1016/j.biortech.2017.06.034 · Cited by 60 · see citing works
Value-added biotransformation of cellulosic sugars by engineered Saccharomyces cerevisiae
Lane, S., Jia, D., & Jin, Y. (2018) · Bioresource Technology · doi:10.1016/j.biortech.2018.04.013 · Cited by 59 · see citing works
Chen, Y., Zhang, Y., Siewers, V., & Nielsen, J. (2015) · FEMS Yeast Research · doi:10.1093/femsyr/fov015 · Cited by 58 · see citing works
“…chemostat cultures of S. cerevisiae (van Maris et al. 2003), Gly1 as a possible source for cytosolic acetyl-CoA production was excluded due to its low affinity for threonine and the relatively low intracellular threonine concentration when yeast is grown at excess glucose (van Maris et al. 2004).”
BackgroundÇakar, Z. P., Alkım, C., Turanlı-Yıldız, B., Tokman, N., Akman, S., Sarıkaya, M., Tamerler, C., Benbadis, L., & François, J. (2009) · Journal of Biotechnology · doi:10.1016/j.jbiotec.2009.06.024 · Cited by 57 · see citing works
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 · see citing works
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 56 · see citing works
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 50 · see citing works
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 · see citing works
“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 · see citing works
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 · see citing works
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 · see citing works
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 43 · see citing works
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 · see citing works
“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 · see citing works
Ho, P.-W., Swinnen, S., Duitama, J., & Nevoigt, E. (2017) · Biotechnology for Biofuels · doi:10.1186/s13068-016-0696-6 · Cited by 42 · see citing works
“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 · see citing works
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 · see citing works
“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 · see citing works
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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 · see citing works
“[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 · see citing works
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 · see citing works
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 · see citing works
“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 · see citing works
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 · see citing works
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 · see citing works
“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 · see citing works
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 · see citing works
Schorsch, C., Köhler, T., & Boles, E. (2009) · Current Genetics · doi:10.1007/s00294-009-0252-z · Cited by 35 · see citing works
“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
- 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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