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Novel Evolutionary Engineering Approach for Accelerated Utilization of Glucose, Xylose, and Arabinose Mixtures by Engineered Saccharomyces cerevisiae Strains
Open accessAbstract
Lignocellulosic feedstocks are thought to have great economic and environmental significance for future biotechnological production processes. For cost-effective and efficient industrial processes, complete and fast conversion of all sugars derived from these feedstocks is required. Hence, simultaneous or fast sequential fermentation of sugars would greatly contribute to the efficiency of production processes. One of the main challenges emerging from the use of lignocellulosics for the production of ethanol by the yeast Saccharomyces cerevisiae is efficient fermentation of d -xylose and l -arabinose, as these sugars cannot be used by natural S. cerevisiae strains. In this study, we describe the first engineered S. cerevisiae strain (strain IMS0003) capable of fermenting mixtures of glucose, xylose, and arabinose with a high ethanol yield (0.43 g g −1 of total sugar) without formation of the side products xylitol and arabinitol. The kinetics of anaerobic fermentation of glucose-xylose-arabinose mixtures were greatly improved by using a novel evolutionary engineering strategy. This strategy included a regimen consisting of repeated batch cultivation with repeated cycles of consecutive growth in three media with different compositions (glucose, xylose, and arabinose; xylose and arabinose; and only arabinose) and allowed rapid selection of an evolved strain (IMS0010) exhibiting improved specific rates of consumption of xylose and arabinose. This evolution strategy resulted in a 40% reduction in the time required to completely ferment a mixture containing 30 g liter −1 glucose, 15 g liter −1 xylose, and 15 g liter −1 arabinose.
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“whereas a similar study with a different selection procedure identified mutations in glpF and fabA, accompanied with increased membrane fatty acid saturation as critical factors towards increased thermo-tolerance [90].”
From Adaptive laboratory evolution—Principles and applications for biotechnology (2013) · cites this paper as [90]
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Verduyn, C., Postma, E., Scheffers, W. A., & van Dijken, J. P. (1992) · Yeast · doi:10.1002/yea.320080703 · Cited by 1,510
A review of the production of ethanol from softwood
Galbe, M., & Zacchi, G. (2002) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-002-1058-9 · Cited by 1,112
Zaldivar, J., Nielsen, J., & Lisbeth Olsson, A. (2001) · Applied Microbiology and Biotechnology · doi:10.1007/s002530100624 · Cited by 953
Towards industrial pentose-fermenting yeast strains
Hahn‐Hägerdal, B., Karhumaa, K., Fonseca, C., Spencer‐Martins, I., & Gorwa‐Grauslund, M. F. (2007) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-006-0827-2 · Cited by 784
Lynd, L. R. (1996) · Annual Review of Energy and the Environment · doi:10.1146/annurev.energy.21.1.403 · Cited by 775
Innovations and Green Chemistry
Horváth, I. T., & Anastas, P. T. (2007) · Chemical Reviews · doi:10.1021/cr078380v · Cited by 761
Andreasen, A. A., & Stier, T. J. B. (1953) · Journal of Cellular and Comparative Physiology · doi:10.1002/jcp.1030410103 · Cited by 555
van Maris, A. J. A., Abbott, D. A., Bellissimi, E., van den Brink, J., Kuyper, M., Luttik, M. A. H., Wisselink, H. W., Scheffers, W. A., van Dijken, J. P., & Pronk, J. T. (2006) · Antonie van Leeuwenhoek · doi:10.1007/s10482-006-9085-7 · Cited by 546
Self-citationPhysiology of Saccharomyces Cerevisiae in Anaerobic Glucose-Limited Chemostat Culturesx
Verduyn, C., Postma, E., Scheffers, W. A., & van Dijken, J. P. (1990) · Journal of General Microbiology · doi:10.1099/00221287-136-3-395 · Cited by 471
Metabolic engineering applications to renewable resource utilization
Aristidou, A. A., & Penttilä, M. E. (2000) · Current Opinion in Biotechnology · doi:10.1016/s0958-1669(00)00085-9 · Cited by 452
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Martin‐Yken, H., Ribaud, V., Poli, J., Hoareau‐Aveilla, C., Spichal, M., Beaufort, S., Tilloy, V., Delerue, T., Capp, J., & Parrou, J. (2012) · Research in Microbiology · doi:10.1016/j.resmic.2012.05.007
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Caspeta, L., & Castillo, T. (2017) · Springer eBooks · doi:10.1007/978-3-319-51729-2_2
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Nijland, J. G., Zhang, X., & Driessen, A. J. M. (2024) · Figshare · doi:10.6084/m9.figshare.26583006
Cadière, A. (2010) · theses.fr (ABES) · doi:10.70675/71b2c9a3zd6f1z4ebdzb945z9d8ab613075d
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Metadata
- Authors
- Wisselink, H. W., Toirkens, M. J., Wu, Q., Pronk, J. T., & van Maris, A. J. A.
- Affiliations
- Delft University of Technology (NL)
- Department of Biotechnology, Delft University of Technology, Julianalaan 67, 2628 BC Delft, The Netherlands
- ORCID
- Pronk, Jack T.
- Venue
- Applied and Environmental Microbiology
- Publisher
- American Society for Microbiology
- Published
- 2009-02-15
- Volume
- 75
- Issue
- 4
- Pages
- 907-914
- ISSN
- 0099-2240 (ISSN-L)
- 1098-5336
- PMC
- PMC2643596
- OpenAlex
- W2146497852
- Cited by
- 247
- References
- 28
- Citations by year
- 2026: 5 · 2025: 3 · 2024: 3 · 2023: 4 · 2022: 5 · 2021: 5 · 2020: 12 · 2019: 18 · 2018: 15 · 2017: 22 · 2016: 13 · 2015: 16 · 2014: 19 · 2013: 25 · 2012: 23
- FWCI
- 13.04
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Applied and Environmental Microbiology (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Research Repository (Delft University of Technology) (submittedVersion)
- Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
- Topics
- Physical Sciences › Engineering › Biomedical Engineering › Biofuel production and bioconversion
- 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
- Keywords
- Saccharomyces cerevisiae, xylose fermentation, arabinose fermentation, lignocellulosic biomass, ethanol production, evolutionary engineering, adaptive laboratory evolution, xylitol, arabinitol, fermentation kinetics
- MeSH terms
- Ethanol, Anaerobiosis, Arabinose, Fermentation, Glucose, Lignin, Saccharomyces cerevisiae, Xylitol, Xylose
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