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.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“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]
Citations
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
Gombert, A. K., dos Santos, M. M., Christensen, B. B., & Nielsen, J. (2001) · Journal of Bacteriology · doi:10.1128/jb.183.4.1441-1451.2001 · Cited by 348
Dykhuizen, D. E., & Hartl, D. L. (1983) · Microbiological Reviews · doi:10.1128/mr.47.2.150-168.1983 · Cited by 324
Evolutionary Engineering of Industrially Important Microbial Phenotypes
Sauer, U. (2001) · Advances in biochemical engineering, biotechnology · doi:10.1007/3-540-45300-8_7 · Cited by 300
Self-citationUtilization of xylose by bacteria, yeasts, and fungi
Jeffries, T. W. (2005) · Springer eBooks · doi:10.1007/bfb0009101 · Cited by 297
Evolution of Escherichia coli During Growth in a Constant Environment
Helling, R. B., Vargas, C. N., & Adams, J. (1987) · Genetics · doi:10.1093/genetics/116.3.349 · Cited by 283
Treves, D. S., Manning, S. D., & Adams, J. (1998) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a025984 · Cited by 271
Walfridsson, M., Bao, X., Anderlund, M., Lilius, G., Bülow, L., & Hahn‐Hägerdal, B. (1996) · Applied and Environmental Microbiology · doi:10.1128/aem.62.12.4648-4651.1996 · Cited by 252
Toivari, M. H., Aristidou, A. A., Ruohonen, L., & Penttilä, M. E. (2001) · Metabolic Engineering · doi:10.1006/mben.2000.0191 · Cited by 248
Metabolic Engineering of Saccharomyces cerevisiae for Xylose Utilization
Hahn‐Hägerdal, B., Wahlbom, C. F., Gárdonyi, M., van Zyl, W. H., Otero, R. R. C., & Jönsson, L. J. (2001) · Advances in biochemical engineering, biotechnology · doi:10.1007/3-540-45300-8_4 · Cited by 226
Walfridsson, M., Hallborn, J., Penttilä, M., Ker�nen, S., & Hahn-H�gerdal, B. (1995) · Applied and Environmental Microbiology · doi:10.1128/aem.61.12.4184-4190.1995 · Cited by 219
Metabolic-Flux Profiling of the Yeasts Saccharomyces cerevisiae and Pichia stipitis
Fiaux, J., Çakar, Z. P., Sonderegger, M., Kurt Wüthrich, A., Szyperski, T., & Sauer, U. (2003) · Eukaryotic Cell · doi:10.1128/ec.2.1.170-180.2003 · Cited by 160
Self-citationLessons from metabolic engineering for functional genomics and drug discovery
Bailey, J. E. (1999) · Nature Biotechnology · doi:10.1038/10794 · Cited by 153
Ho, N. W. Y., Chen, Z., Brainard, A. P., & Sedlák, M. (1999) · Advances in biochemical engineering, biotechnology · doi:10.1007/3-540-49194-5_7 · Cited by 116
Zaldivar, J., Borges, A., Johansson, B., Smits, H., as, S. V.-B. X. F., Nielsen, J., & Lisbeth Olsson, A. (2002) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-002-1056-y · Cited by 113
Strain selection, taxonomy, and genetics of xylose-fermenting yeasts
Jeffries, T. W., & Kurtzman, C. P. (1994) · Enzyme and Microbial Technology · doi:10.1016/0141-0229(94)90001-9 · Cited by 102
Genetic Engineering for Improved Xylose Fermentation by Yeasts
Jeffries, T. W., & Shi, N. (1999) · Advances in biochemical engineering, biotechnology · doi:10.1007/3-540-49194-5_6 · Cited by 94
Teunissen, A. W. R. H., Dumortier, F. M., Gorwa‐Grauslund, M. F., Bauer, J., Tanghe, A., Loïez, A., Smet, P., Dijck, P. V., & Thevelein, J. M. (2002) · Applied and Environmental Microbiology · doi:10.1128/aem.68.10.4780-4787.2002 · Cited by 80
Screening for L-arabinose fermenting yeasts.
Dien, B. S., Kurtzman, C. P., Badal Chandra, S. A. H. A., & Bothast, R. J. (1996) · PubMed · Cited by 64
Weikert, C., Sauer, U., & Bailey, J. E. (1997) · Microbiology · doi:10.1099/00221287-143-5-1567 · Cited by 63
Self-citationChemostat Approach for the Directed Evolution of Biodesulfurization Gain-of-Function Mutants
Arensdorf, J. J., Loomis, A. K., DiGrazia, P. M., Monticello, D. J., & Pienkos, P. T. (2002) · Applied and Environmental Microbiology · doi:10.1128/aem.68.2.691-698.2002 · Cited by 58
Rohlin, L., Oh, M., & Liao, J. C. (2001) · Current Opinion in Microbiology · doi:10.1016/s1369-5274(00)00213-7 · Cited by 54
Metabolic engineering as an integrating platform for strain development
Stafford, D. E., & Stephanopoulos, G. N. (2001) · Current Opinion in Microbiology · doi:10.1016/s1369-5274(00)00214-9 · Cited by 45
Zelder, O., & Hauer, B. (2000) · Current Opinion in Microbiology · doi:10.1016/s1369-5274(00)00084-9 · Cited by 44
Schneider, K., Jaekel, G., Hoffmann, R., & Giffhorn, F. (1995) · Microbiology · doi:10.1099/13500872-141-8-1865 · Cited by 38
Genetics Society of America 1994 Records, Proceedings and Reports
Roeder, S. (1994) · Genetics · doi:10.1093/genetics/137.4.1 · Cited by 17
O’Kennedy, R. D., & Patching, J. W. (1999) · Journal of Biotechnology · doi:10.1016/s0168-1656(99)00047-4 · Cited by 4
Votruba, J., & Páca, J. (1992) · Folia Microbiologica · doi:10.1007/bf02836618 · Cited by 3
Flagged first, then by citations
1 of the 38 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Ethanol from lignocellulosic biomass: techno-economic performance in short-, middle- and long-term
Hamelinck, C. N., Hooijdonk, G. V., & Faaij, A. P. (2005) · Biomass and Bioenergy · doi:10.1016/j.biombioe.2004.09.002 · Cited by 1,620
Ethanol fermentation from biomass resources: current state and prospects
Lin, Y., & Tanaka, S. (2005) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-005-0229-x · Cited by 1,622
“Therefore, metabolic engineering of xylose fermentation in S. cerevisiae is an attractive approach ( Sonderegger and Sauer 2003 ).”
BackgroundHemicelluloses for fuel ethanol: A review
Gírio, F. M., Fonseca, C., Carvalheiro, F., Duarte, L. C., Marques, S., & Bogel‐Łukasik, R. (2010) · Bioresource Technology · doi:10.1016/j.biortech.2010.01.088 · Cited by 1,648
“mutant subpopulations with distinct and improved characteristics for xylose utilization (Sonderegger and Sauer, 2003).”
BackgroundOutlook for cellulase improvement: Screening and selection strategies
Zhang, Y.-H. P., Himmel, M. E., & Mielenz, J. R. (2006) · Biotechnology Advances · doi:10.1016/j.biotechadv.2006.03.003 · Cited by 1,376
“A Saccharomyces cerevisiae mutant containing several recombinant key intracellular genes for xylose (RS), enzyme location, and substrate solubility. catabolism has been selected to utilize xylose efficiently under anaerobic conditions after 460 generations (Sonderegger and Sauer, 2003).”
Adaptive laboratory evolution—Principles and applications for biotechnology
Dragosits, M., & Mattanovich, D. (2013) · Microbial Cell Factories · doi:10.1186/1475-2859-12-64 · Cited by 827
“cerevisiae in order to achieve increased nutrient utilization and stress resistance [95,113,114].”
Background
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
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review