Cited by 251Microbial Metabolic Engineering and BioproductionBiofuel production and bioconversionFungal and yeast genetics research

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Evolutionary Engineering of Saccharomyces cerevisiae for Anaerobic Growth on Xylose

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Sonderegger, Marco, Sauer, Uwe·2003·Applied and Environmental Microbiology

DOI 10.1128/aem.69.4.1990-1998.2003PMC PMC154834

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Abstract

Xylose utilization is of commercial interest for efficient conversion of abundant plant material to ethanol. Perhaps the most important ethanol-producing organism, Saccharomyces cerevisiae , however, is incapable of xylose utilization. While S. cerevisiae strains have been metabolically engineered to utilize xylose, none of the recombinant strains or any other naturally occurring yeast has been able to grow anaerobically on xylose. Starting with the recombinant S. cerevisiae strain TMB3001 that overexpresses the xylose utilization pathway from Pichia stipitis , in this study we developed a selection procedure for the evolution of strains that are capable of anaerobic growth on xylose alone. Selection was successful only when organisms were first selected for efficient aerobic growth on xylose alone and then slowly adapted to microaerobic conditions and finally anaerobic conditions, which indicated that multiple mutations were necessary. After a total of 460 generations or 266 days of selection, the culture reproduced stably under anaerobic conditions on xylose and consisted primarily of two subpopulations with distinct phenotypes. Clones in the larger subpopulation grew anaerobically on xylose and utilized both xylose and glucose simultaneously in batch culture, but they exhibited impaired growth on glucose. Surprisingly, clones in the smaller subpopulation were incapable of anaerobic growth on xylose. However, as a consequence of their improved xylose catabolism, these clones produced up to 19% more ethanol than the parental TMB3001 strain produced under process-like conditions from a mixture of glucose and xylose.

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BackgroundMethodInfluential
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Background
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Background
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BackgroundSelf-citation
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Background
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Background
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BackgroundInfluential
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Background
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Combining inhibitor tolerance and D-xylose fermentation in industrial Saccharomyces cerevisiae for efficient lignocellulose-based bioethanol production
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“As a result, most progress in this field has been made up to now with unbiased approaches, like mutagenesis, selection and evolutionary engineering, where the underlying genetic changes responsible for the improvement in performance generally remain unknown [16,17,23,24,37-43].”
Background
Stress‐related challenges in pentose fermentation to ethanol by the yeast Saccharomyces cerevisiae
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“strain E2 (18, 19) or a combination of xylose reductase and xylitol dehydrogenase from the yeast Pichia stipitis (10, 24, 27).”
Background
Improvement of xylose fermentation in respiratory-deficient xylose-fermenting Saccharomyces cerevisiae
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“Evolutionary engineering was suggested in previous reports as an effective way to enhance xylose fermentation (Kuyper et al., 2005b; Matsushika et al., 2010; Sonderegger and Sauer, 2003).”
Background
An efficient xylose-fermenting recombinant Saccharomyces cerevisiae strain obtained through adaptive evolution and its global transcription profile
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“stipitis obtained through evolutionary engineering (Sonderegger and Sauer 2003).”
Background
Developments and opportunities in fungal strain engineering for the production of novel enzymes and enzyme cocktails for plant biomass degradation
Kun, R. S., Gomes, A. C. D. S., Hildén, K., Salazar-Cerezo, S., Mäkelä, M., & de Vries, R. P. (2019) · Biotechnology Advances · doi:10.1016/j.biotechadv.2019.02.017 · Cited by 107
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Method
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Adaptive Evolution of a Lactose-Consuming Saccharomyces cerevisiae Recombinant
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“Recombinant strains with the genetic potential to utilize the new substrate (xylose) were subjected to long-term evolution experiments (using chemostats and/or serial batch cultivations), which resulted in improved strains (15, 17, 18, 38, 39).”
Background
Use of population genetics to derive nonrecombinantSaccharomyces cerevisiaestrains that grow using xylose as a sole carbon source
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“…employing genetic engineering, who have found that subsequent application of chemical-mutagenesis and adaptive-culturing methods to recombinant strains of S. cerevisiae results in improved xylose-utilization characteristics (Sonderegger & Sauer, 2003; Wahlbom et al., 2003; Kuyper et al., 2005a).”
Background
Unraveling the genetic basis of xylose consumption in engineered Saccharomyces cerevisiae strains
dos Santos, L. V., Carazzolle, M. F., Nagamatsu, S. T., Sampaio, N. M. V., Almeida, L. D., Pirolla, R. A. S., Borelli, G., Côrrea, T. L. R., Argueso, J. L., & Pereira, G. A. G. (2016) · Scientific Reports · doi:10.1038/srep38676 · Cited by 93
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Increased Ethanol Productivity in Xylose-Utilizing Saccharomyces cerevisiae via a Randomly Mutagenized Xylose Reductase
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“cerevisiae strain employing the XR/XDH pathway (Table 4) (21, 24, 33, 37, 40, 42).”
Bioconversion of lignocellulose-derived sugars to ethanol by engineered Saccharomyces cerevisiae
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“Sonderegger and Sauer (2003) observed that the XYL1-XYL2-XKS expressing S. cerevisiae strain TMB3001, which was incapable of anaerobic growth on xylose, could be slowly adapted to grow on xylose.”
Background
Engineering Saccharomyces cerevisiae for efficient anaerobic xylose fermentation: Reflections and perspectives
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“For instance, strain TMB3001C1 lost 50% of its aerobic glucose growth rate when gaining the ability of anaerobic growth on xylose after evolution [49].”
Background
PHO13 deletion-induced transcriptional activation prevents sedoheptulose accumulation during xylose metabolism in engineered Saccharomyces cerevisiae
Xu, H., Kim, S., Sorek, H., Lee, Y.-S., Jeong, D., Kim, J., Oh, E. J., Yun, E. J., Wemmer, D. E., Kim, K. H., et al. (2015) · Metabolic Engineering · doi:10.1016/j.ymben.2015.12.007 · Cited by 90
“…the most effective metabolic engineering strategies as demonstrated in many studies (Farwick et al., 2014; Kim et al., 2013c; Kuyper et al., 2005b; Lee et al., 2014b; Liu and Hu, 2010; Peng et al., 2015; Peng et al., 2012; Sanchez et al., 2010; Sonderegger and Sauer, 2003; Wisselink et al., 2009).”
Background
Evolutionary engineering of Saccharomyces cerevisiae for efficient aerobic xylose consumption
Scalcinati, G., Otero, J. M., Vleet, J. R. H., Jeffries, T. W., Olsson, L., & Nielsen, J. (2012) · FEMS Yeast Research · doi:10.1111/j.1567-1364.2012.00808.x · Cited by 89
Efficient malic acid production from glycerol with Ustilago trichophora TZ1
Zambanini, T., Sarikaya, E., Kleineberg, W., Buescher, J. M., Meurer, G., Wierckx, N. J. P., & Blank, L. M. (2016) · Biotechnology for Biofuels · doi:10.1186/s13068-016-0483-4 · Cited by 91
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Background
Growth and fermentation of D-xylose by Saccharomyces cerevisiae expressing a novel D-xylose isomerase originating from the bacterium Prevotella ruminicola TC2-24
Hector, R. E., Dien, B. S., Cotta, M. A., & Mertens, J. A. (2013) · Biotechnology for Biofuels · doi:10.1186/1754-6834-6-84 · Cited by 85
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Background
Genome-wide analytical approaches for reverse metabolic engineering of industrially relevant phenotypes in yeast
Oud, B., Maris, A. J. A., Daran, J.-M., & Pronk, J. T. (2012) · FEMS Yeast Research · doi:10.1111/j.1567-1364.2011.00776.x · Cited by 82
“For example, after laboratory evolution of strains for anaerobic growth on pentose sugars or for strongly induced ethanol or acetic acid tolerance (Sonderegger & Sauer, 2003; Stanley et al., 2010a; Wisselink et al., 2010; Wright et al., 2011), the reference strain cannot be grown under the…”
Background
Adaptive evolution of Saccharomyces cerevisiae to generate strains with enhanced glycerol production
Kutyna, D. R., Varela, C., Stanley, G. A., Borneman, A. R., Henschke, P. A., & Chambers, P. J. (2011) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-011-3622-7 · Cited by 83
“…examples illustrating the power of this approach, such as the creation of yeast strains that can anaerobically utilize xylose (Kuyper et al. 2005; Sonderegger and Sauer 2003), yeast with enhanced maltose utilisation and osmotolerance (Higgins et al. 2001), yeast with enhanced ethanol tolerance…”
Background
Stoichiometric network constraints on xylose metabolism by recombinant Saccharomyces cerevisiae
Jin, Y., & Jeffries, T. W. (2004) · Metabolic Engineering · doi:10.1016/j.ymben.2003.11.006 · Cited by 85
“FBA cannot simulate xylose metabolism under anaerobic conditions, which has only recently been demonstrated in mutants of S. cerevisiae expressing XYL1, XYL2 and the S. cerevisiae gene for xylulokinase, XKS1 (Sonderegger and Sauer, 2003).”
BackgroundInfluential
Metabolome, transcriptome and metabolic flux analysis of arabinose fermentation by engineered Saccharomyces cerevisiae
Wisselink, H. W., Cipollina, C., Oud, B., Crimi, B., Heijnen, J. J., Pronk, J. T., & van Maris, A. J. A. (2010) · Metabolic Engineering · doi:10.1016/j.ymben.2010.08.003 · Cited by 81
“cerevisiae strains capable of rapidly fermenting xylose have been developed (Jeppsson et al., 2002; Kuyper et al., 2005a; Sedlak and Ho, 2004; Sonderegger and Sauer, 2003).”
Background
Adaptation of the xylose fermenting yeast Saccharomyces cerevisiae F12 for improving ethanol production in different fed-batch SSF processes
Tomás‐Pejó, E., Ballesteros, M., Oliva, J. M., & Lisbeth Olsson, A. (2010) · Journal of Industrial Microbiology & Biotechnology · doi:10.1007/s10295-010-0768-8 · Cited by 81
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Background
Generation of Novel Wine Yeast Strains by Adaptive Evolution
McBryde, C., Gardner, J. M., Lopes, M. D. B., & Jiranek, V. (2006) · American Journal of Enology and Viticulture · doi:10.5344/ajev.2006.57.4.423 · Cited by 79
Production of aromatics in Saccharomyces cerevisiae—A feasibility study
Krömer, J. O., Núñez, D., Averesch, N. J. H., Hampe, J., Varela, J. A., & Varela, C. (2012) · Journal of Biotechnology · doi:10.1016/j.jbiotec.2012.04.014 · Cited by 77
Directed Enzyme Evolution: Advances and Applications
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Employing a combinatorial expression approach to characterize xylose utilization in Saccharomyces cerevisiae
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Dimensionality reduction for metabolome data using PCA, PLS, OPLS, and RFDA with differential penalties to latent variables
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Chemostat-Based Micro-Array Analysis in Baker's Yeast
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Xylose chemostat isolates of Saccharomyces cerevisiae show altered metabolite and enzyme levels compared with xylose, glucose, and ethanol metabolism of the original strain
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“However, neither of the mutants was capable of growth under anaerobic conditions, unlike the mutant described by Sonderegger and Sauer (2003).”
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Construction of a synthetic YdbK-dependent pyruvate:H2 pathway in Escherichia coli BL21(DE3)
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From Saccharomyces cerevisiae to Ethanol: Unlocking the Power of Evolutionary Engineering in Metabolic Engineering Applications
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“…engineering has been widely used as a powerful strategy to improve the ethanol yield and productivity of not only wild-type, but also recombinant S. cerevisiae strains that have been previously obtained by rational metabolic engineering, as they may usually have low yield and productivity [15–17].”

Authors: Sonderegger, M., & Sauer, U.
Affiliations: ETH Zurich (CH)
Corresponding author: Sauer, Uwe
ORCID: Sauer, Uwe
Venue: Applied and Environmental Microbiology
Publisher: American Society for Microbiology
Published: 2003-04
Volume: 69
Issue: 4
Pages: 1990-1998
ISSN: 0099-2240 (ISSN-L)
1098-5336
DOI: 10.1128/aem.69.4.1990-1998.2003
PMC: PMC154834
OpenAlex: W2115470699
Cited by: 251
References: 38
Citations by year: 2026: 2 · 2025: 6 · 2024: 2 · 2023: 5 · 2022: 3 · 2021: 4 · 2020: 14 · 2019: 6 · 2018: 8 · 2017: 17 · 2016: 13 · 2015: 5 · 2014: 12 · 2013: 14 · 2012: 18
FWCI: 3.68
Type: journal article
Language: en
Open access: green
europepmc.org
Licence: journals.asm.org/non-commercial-tdm-license (tdm)
Locations: Applied and Environmental Microbiology (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: European Commission
Office Fédéral de l'Education et de la Science
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Microbial Metabolic Engineering and Bioproduction
Physical Sciences › Engineering › Biomedical Engineering › Biofuel production and bioconversion
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
Keywords: Saccharomyces cerevisiae, xylose utilization, anaerobic growth, evolutionary engineering, ethanol production, glucose utilization, xylose catabolism, recombinant yeast strains
MeSH terms: Aldehyde Reductase, Anaerobiosis, Culture Media, Genetic Engineering, Pichia, Recombination, Genetic, Saccharomyces cerevisiae, Sugar Alcohol Dehydrogenases, Xylose, Phosphotransferases (Alcohol Group Acceptor), Evolution, Molecular, D-Xylulose Reductase

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Evolutionary Engineering of Saccharomyces cerevisiae for Anaerobic Growth on Xylose

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