The DOI matches its Crossref record; 37 of the 38 references it cites were found in a registry or an index.
Evolutionary Engineering of Saccharomyces cerevisiae for Anaerobic Growth on Xylose
Open accessAbstract
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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“In another study it was found that the adaptation to extreme temperature relied on the constitutive expression of GroEL/ES in E. coli[83]”
From Adaptive laboratory evolution—Principles and applications for biotechnology (2013) · cites this paper as [83]
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Cites
Verduyn, C., Postma, E., Scheffers, W. A., & van Dijken, J. P. (1992) · Yeast · doi:10.1002/yea.320080703 · Cited by 1,510
Genetically Engineered Saccharomyces Yeast Capable of Effective Cofermentation of Glucose and Xylose
Ho, N. W. Y., Chen, Z., & Brainard, A. P. (1998) · Applied and Environmental Microbiology · doi:10.1128/aem.64.5.1852-1859.1998 · Cited by 541
Improvement of microbial strains and fermentation processes
Parekh, S. R., Vinci, V. A., & Strobel, R. J. (2000) · Applied Microbiology and Biotechnology · doi:10.1007/s002530000403 · Cited by 536
Xylose fermentation by Saccharomyces cerevisiae
K�tter, P., & Ciriacy, M. (1993) · Applied Microbiology and Biotechnology · doi:10.1007/bf00167144 · Cited by 507
Metabolic Engineering of Saccharomyces cerevisiae
Østergaard, S., Lisbeth Olsson, A., & Nielsen, J. (2000) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.64.1.34-50.2000 · Cited by 462
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
Directed evolution of biocatalysts
Arnold, F. H., & Volkov, A. A. (1999) · Current Opinion in Chemical Biology · doi:10.1016/s1367-5931(99)80010-6 · Cited by 411
Lantz, A. E., Christensson, C., Wahlbom, C. F., & Hahn‐Hägerdal, B. (2000) · Applied and Environmental Microbiology · doi:10.1128/aem.66.8.3381-3386.2000 · Cited by 392
Genome shuffling of Lactobacillus for improved acid tolerance
Patnaik, R., Louie, S., Gavrilovic, V., Perry, K., Stemmer, W. P. C., Ryan, C. M., & del Cardayré, S. B. (2002) · Nature Biotechnology · doi:10.1038/nbt0702-707 · Cited by 377
Rosenzweig, R. F., Sharp, R. R., Treves, D. S., & Adams, J. (1994) · Genetics · doi:10.1093/genetics/137.4.903 · Cited by 357
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Hector, R. E., Mertens, J. A., & Nichols, N. N. (2022) · Fermentation · doi:10.3390/fermentation8120669 · Cited by 4
Silva, C. A. A., & Fonseca, G. G. (2024) · Chemical Engineering Communications · doi:10.1080/00986445.2024.2386310 · Cited by 3
Improving Biomass Sugar Utilization by Engineered Saccharomyces cerevisiae
Matsushika, A., Liu, Z. L., Sawayama, S., & Moon, J. (2011) · Microbiology monographs · doi:10.1007/978-3-642-21467-7_6 · Cited by 3
Evolutionary Engineering of Bacillus for Terephthalic Acid Degradation
Gong, J. X., Li, Z., Li, Q. J., & Zhang, J. F. (2011) · Advanced materials research · doi:10.4028/www.scientific.net/amr.331.148 · Cited by 3
Advances in Biofuel Production by Strain Development in Yeast from Lignocellulosic Biomass
Madhavan, A., Sindhu, R., Arun, K. B., Pandey, A., Binod, P., & Gnansounou, E. (2019) · doi:10.1002/9781119434436.ch14 · Cited by 3
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Bhagat, S. P., Wagh, B. D., Satpute, S. M., Gunjal, M. B., Kasar, S. K., & Roylawar, P. B. (2025) · Clean Energy Production Technologies · doi:10.1007/978-981-96-4636-4_15 · Cited by 2
Evolutionary Adaptation to Enhance Xylose Metabolism in Thermotolerant Kluyveromyces Marxianus
Sharma, N. K., Behera, S., Arora, R., Sharma, A., & Kumar, S. (2025) · Industrial Biotechnology · doi:10.1089/ind.2025.0015 · Cited by 2
“20,21 Jeppsson et al. 22 have obtained the activity 6.07 U/mg for XR in S. cerevisiae TMB2360 grown in xylose as the sole carbon source.”
InfluentialOuahbi, K. E., Asli, A. E., & Benlemlih, M. (2023) · Journal Of Biology Education · doi:10.21043/jobe.v6i2.22893 · Cited by 2
Systems Biology as a Platform for Wine Yeast Strain Development
Borneman, A. R., Chambers, P. J., & Pretorius, I. S. (2008) · Springer eBooks · doi:10.1007/978-3-540-85463-0_22 · Cited by 2
Maury, J., Asadollahi, M. A., Formenti, L. R., Schalk, M., & Nielsen, J. (2012) · Springer eBooks · doi:10.1007/978-1-4614-4063-5_6 · Cited by 2
Ethanol Production from Xylose Through GM Saccharomyces cerevisiae
Aggarwal, N. K., Kumar, N., & Mittal, M. (2022) · Green chemistry and sustainable technology · doi:10.1007/978-3-031-05091-6_12 · Cited by 2
Pastorella, G. (2014) · Arrow@dit (Dublin Institute of Technology) · Cited by 2
Impact of xylose and mannose on central metabolism of yeast Saccharomyces cerevisiae
Pitkänen, J. (2005) · Aaltodoc (Aalto University) · Cited by 1
Ethanol Tolerance and Production by Yeasts
Garrigues, S., & Salazar-Cerezo, S. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-819990-9.00023-8 · Cited by 2
Advancing Metabolic Engineering through Combination of Systems Biology and Adaptive Evolution
Hong, K.-K. (2012) · Chalmers Publication Library (Chalmers University of Technology) · Cited by 2
Microbial Pigments as Bio-based Dyes in Textile
Qasim, F., Ali, W., Niaz, K., Ahmad, M. S., Bento, H. B. S., & Irfan, M. (2025) · SDGs and textiles · doi:10.1007/978-981-95-0347-6_3 · Cited by 1
Fernandes, T., Sousa, M. J., & Franco‐Duarte, R. (2026) · Food Bioscience · doi:10.1016/j.fbio.2026.108871 · Cited by 1
Klimacek, M. (2012) · InTech eBooks · doi:10.5772/31689 · Cited by 1
“Metabolic Engineering of Microbial Cell Factories Exemplified by the Baker’s Yeast 23 2009; Cakar et al. 2005; Garcia Sanchez et al. 2010; Kuyper et al. 2005; Sonderegger and Sauer 2003; Wisselink et al. 2009).”
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Sherlock, G. J., Rosenzweig, R., Levine, R. P., Dunn, B. L., & Schwartz, K. (2005) · Cited by 1
Yuan, D. (2010) · OhioLink ETD Center (Ohio Library and Information Network) · Cited by 1
Recombinant strains of Saccharomyces cerevisiae for ethanol production from plant biomass
Розанов, А. С., Kotenko, A. V., Akberdin, I. R., & Peltek, S. E. (2015) · Russian Journal of Genetics Applied Research · doi:10.1134/s2079059715040139 · Cited by 1
“These approaches were also applied to the yeast strains expressing xylose reductase, xylitol dehydrogenase (Sonderegger and Sauer, 2003), and xylose isomerase (Kuyper et al., 2004).”
MethodAdvanced Technologies and Mechanisms for Yeast Evolutionary Engineering
Ryu, H. (2020) · Microbiology and Biotechnology Letters · doi:10.48022/mbl.2009.09004 · Cited by 1
Blaby, I. K., de Crécy‐Lagard, V., & Lyons, T. J. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-809633-8.09021-x · Cited by 1
Blaby, I. K., de Crécy‐Lagard, V., & Lyons, T. J. (2011) · Elsevier eBooks · doi:10.1016/b978-0-08-088504-9.00034-9 · Cited by 1
Kawanishi, Y., & Matsunaga, S. (2021) · CYTOLOGIA · doi:10.1508/cytologia.86.277 · Cited by 1
“In addition, Adaptive Laboratory Evolution (ALE) was developed, which uses chemostats to limit the organic carbon source and perform gradual selection (Sonderegger and Sauer 2003, Blount et al. 2012).”
MethodA Microbial Perspective on Ethanolic Lignocellulose Fermentation
Parachin, N. S., Hahn‐Hägerdal, B., & Bettiga, M. (2011) · Elsevier eBooks · doi:10.1016/b978-0-444-64046-8.00379-7 · Cited by 1
Molecular basis of stress resistance in Saccharomyces cerevisiae
Heer, D. (2009) · Repository for Publications and Research Data (ETH Zurich) · doi:10.3929/ethz-a-006032739 · Cited by 1
Strain Improvement via Evolutionary Engineering
Kim, B., Du, J., & Zhao, H. (2012) · Wiley eBooks · doi:10.1002/9781118433034.ch4
Energy Metabolism of Cells Used for Industrial Production
Butler, M., Sparling, R., & Court, D. A. (2010) · Wiley eBooks · doi:10.1002/9780470054581.eib269
Shaheed, S. M., Rohit, J. P., Madhan, R., & Selvakumar, K. (2011) · Nature Precedings · doi:10.1038/npre.2011.6579.1
Metabolic Engineering of Saccharomyces cerevisiae for Sesquiterpene Production
Scalcinati, G. (2012) · Chalmers Publication Library (Chalmers University of Technology)
Malán, A. K., Fagúndez, A., Gill, P. R., & Batista, S. B. (2016) · Springer eBooks · doi:10.1007/978-981-10-2555-6_3
Caspeta, L., & Castillo, T. (2017) · Springer eBooks · doi:10.1007/978-3-319-51729-2_2
“Adaptive laboratory evolution of this strain over 460 generations on, consecutively, aerobic, microaerobic and anaerobic serial cultivations allowed for the generation of strains able to utilize xylose under anaerobic conditions (Sonderegger and Sauer 2003).”
BackgroundEngineering saccharomyces for biofuel production improvement
Qiu, Z. (2017) · DR-NTU (Nanyang Technological University) · doi:10.32657/10356/72681
Probiotic microbe activity for application as anti- fungal and feed intake rate of ruminants
Ali, S. I. S., & Imranudin, S. (2015)
Genetic Engineering of Yeast with Novel Properties Using Localized Hypermutation
Xhialli, B. (2020) · uO Research (University of Ottawa) · doi:10.20381/ruor-24765
OBSOLETE: Genetic Engineering for Strain Improvement in Filamentous Fungi
Garrigues, S. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-809633-8.00006-6
Evolutionary tools in metabolic engineering
Schmidt‐Dannert, C. (2009)
Metabolic and evolutionary engineering of a xylose-fermenting strain of Saccharomyces cerevisiae
Pechacek, J. (2011) · Spectrum Research Repository (Concordia University)
(2003) · Yeast · doi:10.1002/yea.948
(2012) · Wiley eBooks · doi:10.1002/9781118414514.refs
Microbial Colorants: Past, Present and Future
Maiti, S., & Adivarekar, R. V. (2025) · Springer eBooks · doi:10.1007/978-981-96-5091-0_9
Conversion of Komagataella phaffii Biomass Waste to Yeast Extract Supplement
Murphy, L., & O’Connell, D. J. (2025) · Applied Microbiology · doi:10.3390/applmicrobiol5030095
“Wet cell biomass yields were approximately 2.17 g wet biomass per gram of glucose consumed for the YPD-C and YPD + 2% peptone formulations, closely matching the literature benchmarks of around 2.0–2.5 g wet biomass per gram of glucose for yeast grown in rich media [33–35].”
InfluentialLactose fermentation by recombinant Saccharomyces cerevisiae strains
Guimarães, P. M. R., Teixeira, J. A., & Domingues, L. (2008) · Portuguese National Funding Agency for Science, Research and Technology (RCAAP Project by FCT)
Adaptive evolution of a lactose-consuming Saccharomyces cerevisiae recombinant
Guimarães, P. M. R., François, J., Parrou, J., Teixeira, J. A., & Domingues, L. (2007) · Portuguese National Funding Agency for Science, Research and Technology (RCAAP Project by FCT)
Cadière, A. (2010) · theses.fr (ABES) · doi:10.70675/71b2c9a3zd6f1z4ebdzb945z9d8ab613075d
Stress resistance during the lag phase of wine fermentation and development of optimized yeasts
Ferreira, D. (2017) · theses.fr (ABES) · doi:10.70675/da4d4ca2za700z46bdz95edz3ee2390171c0
Genetic Improvement of a Wild-Type Saccharomyces cerevisiae Strain for Enhanced Xylitol Production
Lagos, M. A. P., Pinzón, D. C. T., Caviativa, J. A. C., Velásquez-Lozano, M. E., & Stambuk, B. U. (2026) · Fermentation · doi:10.3390/fermentation12080354
Screening of Dual Defects Strain and Effects on l-Isoleucine Production in Escherichia coli NML
Yu, L., Liu, H., Fang, H., & Wu, Q. Y. (2015) · Lecture notes in electrical engineering · doi:10.1007/978-3-662-46318-5_15
Metadata
- 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
- 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
- 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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