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.
Integrity signals
Registry
Cites
Statistics
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?
Adaptation to extreme temperature relied on the constitutive expression of GroEL/ES in E. coli.
“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]
Cites
Verduyn, C., Postma, E., Scheffers, W. A., & van Dijken, J. P. (1992) · Yeast · doi:10.1002/yea.320080703 · Cited by 1,510 · see citing works
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 · see citing works
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 · see citing works
Xylose fermentation by Saccharomyces cerevisiae
K�tter, P., & Ciriacy, M. (1993) · Applied Microbiology and Biotechnology · doi:10.1007/bf00167144 · Cited by 507 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
Rosenzweig, R. F., Sharp, R. R., Treves, D. S., & Adams, J. (1994) · Genetics · doi:10.1093/genetics/137.4.903 · Cited by 357 · see citing works
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 · see citing works
Dykhuizen, D. E., & Hartl, D. L. (1983) · Microbiological Reviews · doi:10.1128/mr.47.2.150-168.1983 · Cited by 324 · see citing works
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 297 · see citing works
Self-citationUtilization of xylose by bacteria, yeasts, and fungi
Jeffries, T. W. (2005) · Springer eBooks · doi:10.1007/bfb0009101 · Cited by 291 · see citing works
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 · see citing works
Treves, D. S., Manning, S. D., & Adams, J. (1998) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a025984 · Cited by 271 · see citing works
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 · see citing works
Toivari, M. H., Aristidou, A. A., Ruohonen, L., & Penttilä, M. E. (2001) · Metabolic Engineering · doi:10.1006/mben.2000.0191 · Cited by 248 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
Self-citationLessons from metabolic engineering for functional genomics and drug discovery
Bailey, J. E. (1999) · Nature Biotechnology · doi:10.1038/10794 · Cited by 153 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
Weikert, C., Sauer, U., & Bailey, J. E. (1997) · Microbiology · doi:10.1099/00221287-143-5-1567 · Cited by 63 · see citing works
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 · see citing works
Rohlin, L., Oh, M., & Liao, J. C. (2001) · Current Opinion in Microbiology · doi:10.1016/s1369-5274(00)00213-7 · Cited by 54 · see citing works
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 · see citing works
Zelder, O., & Hauer, B. (2000) · Current Opinion in Microbiology · doi:10.1016/s1369-5274(00)00084-9 · Cited by 44 · see citing works
Schneider, K., Jaekel, G., Hoffmann, R., & Giffhorn, F. (1995) · Microbiology · doi:10.1099/13500872-141-8-1865 · Cited by 38 · see citing works
Genetics Society of America 1994 Records, Proceedings and Reports
Roeder, S. (1994) · Genetics · doi:10.1093/genetics/137.4.1 · Cited by 17 · see citing works
O’Kennedy, R. D., & Patching, J. W. (1999) · Journal of Biotechnology · doi:10.1016/s0168-1656(99)00047-4 · Cited by 4 · see citing works
Votruba, J., & Páca, J. (1992) · Folia Microbiologica · doi:10.1007/bf02836618 · Cited by 3 · see citing works
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 · see citing works
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 · see citing works
Hemicelluloses 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 1,590 · see citing works
Outlook 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 1,349 · see citing works
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 · see citing works
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 · see citing works
Technological trends, global market, and challenges of bio-ethanol production
Mussatto, S. I., Dragone, G., Guimarães, P. M. R., Silva, J. P. A., Carneiro, L. M., Roberto, I. C., Vicente, A. A., Domingues, L., & Teixeira, J. A. (2010) · Biotechnology Advances · doi:10.1016/j.biotechadv.2010.07.001 · Cited by 730 · see citing works
Progress in Metabolic Engineering of Saccharomyces cerevisiae
Nevoigt, E. (2008) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00025-07 · Cited by 597 · see citing works
Sandberg, T. E., Salazar, M. J., Weng, L. L., Palsson, B. Ø., & Feist, A. M. (2019) · Metabolic Engineering · doi:10.1016/j.ymben.2019.08.004 · Cited by 558 · see citing works
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 · see citing works
Conversion of Escherichia coli to Generate All Biomass Carbon from CO2
Gleizer, S., Ben-Nissan, R., Bar‐On, Y. M., Antonovsky, N., Noor, Ε., Zohar, Y., Jona, G., Krieger, E., Shamshoum, M., Bar‐Even, A., et al. (2019) · Cell · doi:10.1016/j.cell.2019.11.009 · Cited by 528 · see citing works
Engineering yeasts for xylose metabolism
Jeffries, T. W. (2006) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2006.05.008 · Cited by 517 · see citing works
Metabolic engineering for improved fermentation of pentoses by yeasts
Jeffries, T. W., & Jin, Y. (2004) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-003-1450-0 · Cited by 501 · see citing works
Improving industrial yeast strains: exploiting natural and artificial diversity
Steensels, J., Snoek, T., Meersman, E., Nicolino, M. P., Voordeckers, K., & Verstrepen, K. J. (2014) · FEMS Microbiology Reviews · doi:10.1111/1574-6976.12073 · Cited by 486 · see citing works
Bacterial pigments and their applications
Venil, C. K., Zakaria, Z. A., & Ahmad, W. A. (2013) · Process Biochemistry · doi:10.1016/j.procbio.2013.06.006 · Cited by 465 · see citing works
Utilization of bioresources for sustainable biofuels: A Review
Gaurav, N., Sivasankari, S., Kiran, G., Ninawe, A., & Selvin, J. (2017) · Renewable and Sustainable Energy Reviews · doi:10.1016/j.rser.2017.01.070 · Cited by 443 · see citing works
Matsushika, A., Inoue, H., Kodaki, T., & Sawayama, S. (2009) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-009-2101-x · Cited by 439 · see citing works
Lignocellulosic Agricultural Waste Valorization to Obtain Valuable Products: An Overview
Blasi, A., Verardi, A., Lopresto, C. G., Siciliano, S., & Sangiorgio, P. (2023) · Recycling · doi:10.3390/recycling8040061 · Cited by 371 · see citing works
Evolutionary engineering of mixed-sugar utilization by a xylose-fermenting strain
KUYPER, M., TOIRKENS, M., DIDERICH, J., WINKLER, A., VANDIJKEN, J., & PRONK, J. (2005) · FEMS Yeast Research · doi:10.1016/j.femsyr.2005.04.004 · Cited by 341 · see citing works
Production of recombinant proteins by yeast cells
Çelik, E., & Çalı́k, P. (2011) · Biotechnology Advances · doi:10.1016/j.biotechadv.2011.09.011 · Cited by 338 · see citing works
Demeke, M. M., Dietz, H., Li, Y., Foulquié-Moreno, M. R., Mutturi, S., Deprez, S., Abt, T. D., Bonini, B. M., Lidén, G., Dumortier, F. M., et al. (2013) · Biotechnology for Biofuels · doi:10.1186/1754-6834-6-89 · Cited by 331 · see citing works
Xylose Fermentation by Saccharomyces cerevisiae: Challenges and Prospects
Moysés, D. N., Reis, V., de Almeida, J. R. M., de Moraes, L. M. P., & Torres, F. A. G. (2016) · International Journal of Molecular Sciences · doi:10.3390/ijms17030207 · Cited by 328 · see citing works
Adaptive laboratory evolution — harnessing the power of biology for metabolic engineering
Portnoy, V. A., Bezdan, D., & Zengler, K. (2011) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2011.03.007 · Cited by 309 · see citing works
Functional Expression of a Bacterial Xylose Isomerase in Saccharomyces cerevisiae
Brat, D., Boles, E., & Wiedemann, B. (2009) · Applied and Environmental Microbiology · doi:10.1128/aem.02522-08 · Cited by 291 · see citing works
Zhou, H., Cheng, J.-S., Wang, B. L., Fink, G. R., & Stephanopoulos, G. (2012) · Metabolic Engineering · doi:10.1016/j.ymben.2012.07.011 · Cited by 287 · see citing works
Metabolic Engineering for Pentose Utilization in Saccharomyces cerevisiae
Hahn‐Hägerdal, B., Karhumaa, K., Jeppsson, M., & Gorwa‐Grauslund, M. F. (2007) · Springer eBooks · doi:10.1007/10_2007_062 · Cited by 280 · see citing works
Adaptive laboratory evolution principles and applications in industrial biotechnology
Mavrommati, M., Daskalaki, A., Papanikolaou, S., & Aggelis, G. (2021) · Biotechnology Advances · doi:10.1016/j.biotechadv.2021.107795 · Cited by 269 · see citing works
Hasunuma, T., & Kondo, A. (2011) · Biotechnology Advances · doi:10.1016/j.biotechadv.2011.10.011 · Cited by 259 · see citing works
Minimal metabolic engineering of for efficient anaerobic xylose fermentation: a proof of principle
Kuyper, M., Winkler, A. A., VANDIJKEN, J., & Pronk, J. T. (2004) · FEMS Yeast Research · doi:10.1016/j.femsyr.2004.01.003 · Cited by 261 · see citing works
Strain engineering of Saccharomyces cerevisiae for enhanced xylose metabolism
Kim, S. R., Park, Y., Jin, Y., & Seo, J. (2013) · Biotechnology Advances · doi:10.1016/j.biotechadv.2013.03.004 · Cited by 250 · see citing works
Wisselink, H. W., Toirkens, M. J., Wu, Q., Pronk, J. T., & van Maris, A. J. A. (2009) · Applied and Environmental Microbiology · doi:10.1128/aem.02268-08 · Cited by 247 · see citing works
van Maris, A. J. A., Winkler, A. A., Kuyper, M., de Laat, W. T. A. M., van Dijken, J. P., & Pronk, J. T. (2007) · Advances in biochemical engineering, biotechnology · doi:10.1007/10_2007_057 · Cited by 245 · see citing works
Enhanced biofuel production through coupled acetic acid and xylose consumption by engineered yeast
Wei, N., Quarterman, J., Kim, S. R., Cate, J. H. D., & Jin, Y. (2013) · Nature Communications · doi:10.1038/ncomms3580 · Cited by 243 · see citing works
Genetic improvement of Saccharomyces cerevisiae for xylose fermentation
Chu, B. C. H., & Lee, H. (2007) · Biotechnology Advances · doi:10.1016/j.biotechadv.2007.04.001 · Cited by 241 · see citing works
Role of cultivation media in the development of yeast strains for large scale industrial use
Hahn‐Hägerdal, B., Karhumaa, K., Larsson, C. U., Gorwa‐Grauslund, M. F., Görgens, J. F., & van Zyl, W. H. (2005) · Microbial Cell Factories · doi:10.1186/1475-2859-4-31 · Cited by 237 · see citing works
Engineering tolerance to industrially relevant stress factors in yeast cell factories
Deparis, Q., Claes, A., Foulquié-Moreno, M. R., & Thevelein, J. M. (2017) · FEMS Yeast Research · doi:10.1093/femsyr/fox036 · Cited by 231 · see citing works
Chen, X., Zhou, L., Tian, K., Kumar, A., Singh, S., Prior, B. A., & Wang, Z. (2013) · Biotechnology Advances · doi:10.1016/j.biotechadv.2013.02.009 · Cited by 224 · see citing works
Jansen, M. L. A., Bracher, J. M., Papapetridis, I., Verhoeven, M. D., de Bruijn, H., de Waal, P. P., van Maris, A. J. A., Klaassen, P., & Pronk, J. T. (2017) · FEMS Yeast Research · doi:10.1093/femsyr/fox044 · Cited by 217 · see citing works
Saloheimo, A., Rauta, J., Stasyk, O. V., Sibirny, A. А., Penttilä, M. E., & Ruohonen, L. (2006) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-006-0747-1 · Cited by 210 · see citing works
Wisselink, H. W., Toirkens, M. J., del Rosario Franco Berriel, M., Winkler, A. A., van Dijken, J. P., Pronk, J. T., & van Maris, A. J. A. (2007) · Applied and Environmental Microbiology · doi:10.1128/aem.00177-07 · Cited by 209 · see citing works
Evolutionary engineering of multiple-stress resistant
Çakar, Z. P., Şeker, U. Ö. Ş., Tamerler, C., Sonderegger, M., & Sauer, U. (2004) · FEMS Yeast Research · doi:10.1016/j.femsyr.2004.10.010 · Cited by 208 · see citing works
Self-citationBioethanol production from pentose sugars: Current status and future prospects
Kuhad, R. C., Gupta, R., Khasa, Y. P., Singh, A., & Zhang, Y.-H. P. (2011) · Renewable and Sustainable Energy Reviews · doi:10.1016/j.rser.2011.07.058 · Cited by 205 · see citing works
Wenger, J. W., Schwartz, K., & Sherlock, G. J. (2010) · PLoS Genetics · doi:10.1371/journal.pgen.1000942 · Cited by 201 · see citing works
Fong, S. S., Nanchen, A., Palsson, B. Ø., & Sauer, U. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m510016200 · Cited by 189 · see citing works
Self-citationSaccharomyces cerevisiae Engineered for Xylose Metabolism Exhibits a Respiratory Response
Jin, Y., Laplaza, J. M., & Jeffries, T. W. (2004) · Applied and Environmental Microbiology · doi:10.1128/aem.70.11.6816-6825.2004 · Cited by 178 · see citing works
Bengtsson, O., Hahn‐Hägerdal, B., & Gorwa‐Grauslund, M. F. (2009) · Biotechnology for Biofuels · doi:10.1186/1754-6834-2-9 · Cited by 168 · see citing works
A rare sugar xylitol. Part I: the biochemistry and biosynthesis of xylitol
Granström, T. B., Izumori, K., & LEISOLA, M. S. A. (2007) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-006-0761-3 · Cited by 160 · see citing works
Evolutionary engineering of Saccharomyces cerevisiae for improved industrially important properties
Çakar, Z. P., Turanlı-Yıldız, B., Alkım, C., & Yılmaz, Ü. (2011) · FEMS Yeast Research · doi:10.1111/j.1567-1364.2011.00775.x · Cited by 152 · see citing works
Sánchez, R. G., Karhumaa, K., Fonseca, C., Nogué, V. S. I., de Almeida, J. R. M., Larsson, C. U., Bengtsson, O., Bettiga, M., Hahn‐Hägerdal, B., & Gorwa‐Grauslund, M. F. (2010) · Biotechnology for Biofuels · doi:10.1186/1754-6834-3-13 · Cited by 149 · see citing works
Sonderegger, M., Jeppsson, M., Larsson, C., Gorwa‐Grauslund, M. F., Boles, E., Lisbeth Olsson, A., Spencer‐Martins, I., Hahn‐Hägerdal, B., & Sauer, U. (2004) · Biotechnology and Bioengineering · doi:10.1002/bit.20094 · Cited by 144 · see citing works
Self-citationGenome shuffling: Progress and applications for phenotype improvement
Gong, J., Zheng, H., Wu, Z., Chen, T., & Zhao, X. (2009) · Biotechnology Advances · doi:10.1016/j.biotechadv.2009.05.016 · Cited by 144 · see citing works
Cadière, A., Ortiz-Julien, A., Camarasa, C., & Dequin, S. (2011) · Metabolic Engineering · doi:10.1016/j.ymben.2011.01.008 · Cited by 141 · see citing works
Sonderegger, M., Jeppsson, M., Hahn‐Hägerdal, B., & Sauer, U. (2004) · Applied and Environmental Microbiology · doi:10.1128/aem.70.4.2307-2317.2004 · Cited by 140 · see citing works
Self-citationMicrobiological approaches to lowering ethanol concentration in wine
Kutyna, D. R., Varela, C., Henschke, P. A., Chambers, P. J., & Stanley, G. A. (2010) · Trends in Food Science & Technology · doi:10.1016/j.tifs.2010.03.004 · Cited by 136 · see citing works
Current Status and Applications of Adaptive Laboratory Evolution in Industrial Microorganisms
Lee, S., & Kim, P. (2020) · Journal of Microbiology and Biotechnology · doi:10.4014/jmb.2003.03072 · Cited by 127 · see citing works
Sonderegger, M., Schümperli, M., & Sauer, U. (2004) · Applied and Environmental Microbiology · doi:10.1128/aem.70.5.2892-2897.2004 · Cited by 127 · see citing works
Self-citationEngineering Complex Phenotypes in Industrial Strains
Patnaik, R. (2007) · Biotechnology Progress · doi:10.1021/bp0701214 · Cited by 124 · see citing works
Food additives: production of microbial pigments and their antioxidant properties
Nigam, P. S. N., & Luke, J. S. (2016) · Current Opinion in Food Science · doi:10.1016/j.cofs.2016.02.004 · Cited by 124 · see citing works
Engineering of Saccharomyces cerevisiae for the efficient co-utilization of glucose and xylose
Hou, J., Qiu, C., Shen, Y., Li, H., & Bao, X. (2017) · FEMS Yeast Research · doi:10.1093/femsyr/fox034 · Cited by 123 · see citing works
Opportunities for yeast metabolic engineering: Lessons from synthetic biology
Krivoruchko, A., Siewers, V., & Nielsen, J. (2011) · Biotechnology Journal · doi:10.1002/biot.201000308 · Cited by 121 · see citing works
Laluce, C., Schenberg, A. C. G., Gallardo, J. C. M., Coradello, L. F. C., & Sponchiado, S. R. P. (2012) · Applied Biochemistry and Biotechnology · doi:10.1007/s12010-012-9619-6 · Cited by 133 · see citing works
Engineering primary metabolic pathways of industrial micro-organisms
Kern, A., Tilley, E., Hunter, I. S., Legiša, M., & Glieder, A. (2006) · Journal of Biotechnology · doi:10.1016/j.jbiotec.2006.11.021 · Cited by 116 · see citing works
Demeke, M. M., Dumortier, F. M., Li, Y., Broeckx, T., Foulquié-Moreno, M. R., & Thevelein, J. M. (2013) · Biotechnology for Biofuels · doi:10.1186/1754-6834-6-120 · Cited by 116 · see citing works
Stress‐related challenges in pentose fermentation to ethanol by the yeast Saccharomyces cerevisiae
de Almeida, J. R. M., Runquist, D., Nogué, V. S. I., Lidén, G., & Gorwa‐Grauslund, M. F. (2011) · Biotechnology Journal · doi:10.1002/biot.201000301 · Cited by 111 · see citing works
Wiedemann, B., & Boles, E. (2008) · Applied and Environmental Microbiology · doi:10.1128/aem.02395-07 · Cited by 113 · see citing works
Peng, B., Shen, Y., Li, X., Chen, X. D., Hou, J., & Bao, X. (2011) · Metabolic Engineering · doi:10.1016/j.ymben.2011.12.001 · Cited by 113 · see citing works
Shen, Y., Chen, X. D., Peng, B., Chen, L., Hou, J., & Bao, X. (2012) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-012-4418-0 · Cited by 112 · see citing works
Xylose fermentation as a challenge for commercialization of lignocellulosic fuels and chemicals
Nogué, V. S. I., & Karhumaa, K. (2014) · Biotechnology Letters · doi:10.1007/s10529-014-1756-2 · Cited by 110 · see citing works
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 · see citing works
Recent advances in the evolutionary engineering of industrial biocatalysts
Winkler, J. D., & Kao, K. C. (2014) · Genomics · doi:10.1016/j.ygeno.2014.09.006 · Cited by 103 · see citing works
Wright, J., Bellissimi, E., de Hulster, E., Wagner, A., Pronk, J. T., & van Maris, A. J. A. (2011) · FEMS Yeast Research · doi:10.1111/j.1567-1364.2011.00719.x · Cited by 98 · see citing works
Lachancea thermotolerans, the Non-Saccharomyces Yeast that Reduces the Volatile Acidity of Wines
Vilela, A. (2018) · Fermentation · doi:10.3390/fermentation4030056 · Cited by 100 · see citing works
Adaptive Evolution of a Lactose-Consuming Saccharomyces cerevisiae Recombinant
Guimarães, P. M. R., François, J., Parrou, J. L., Teixeira, J. A., & Domingues, L. (2008) · Applied and Environmental Microbiology · doi:10.1128/aem.00186-08 · Cited by 96 · see citing works
Attfield, P. V., & Bell, P. (2006) · FEMS Yeast Research · doi:10.1111/j.1567-1364.2006.00098.x · Cited by 96 · see citing works
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 · see citing works
Runquist, D., Hahn‐Hägerdal, B., & Bettiga, M. (2010) · Applied and Environmental Microbiology · doi:10.1128/aem.01505-10 · Cited by 94 · see citing works
Bioconversion of lignocellulose-derived sugars to ethanol by engineered Saccharomyces cerevisiae
Madhavan, A., Srivastava, A., Kondo, A., & Bisaria, V. S. (2011) · Critical Reviews in Biotechnology · doi:10.3109/07388551.2010.539551 · Cited by 93 · see citing works
Cai, Z., Zhang, B., & Li, Y. (2011) · Biotechnology Journal · doi:10.1002/biot.201100053 · Cited by 93 · see citing works
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 · see citing works
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 · see citing works
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 88 · see citing works
Hector, R. E., Dien, B. S., Cotta, M. A., & Qureshi, N. (2010) · Journal of Industrial Microbiology & Biotechnology · doi:10.1007/s10295-010-0896-1 · Cited by 86 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 82 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 79 · see citing works
Directed Enzyme Evolution: Advances and Applications
Alcalde, M. (2017) · Springer eBooks · doi:10.1007/978-3-319-50413-1 · Cited by 80 · see citing works
Yeast systems biotechnology for the production of heterologous proteins
Graf, A. B., Dragosits, M., Gasser, B., & Mattanovich, D. (2009) · FEMS Yeast Research · doi:10.1111/j.1567-1364.2009.00507.x · Cited by 77 · see citing works
Latimer, L. N., Lee, M. E., Medina-Cleghorn, D. A., Kohnz, R. A., Nomura, D. K., & Dueber, J. E. (2014) · Metabolic Engineering · doi:10.1016/j.ymben.2014.06.002 · Cited by 76 · see citing works
Yamamoto, H., Yamaji, H., Abe, Y., Harada, K., Waluyo, D., Fukusaki, E., Kondo, A., Ohno, H., & Fukuda, H. (2009) · Chemometrics and Intelligent Laboratory Systems · doi:10.1016/j.chemolab.2009.05.006 · Cited by 75 · see citing works
Smith, J., van Rensburg, E., & Görgens, J. F. (2014) · BMC Biotechnology · doi:10.1186/1472-6750-14-41 · 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
Grotkjær, T., Christakopoulos, P., Nielsen, J., & Lisbeth Olsson, A. (2005) · Metabolic Engineering · doi:10.1016/j.ymben.2005.07.003 · Cited by 72 · see citing works
Pitkänen, J., Rintala, E., Aristidou, A. A., Ruohonen, L., & Penttilä, M. E. (2005) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-004-1798-9 · Cited by 71 · see citing works
Construction of a synthetic YdbK-dependent pyruvate:H2 pathway in Escherichia coli BL21(DE3)
Akhtar, M. K., & Jones, P. R. (2009) · Metabolic Engineering · doi:10.1016/j.ymben.2009.01.002 · Cited by 68 · see citing works
Topaloğlu, A., Esen, Ö., Turanlı-Yıldız, B., Arslan, M., & Çakar, Z. P. (2023) · Journal of Fungi · doi:10.3390/jof9100984 · Cited by 67 · see citing works
- 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