Xylose isomerase overexpression along with engineering of the pentose phosphate pathway and evolutionary engineering enable rapid xylose utilization and ethanol production by Saccharomyces cerevisiae
Abstract
Xylose is the main pentose and second most abundant sugar in lignocellulosic feedstocks. To improve xylose utilization, necessary for the cost-effective bioconversion of lignocellulose, several metabolic engineering approaches have been employed in the yeast Saccharomyces cerevisiae. In this study, we describe the rational metabolic engineering of a S. cerevisiae strain, including overexpression of the Piromyces xylose isomerase gene (XYLA), Pichia stipitis xylulose kinase (XYL3) and genes of the non-oxidative pentose phosphate pathway (PPP). This engineered strain (H131-A3) was used to initialize a three-stage process of evolutionary engineering, through first aerobic and anaerobic sequential batch cultivation followed by growth in a xylose-limited chemostat. The evolved strain H131-A3-AL(CS) displayed significantly increased anaerobic growth rate (0.203±0.006 h⁻¹) and xylose consumption rate (1.866 g g⁻¹ h⁻¹) along with high ethanol conversion yield (0.41 g/g). These figures exceed by a significant margin any other performance metrics on xylose utilization and ethanol production by S. cerevisiae reported to-date. Further inverse metabolic engineering based on functional complementation suggested that efficient xylose assimilation is attributed, in part, to the elevated expression level of xylose isomerase, which was accomplished through the multiple-copy integration of XYLA in the chromosome of the evolved strain.
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A S. cerevisiae strain with deficient pyruvate decarboxylase activity was evolved for high-glucose tolerance.
“In another study, van Maris and co-workers evolved a S. cerevisiae strain with deficient pyruvate decarboxylase activity for high-glucose tolerance [97].”
From Adaptive laboratory evolution—Principles and applications for biotechnology (2013) · cites this paper as [97]
Cites
Sikorski, R. S., & Hieter, P. (1989) · Genetics · doi:10.1093/genetics/122.1.19 · Cited by 8,685 · see citing works
Mumberg, D., Müller, R., & Funk, M. (1995) · Gene · doi:10.1016/0378-1119(95)00037-7 · Cited by 1,972 · see citing works
An electrophoretic karyotype for yeast.
Carle, G. F., & Olson, M. V. (1985) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.82.11.3756 · Cited by 787 · 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
Andreasen, A. A., & Stier, T. J. B. (1953) · Journal of Cellular and Comparative Physiology · doi:10.1002/jcp.1030410103 · Cited by 555 · 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
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
Double-strand breaks at an initiation site for meiotic gene conversion
Sun, H., Treco, D. A., Schultes, N. P., & Szostak, J. W. (1989) · Nature · doi:10.1038/338087a0 · Cited by 524 · see citing works
Kuyper, M., HARTOG, M., Toirkens, M. J., Almering, M. J. H., Winkler, A. A., VANDIJKEN, J., & Pronk, J. T. (2004) · FEMS Yeast Research · doi:10.1016/j.femsyr.2004.09.010 · Cited by 404 · see citing works
Andreasen, A. A., & Stier, T. J. B. (1954) · Journal of Cellular and Comparative Physiology · doi:10.1002/jcp.1030430303 · Cited by 392 · see citing works
Kuyper, M., Harhangi, H. R., STAVE, A., Winkler, A. A., Jetten, M. S. M., DELAAT, W., DENRIDDER, J., den Camp, H. J. M. O., VANDIJKEN, J., & Pronk, J. T. (2003) · FEMS Yeast Research · doi:10.1016/s1567-1356(03)00141-7 · Cited by 366 · 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
Auxotrophic Yeast Strains in Fundamental and Applied Research
Pronk, J. T. (2002) · Applied and Environmental Microbiology · doi:10.1128/aem.68.5.2095-2100.2002 · Cited by 317 · 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
Utilization of xylose by bacteria, yeasts, and fungi
Jeffries, T. W. (2005) · Springer eBooks · doi:10.1007/bfb0009101 · Cited by 291 · 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
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
The role of redox balances in the anaerobic fermentation of xylose by yeasts
Bruinenberg, P. M., de Bot, P. H. M., van Dijken, J. P., & Scheffers, W. A. (1983) · Applied Microbiology and Biotechnology · doi:10.1007/bf00500493 · Cited by 264 · see citing works
A Modified Saccharomyces cerevisiae Strain That Consumes l -Arabinose and Produces Ethanol
Becker, J., & Boles, E. (2003) · Applied and Environmental Microbiology · doi:10.1128/aem.69.7.4144-4150.2003 · Cited by 253 · 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
Evolutionary Engineering of <i>Saccharomyces cerevisiae</i> for Anaerobic Growth on Xylose
Sonderegger, M., & Sauer, U. (2003) · Applied and Environmental Microbiology · doi:10.1128/aem.69.4.1990-1998.2003 · Cited by 251 · 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
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
Yeast metabolic engineering for hemicellulosic ethanol production
Van Vleet, J., & Jeffries, T. (2009) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2009.06.001 · Cited by 241 · see citing works
Karhumaa, K., Hahn‐Hägerdal, B., & Gorwa‐Grauslund, M. F. (2005) · Yeast · doi:10.1002/yea.1216 · Cited by 214 · see citing works
Expander: from expression microarrays to networks and functions
Ulitsky, I., Maron‐Katz, A., Shavit, S., Sagir, D., Linhart, C., Elkon, R., Tanay, A., Sharan, R., Shiloh, Y., & Ron Shamir, A. (2010) · Nature Protocols · doi:10.1038/nprot.2009.230 · Cited by 194 · see citing works
Jin, Y., Ni, H., Laplaza, J. M., & Jeffries, T. W. (2003) · Applied and Environmental Microbiology · doi:10.1128/aem.69.1.495-503.2003 · Cited by 181 · see citing works
Madhavan, A., Tamalampudi, S., Ushida, K., Kanai, D., Katahira, S., Srivastava, A., Fukuda, H., Bisaria, V. S., & Kondo, A. (2008) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-008-1794-6 · Cited by 180 · see citing works
Saccharomyces 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
Expression of the Escherichia coli xylose isomerase gene in Saccharomyces cerevisiae
Sarthy, A. V., McConaughy, B. L., Lobo, Z., Sundstrom, J. A., Furlong, C. E., & Hall, B. D. (1987) · Applied and Environmental Microbiology · doi:10.1128/aem.53.9.1996-2000.1987 · Cited by 160 · see citing works
Hauf, J., Zimmermann, F. K., & Müller, S. (2000) · Enzyme and Microbial Technology · doi:10.1016/s0141-0229(00)00160-5 · Cited by 151 · 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
Karhumaa, K., Wiedemann, B., Hahn‐Hägerdal, B., Boles, E., & Gorwa‐Grauslund, M. F. (2006) · Microbial Cell Factories · doi:10.1186/1475-2859-5-18 · Cited by 149 · see citing works
Jin, Y., Alper, H. S., Yang, Y.-T., & Stephanopoulos, G. N. (2005) · Applied and Environmental Microbiology · doi:10.1128/aem.71.12.8249-8256.2005 · Cited by 148 · see citing works
Self-citationJohansson, B., Christensson, C., Hobley, T. J., & Hahn‐Hägerdal, B. (2001) · Applied and Environmental Microbiology · doi:10.1128/aem.67.9.4249-4255.2001 · Cited by 137 · see citing works
Uptake and catabolism of D-xylose in Salmonella typhimurium LT2
Shamanna, D. K., & Sanderson, K. E. (1979) · Journal of Bacteriology · doi:10.1128/jb.139.1.64-70.1979 · Cited by 131 · see citing works
Amore, R., Wilhelm, M., & Hollenberg, C. P. (1989) · Applied Microbiology and Biotechnology · doi:10.1007/bf00296623 · Cited by 122 · see citing works
Wahlbom, C. F., Otero, R. R. C., van Zyl, W. H., Hahn‐Hägerdal, B., & Jönsson, L. J. (2003) · Applied and Environmental Microbiology · doi:10.1128/aem.69.2.740-746.2003 · Cited by 120 · see citing works
Wiedemann, B., & Boles, E. (2008) · Applied and Environmental Microbiology · doi:10.1128/aem.02395-07 · Cited by 113 · see citing works
Johansson, B., & Hähn‐Hägerdal, B. (2002) · FEMS Yeast Research · doi:10.1111/j.1567-1364.2002.tb00095.x · Cited by 105 · see citing works
Marteinsson, V., Kristjánsson, J. K., Kristmannsdóttir, H., Dahlkvist, M., Sæmundsson, K., Hannington, M. D., Pétursdóttir, S. K., Geptner, A. R., & Stoffers, P. (2001) · Applied and Environmental Microbiology · doi:10.1128/aem.67.2.827-833.2001 · Cited by 103 · see citing works
Utilization of Xylose by Bacteria, Yeasts, and Fungi
Jeffries, T. W. (1983) · De Gruyter eBooks · doi:10.1515/9783112620809-002 · Cited by 101 · see citing works
Moes, C. J., Pretorius, I. S., & van Zyl, W. H. (1996) · Biotechnology Letters · doi:10.1007/bf00142943 · Cited by 92 · see citing works
Madhavan, A., Tamalampudi, S., Srivastava, A., Fukuda, H., Bisaria, V. S., & Kondo, A. (2009) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-008-1818-2 · Cited by 87 · see citing works
Transposon Mutagenesis To Improve the Growth of Recombinant Saccharomyces cerevisiae on d -Xylose
Ni, H., Laplaza, J. M., & Jeffries, T. W. (2007) · Applied and Environmental Microbiology · doi:10.1128/aem.02564-06 · Cited by 84 · see citing works
Gárdonyi, M., & Hahn‐Hägerdal, B. (2002) · Enzyme and Microbial Technology · doi:10.1016/s0141-0229(02)00285-5 · 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
Akinterinwa, O., & Cirino, P. C. (2008) · Metabolic Engineering · doi:10.1016/j.ymben.2008.07.006 · Cited by 62 · see citing works
Ohta, K., & Hayashida, S. (1983) · Applied and Environmental Microbiology · doi:10.1128/aem.46.4.821-825.1983 · Cited by 60 · see citing works
Kinetic characterization of d-xylose isomerases by enzymatic assays using d-sorbitol dehydrogenase
Kersters-Hilderson, H., Callens, M. C., Opstal, O. V., Vangrysperre, W., & Bruyne, C. K. D. (1987) · Enzyme and Microbial Technology · doi:10.1016/0141-0229(87)90067-6 · Cited by 34 · see citing works
Baerends, R. J. S., Qiu, J., Rasmussen, S., Nielsen, H. B., & Brandt, A. (2009) · Applied and Environmental Microbiology · doi:10.1128/aem.00989-09 · Cited by 21 · see citing works
Mutations of the human MUT S homologue 6 gene in ampullary carcinoma and gastric cancer
Imai, Y., Inoue, T., & Ishikawa, T. (1998) · International Journal of Cancer · doi:10.1002/(sici)1097-0215(19981123)78:5 · Cited by 7 · see citing works
Wang, B. L. (2009) · DSpace@MIT (Massachusetts Institute of Technology) · Cited by 3 · see citing works
Self-citation
Flagged first, then by citations
1 of the 54 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
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
Review of Second-Generation Bioethanol Production from Residual Biomass
Robak, K., & Balcerek, M. (2018) · Food Technology and Biotechnology · doi:10.17113/ftb.56.02.18.5428 · Cited by 661 · 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
Davis, R., Office of Renewable Energy Office of Energy Efficiency and Renewable Energy (EERE), Tan, E. C. D., Tan, E., Biddy, M., Beckham, G. T., Scarlata, C., Jacobson, J., Cafferty, K., Ross, J., et al. (2013) · doi:10.2172/1107470 · Cited by 439 · see citing works
Selection of chromosomal DNA libraries using a multiplex CRISPR system
Ryan, O. W., Skerker, J. M., Maurer, M. J., Li, X., Tsai, J. C., Poddar, S., Lee, M. E., DeLoache, W., Dueber, J. E., Arkin, A. P., et al. (2014) · eLife · doi:10.7554/elife.03703 · Cited by 367 · 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
Wang, B. L., Ghaderi, A., Zhou, H., Agresti, J. J., Weitz, D. A., Fink, G. R., & Stephanopoulos, G. N. (2014) · Nature Biotechnology · doi:10.1038/nbt.2857 · Cited by 330 · see citing works
Self-citationXylose 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
Metabolic engineering of yeast for production of fuels and chemicals
Nielsen, J., Larsson, C., van Maris, A. J. A., & Pronk, J. T. (2013) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2013.03.023 · Cited by 318 · see citing works
Kwak, S., & Jin, Y. (2017) · Microbial Cell Factories · doi:10.1186/s12934-017-0694-9 · Cited by 272 · 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
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
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
Salehi Jouzani, G., & Taherzadeh, M. J. (2015) · Biofuel Research Journal · doi:10.18331/brj2015.2.1.4 · Cited by 224 · see citing works
Kim, S. R., Skerker, J. M., Kang, W., Lesmana, A., Wei, N., Arkin, A. P., & Jin, Y. (2013) · PLoS ONE · doi:10.1371/journal.pone.0057048 · Cited by 219 · 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
Biochemical routes for uptake and conversion of xylose by microorganisms
Zhe, Z., Xian, M., Liu, M., & Zhao, G. (2020) · Biotechnology for Biofuels · doi:10.1186/s13068-020-1662-x · Cited by 216 · see citing works
Engineering alcohol tolerance in yeast
Lam, F. H., Ghaderi, A., Fink, G. R., & Stephanopoulos, G. N. (2014) · Science · doi:10.1126/science.1257859 · Cited by 213 · see citing works
Self-citationCunha, J. T., Soares, P. O., Romaní, A., Thevelein, J. M., & Domingues, L. (2019) · Biotechnology for Biofuels · doi:10.1186/s13068-019-1360-8 · Cited by 194 · see citing works
Mans, R., Daran, J.-M. G., & Pronk, J. T. (2017) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2017.10.011 · Cited by 167 · see citing works
Microbial Experimental Evolution – a proving ground for evolutionary theory and a tool for discovery
McDonald, M. J. (2019) · EMBO Reports · doi:10.15252/embr.201846992 · Cited by 165 · see citing works
Yeast's balancing act between ethanol and glycerol production in low‐alcohol wines
Goold, H. D., Kroukamp, H., Williams, T. C., Paulsen, I. T., Varela, C., & Pretorius, I. S. (2017) · Microbial Biotechnology · doi:10.1111/1751-7915.12488 · Cited by 165 · see citing works
Apel, A. R., Ouellet, M., Szmidt, H. L., Keasling, J. D., & Mukhopadhyay, A. (2016) · Scientific Reports · doi:10.1038/srep19512 · Cited by 159 · see citing works
The Pentose Phosphate Pathway in Yeasts–More Than a Poor Cousin of Glycolysis
Bertels, L.-K., Murillo, L. F., & Heinisch, J. J. (2021) · Biomolecules · doi:10.3390/biom11050725 · Cited by 127 · see citing works
Chen, Y., & Nielsen, J. (2013) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2013.03.008 · Cited by 125 · 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
Kang, Y., Xu, L., Wang, F., & Wei, D. (2014) · Metabolic Engineering · doi:10.1016/j.ymben.2014.05.005 · Cited by 118 · see citing works
Systematic and evolutionary engineering of a xylose isomerase-based pathway in
Lee, S., Jellison, T., & Alper, H. S. (2014) · Biotechnology for Biofuels · doi:10.1186/s13068-014-0122-x · Cited by 118 · 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
Engineering co-utilization of glucose and xylose for chemical overproduction from lignocellulose
Gao, J., Yu, W., Li, Y., Jin, M., Yao, L., & Zhou, Y. J. (2023) · Nature Chemical Biology · doi:10.1038/s41589-023-01402-6 · Cited by 115 · see citing works
Simultaneous utilization of glucose and xylose via novel mechanisms in engineered Escherichia coli
Kim, S. M., Choi, B. Y., Ryu, Y. S., Jung, S. H., Park, J. M., Kim, G.-H., & Lee, S. K. (2015) · Metabolic Engineering · doi:10.1016/j.ymben.2015.05.002 · Cited by 114 · see citing works
Genome-scale modeling for metabolic engineering
Simeonidis, E., & Price, N. D. (2015) · Journal of Industrial Microbiology & Biotechnology · doi:10.1007/s10295-014-1576-3 · 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
Qin, L., Dong, S., Yu, J., Ning, X., Xu, K., Zhang, S.-J., Xu, L., Li, B., Li, J., Yuan, Y., et al. (2020) · Metabolic Engineering · doi:10.1016/j.ymben.2020.06.003 · Cited by 107 · see citing works
Application of synthetic biology for production of chemicals in yeastSaccharomyces cerevisiae
Li, M., & Borodina, I. (2014) · FEMS Yeast Research · doi:10.1111/1567-1364.12213 · Cited by 105 · see citing works
Tran, P. H. N., Ko, J. K., Gong, G., Um, Y., & Lee, S. (2020) · Biotechnology for Biofuels · doi:10.1186/s13068-019-1641-2 · Cited by 101 · see citing works
Combining C6 and C5 sugar metabolism for enhancing microbial bioconversion
Zhang, G.-C., Liu, J., Kong, I. I., Kwak, S., & Jin, Y. (2015) · Current Opinion in Chemical Biology · doi:10.1016/j.cbpa.2015.09.008 · Cited by 99 · 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
Pigments and Colorants from Filamentous Fungi
Caro, Y., Venkatachalam, M., Lebeau, J., Fouillaud, M., & Dufossé, L. (2015) · Springer eBooks · doi:10.1007/978-3-319-19456-1_26-1 · Cited by 92 · see citing works
Experimental Evolution Reveals Favored Adaptive Routes to Cell Aggregation in Yeast
Hope, E. A., Amorosi, C. J., Miller, A. W., Dang, K., Heil, C. S., & Dunham, M. J. (2017) · Genetics · doi:10.1534/genetics.116.198895 · Cited by 89 · see citing works
Engineering Shewanella oneidensis enables xylose-fed microbial fuel cell
Li, F., Li, Y., Sun, L., Li, X., Yin, C., An, X., Chen, X., Tian, Y., & Song, H. (2017) · Biotechnology for Biofuels · doi:10.1186/s13068-017-0881-2 · Cited by 91 · 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
Engineering of Pentose Transport in Saccharomyces cerevisiae for Biotechnological Applications
Nijland, J. G., & Driessen, A. J. M. (2020) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2019.00464 · Cited by 90 · see citing works
Claes, A., Deparis, Q., Foulquié-Moreno, M. R., & Thevelein, J. M. (2020) · Metabolic Engineering · doi:10.1016/j.ymben.2020.02.004 · Cited by 87 · see citing works
Wei, N., Oh, E. J., Million, G., Cate, J. H. D., & Jin, Y. (2015) · ACS Synthetic Biology · doi:10.1021/sb500364q · Cited by 86 · see citing works
Matsushika, A., Goshima, T., & Hoshino, T. (2014) · Microbial Cell Factories · doi:10.1186/1475-2859-13-16 · Cited by 84 · 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
Li, H., Shen, Y., Wu, M., Hou, J., Jiao, C., Li, Z., Liu, X., & Bao, X. (2016) · Bioresources and Bioprocessing · doi:10.1186/s40643-016-0126-4 · Cited by 84 · see citing works
Kim, B., Du, J., Eriksen, D. T., & Zhao, H. (2012) · Applied and Environmental Microbiology · doi:10.1128/aem.02736-12 · Cited by 82 · see citing works
Diao, L., Liu, Y., Qian, F., Yang, J., Jiang, Y., & Yang, S. (2013) · BMC Biotechnology · doi:10.1186/1472-6750-13-110 · Cited by 82 · see citing works
Wasylenko, T. M., & Stephanopoulos, G. N. (2014) · Biotechnology and Bioengineering · doi:10.1002/bit.25447 · Cited by 82 · see citing works
Self-citationRecycling Carbon Dioxide during Xylose Fermentation by Engineered Saccharomyces cerevisiae
Xia, P., Zhang, G.-C., Walker, B. J., Seo, S.-O., Kwak, S., Liu, J., Kim, H., Ort, D. R., Wang, S.-G., & Jin, Y. (2016) · ACS Synthetic Biology · doi:10.1021/acssynbio.6b00167 · Cited by 81 · see citing works
Lugani, Y., Rai, R., Prabhu, A. A., Maan, P., Hans, M., Kumar, V., Kumar, S., Chandel, A. K., & Sengar, R. S. (2020) · Biofuel Research Journal · doi:10.18331/brj2020.7.4.5 · Cited by 80 · see citing works
Chen, S., Xu, Z., Ding, B., Zhang, Y., Liu, S., Cai, C., Li, M., Dale, B. E., & Jin, M. (2023) · Science Advances · doi:10.1126/sciadv.add8835 · Cited by 80 · 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
Mao, Y., Li, G., Chang, Z., Tao, R. N., Cui, Z., Wang, Z., Ya-jie Tang, A., Chen, T., & Zhao, X. (2018) · Biotechnology for Biofuels · doi:10.1186/s13068-018-1094-z · Cited by 78 · see citing works
Metabolic engineering for sustainability and health
Kim, G. B., Choi, S. Y., Cho, I., Ahn, D., & Lee, S. Y. (2023) · Trends in biotechnology · doi:10.1016/j.tibtech.2022.12.014 · Cited by 75 · 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
Smith, J., van Rensburg, E., & Görgens, J. F. (2014) · BMC Biotechnology · doi:10.1186/1472-6750-14-41 · Cited by 75 · see citing works
Kourist, R., Bracharz, F., Lorenzen, J., Kracht, O. N., Chovatia, M., Daum, C. G., Deshpande, S., Lipzen, A., Nolan, M., Ohm, R. A., et al. (2015) · mBio · doi:10.1128/mbio.00918-15 · Cited by 74 · see citing works
Enhancing the Co-utilization of Biomass-Derived Mixed Sugars by Yeasts
Gao, M., Ploessl, D. S., & Shao, Z. (2019) · Frontiers in Microbiology · doi:10.3389/fmicb.2018.03264 · Cited by 76 · see citing works
Enhanced xylose fermentation and ethanol production by engineered Saccharomyces cerevisiae strain
Vilela, L. D. F., de Araujo, V. P. G., Paredes, R. D. S., Bon, E. P. S., Torres, F. A. G., Neves, B. C., & Eleuthério, E. C. A. (2015) · AMB Express · doi:10.1186/s13568-015-0102-y · Cited by 73 · see citing works
Verhoeven, M. D., Lee, M., Kamoen, L., van den Broek, M. A., Janssen, D. B., Daran, J.-M. G., van Maris, A. J. A., & Pronk, J. T. (2017) · Scientific Reports · doi:10.1038/srep46155 · Cited by 73 · see citing works
Peng, B., Huang, S., Liu, T., & Geng, A. (2015) · Microbial Cell Factories · doi:10.1186/s12934-015-0253-1 · Cited by 70 · see citing works
Demeke, M. M., Foulquié-Moreno, M. R., Dumortier, F. M., & Thevelein, J. M. (2015) · PLoS Genetics · doi:10.1371/journal.pgen.1005010 · Cited by 67 · see citing works
Evolutionary engineering of industrial microorganisms-strategies and applications
Zhu, Z., Zhang, J., Ji, X., Fang, Z., Wu, Z., Chen, J., & Du, G. (2018) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-018-8937-1 · Cited by 67 · see citing works
Zha, J., Shen, M.-H., Hu, M., Song, H., & Yuan, Y. (2013) · Journal of Industrial Microbiology & Biotechnology · doi:10.1007/s10295-013-1350-y · Cited by 66 · see citing works
Physical methods for genetic transformation of fungi and yeast
Rivera, A. L., Magaña-Ortíz, D., Gómez-Lim, M. Á., Fernández, F., & Loske, A. M. (2014) · Physics of Life Reviews · doi:10.1016/j.plrev.2014.01.007 · Cited by 64 · see citing works
Pentose metabolism and conversion to biofuels and high-value chemicals in yeasts
Ruchała, J., & Sibirny, A. А. (2020) · FEMS Microbiology Reviews · doi:10.1093/femsre/fuaa069 · Cited by 64 · see citing works
OptRAM: In-silico strain design via integrative regulatory-metabolic network modeling
Shen, F., Sun, R., Yao, J., Li, J., Liu, Q., Price, N. D., Liu, C., & Wang, Z. (2019) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1006835 · Cited by 63 · see citing works
Metabolic engineering of Saccharomyces cerevisiae to produce 1-hexadecanol from xylose
Guo, W., Sheng, J., Zhao, H., & Feng, X. (2016) · Microbial Cell Factories · doi:10.1186/s12934-016-0423-9 · Cited by 63 · see citing works
Adaptive laboratory evolution of microbial co‐cultures for improved metabolite secretion
Konstantinidis, D., Pereira, F. M., Geissen, E., Grkovska, K., Kafkia, E., Jouhten, P., Kim, Y., Devendran, S., Zimmermann, M., & Patil, K. R. (2021) · Molecular Systems Biology · doi:10.15252/msb.202010189 · Cited by 60 · see citing works
Papapetridis, I., Verhoeven, M. D., Wiersma, S. J., Goudriaan, M., van Maris, A. J. A., & Pronk, J. T. (2018) · FEMS Yeast Research · doi:10.1093/femsyr/foy056 · Cited by 59 · see citing works
Zhang, Y., Lane, S., Chen, J., Hammer, S. K., Luttinger, J., Yang, L., Jin, Y., & Avalos, J. L. (2019) · Biotechnology for Biofuels · doi:10.1186/s13068-019-1560-2 · Cited by 60 · see citing works
Feng, X., & Zhao, H. (2013) · Microbial Cell Factories · doi:10.1186/1475-2859-12-114 · Cited by 58 · see citing works
Optimization of an acetate reduction pathway for producing cellulosic ethanol by engineered yeast
Zhang, G., Kong, I. I., Wei, N., Peng, D., Turner, T. L., Sung, B. H., Sohn, J., & Jin, Y. (2016) · Biotechnology and Bioengineering · doi:10.1002/bit.26021 · Cited by 59 · see citing works
Metabolic engineering of yeast for lignocellulosic biofuel production
Jin, Y., & Cate, J. H. D. (2017) · Current Opinion in Chemical Biology · doi:10.1016/j.cbpa.2017.10.025 · Cited by 59 · see citing works
Value-added biotransformation of cellulosic sugars by engineered Saccharomyces cerevisiae
Lane, S., Jia, D., & Jin, Y. (2018) · Bioresource Technology · doi:10.1016/j.biortech.2018.04.013 · Cited by 59 · see citing works
Zhang, J., Zhang, B., Wang, D., Gao, X., Sun, L., & Hong, J. (2015) · Metabolic Engineering · doi:10.1016/j.ymben.2015.07.008 · Cited by 57 · see citing works
Engineering Saccharomyces cerevisiae for next generation ethanol production
den Haan, R., Kroukamp, H., Mert, M. J., Viljoen‐Bloom, M., Görgens, J. F., & van Zyl, W. H. (2013) · Journal of Chemical Technology & Biotechnology · doi:10.1002/jctb.4068 · Cited by 57 · see citing works
Seppälä, S., Wilken, S. E., Knop, D., Solomon, K., & O'Malley, M. A. (2017) · Metabolic Engineering · doi:10.1016/j.ymben.2017.09.008 · Cited by 57 · see citing works
Verhoeven, M. D., de Valk, S. C., Daran, J.-M. G., van Maris, A. J. A., & Pronk, J. T. (2018) · FEMS Yeast Research · doi:10.1093/femsyr/foy075 · Cited by 56 · see citing works
Li, H., Wu, M., Xu, L., Hou, J., Guo, T., Bao, X., & Shen, Y. (2015) · Microbial Biotechnology · doi:10.1111/1751-7915.12245 · Cited by 56 · see citing works
Sun, L., & Jin, Y. (2020) · Biotechnology Journal · doi:10.1002/biot.202000142 · Cited by 54 · see citing works
Qiu, Y., Wu, M., Bao, H., Liu, W., & Shen, Y. (2023) · Engineering Microbiology · doi:10.1016/j.engmic.2023.100084 · Cited by 57 · see citing works
Osiro, K. O., Borgström, C., Brink, D. P., Fjölnisdóttir, B. L., & Gorwa‐Grauslund, M. F. (2019) · Microbial Cell Factories · doi:10.1186/s12934-019-1141-x · Cited by 55 · see citing works
Engineering a xylose fermenting yeast for lignocellulosic ethanol production
Zhang, Y., Yang, J., Qian, F., Sutton, K. B., Hjort, C., Wu, W., Jiang, Y., & Yang, S. (2024) · Nature Chemical Biology · doi:10.1038/s41589-024-01771-6 · Cited by 53 · see citing works
Bioconversion of lignocellulosic biomass into bacterial nanocellulose: challenges and perspectives
Li, W., Shen, Y., Liu, H., Huang, X., Xu, B., Zhong, C., & Jia, S. (2022) · Green Chemical Engineering · doi:10.1016/j.gce.2022.04.007 · Cited by 52 · see citing works
Carlsen, S., Ajikumar, P. K., Formenti, L. R., Zhou, K., Too, H., Nielsen, M. L., Lantz, A. E., Kielland‐Brandt, M. C., & Stephanopoulos, G. N. (2013) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-013-4877-y · Cited by 51 · see citing works
Self-citationConstruction of efficient xylose utilizing Pichia pastoris for industrial enzyme production
Li, P., Sun, H., Chen, Z., Li, Y., & Zhu, T. (2015) · Microbial Cell Factories · doi:10.1186/s12934-015-0206-8 · Cited by 51 · see citing works
Hoang, P. T. N., Ko, J. K., Gong, G., Um, Y., & Lee, S. (2018) · Biotechnology for Biofuels · doi:10.1186/s13068-018-1269-7 · Cited by 50 · see citing works
Cao, L., Tang, X., Zhang, X., Zhang, J., Tian, X.-L., Wang, J., Xiong, M., & Xiao, W. (2014) · Metabolic Engineering · doi:10.1016/j.ymben.2014.05.001 · Cited by 50 · see citing works
An in vivo gene amplification system for high level expression in Saccharomyces cerevisiae
Peng, B., Esquirol, L., Lu, Z. M., Shen, Q., Cheah, L. C., Howard, C. B., Scott, C. S., Trau, M., Dumsday, G. J., & Vickers, C. E. (2022) · Nature Communications · doi:10.1038/s41467-022-30529-8 · Cited by 49 · see citing works
Henningsen, B. M., Hon, S., Covalla, S. F., Sonu, C., Argyros, D. A., Barrett, T. F., Wiswall, E., Froehlich, A. C., & Zelle, R. M. (2015) · Applied and Environmental Microbiology · doi:10.1128/aem.01689-15 · Cited by 49 · see citing works
Cheng, C., Tang, R.-Q., Xiong, L., Hector, R. E., Bai, F., & Zhao, X. (2018) · Biotechnology for Biofuels · doi:10.1186/s13068-018-1018-y · Cited by 48 · see citing works
Xylose Metabolism in Bioethanol Production: Saccharomyces cerevisiae vs Non-Saccharomyces Yeasts
Ochoa-Chacón, A., Martı́nez, A., Poggi-Varaldo, H. M., Villa‐Tanaca, L., Ramos-Valdivia, A. C., & Ponce‐Noyola, T. (2021) · BioEnergy Research · doi:10.1007/s12155-021-10340-x · Cited by 49 · see citing works
Agro-residues as Alternative for Xylanase Production by Filamentous Fungi
Knob, A., Fortkamp, D., Prolo, T., Izidoro, S. C., & de Almeida, J. M. (2014) · DOAJ (DOAJ: Directory of Open Access Journals) · doi:10.15376/biores.9.3.5738-5773 · Cited by 48 · see citing works
Sharma, N. K., Behera, S., Arora, R., & Kumar, S. (2016) · Bioprocess and Biosystems Engineering · doi:10.1007/s00449-016-1563-3 · Cited by 48 · see citing works
Zhang, B., Zhu, Y., Zhang, J., Wang, D., Sun, L., & Hong, J. (2016) · Bioresource Technology · doi:10.1016/j.biortech.2016.11.110 · Cited by 47 · see citing works
Engineered yeast tolerance enables efficient production from toxified lignocellulosic feedstocks
Lam, F. H., Turanlı-Yıldız, B., Liu, D., Resch, M. G., Fink, G. R., & Stephanopoulos, G. N. (2021) · Science Advances · doi:10.1126/sciadv.abf7613 · Cited by 47 · see citing works
Self-citation
- Authors
- Zhou, H., Cheng, J.-S., Wang, B. L., Fink, G. R., & Stephanopoulos, G.
- Affiliations
- Massachusetts Institute of Technology (US)
- Whitehead Institute for Biomedical Research (US)
- Corresponding author
- Stephanopoulos, Gregory
- Venue
- Metabolic Engineering
- Publisher
- Elsevier BV
- Published
- 2012-11
- Volume
- 14
- Issue
- 6
- Pages
- 611-622
- ISSN
- 1096-7176 (ISSN-L)
- OpenAlex
- W2060718895
- Cited by
- 287
- References
- 54
- Citations by year
- 2026: 9 · 2025: 5 · 2024: 12 · 2023: 10 · 2022: 21 · 2021: 14 · 2020: 19 · 2019: 24 · 2018: 28 · 2017: 31 · 2016: 24 · 2015: 29 · 2014: 29 · 2013: 28 · 2012: 4
- FWCI
- 11.58
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Metabolic Engineering (publishedVersion)
- PubMed (publishedVersion)
- 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
- xylose isomerase, Saccharomyces cerevisiae, xylose utilization, ethanol production, pentose phosphate pathway, xylulose kinase, Pichia stipitis, evolutionary engineering, lignocellulosic biomass, xylose uptake, inverse metabolic engineering, functional complementation
- MeSH terms
- Ethanol, Pentose Phosphate Pathway, Pichia, Saccharomyces cerevisiae, Xylose, Protein Engineering, Up-Regulation, Phosphotransferases (Alcohol Group Acceptor), Directed Molecular Evolution, Aldose-Ketose Isomerases, Piromyces, Genetic Enhancement
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