Engineering of yeast hexose transporters to transport d -xylose without inhibition by d -glucose
Open accessAbstract
All known D-xylose transporters are competitively inhibited by D-glucose, which is one of the major reasons hampering simultaneous fermentation of D-glucose and D-xylose, two primary sugars present in lignocellulosic biomass. We have set up a yeast growth-based screening system for mutant D-xylose transporters that are insensitive to the presence of D-glucose. All of the identified variants had a mutation at either a conserved asparagine residue in transmembrane helix 8 or a threonine residue in transmembrane helix 5. According to a homology model of the yeast hexose transporter Gal2 deduced from the crystal structure of the D-xylose transporter XylE from Escherichia coli, both residues are found in the same region of the protein and are positioned slightly to the extracellular side of the central sugar-binding pocket. Therefore, it is likely that alterations sterically prevent D-glucose but not D-xylose from entering the pocket. In contrast, changing amino acids that are supposed to directly interact with the C6 hydroxymethyl group of D-glucose negatively affected transport of both D-glucose and D-xylose. Determination of kinetic properties of the mutant transporters revealed that Gal2-N376F had the highest affinity for D-xylose, along with a moderate transport velocity, and had completely lost the ability to transport hexoses. These transporter versions should prove valuable for glucose-xylose cofermentation in lignocellulosic hydrolysates by Saccharomyces cerevisiae and other biotechnologically relevant organisms. Moreover, our data contribute to the mechanistic understanding of sugar transport because the decisive role of the conserved asparagine residue for determining sugar specificity has not been recognized before.
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Adaptive evolutionary engineering based on metabolic engineering can allow microorganisms to quickly obtain excellent phenotypes, but there are problems such as unclear gene targets and negative mutation interference.
“Adaptive evolutionary engineering based on metabolic engineering can allow microorganisms to quickly obtain excellent phenotypes, but there are problems such as unclear gene targets and negative mutation interference [90,91].”
From Recent Developments in Lignocellulosic Biofuels, a Renewable Source of Bioenergy (2022) · cites this paper as [91]
Cites
The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling
Arnold, K., Bordoli, L., Kopp, J., & Schwede, T. F. (2005) · Bioinformatics · doi:10.1093/bioinformatics/bti770 · Cited by 6,951 · see citing works
Boeke, J. D., Lacroute, F., & Fink, G. R. (1984) · Molecular and General Genetics MGG · doi:10.1007/bf00330984 · Cited by 2,354 · see citing works
A new efficient gene disruption cassette for repeated use in budding yeast
Güldener, U. (1996) · Nucleic Acids Research · doi:10.1093/nar/24.13.2519 · Cited by 1,657 · 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
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
Crystal structure of a bacterial homologue of glucose transporters GLUT1–4
Sun, L., Zeng, X. W., Yan, C., Sun, X., Gong, X., Rao, Y., & Yan, N. (2012) · Nature · doi:10.1038/nature11524 · Cited by 472 · see citing works
Engineered Saccharomyces cerevisiae capable of simultaneous cellobiose and xylose fermentation
Ha, S.-J., Galazka, J. M., Kim, S. R., Choi, J.-H., Yang, X., Seo, J., Glass, N. L., Cate, J. H. D., & Jin, Y. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1010456108 · Cited by 468 · see citing works
Hong, K.-K., & Nielsen, J. (2012) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-012-0945-1 · Cited by 451 · 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
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
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
Self-citationMetabolic 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
Hamacher, T., Becker, J., Gárdonyi, M., Hahn‐Hägerdal, B., & Boles, E. (2002) · Microbiology · doi:10.1099/00221287-148-9-2783 · Cited by 317 · see citing works
Self-citationInvolvement of kinases in glucose and fructose uptake by Saccharomyces cerevisiae.
Bisson, L. F., & Fraenkel, D. G. (1983) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.80.6.1730 · Cited by 306 · 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
Self-citationKötter, P., Amore, R., Hollenberg, C. P., & Ciriacy, M. (1990) · Current Genetics · doi:10.1007/bf00327019 · Cited by 281 · see citing works
Simultaneous co-fermentation of mixed sugars: a promising strategy for producing cellulosic ethanol
Kim, S. R., Ha, S.-J., Wei, N., Oh, E. J., & Jin, Y. (2012) · Trends in biotechnology · doi:10.1016/j.tibtech.2012.01.005 · Cited by 241 · 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
Rewiring yeast sugar transporter preference through modifying a conserved protein motif
Young, E. M., Tong, A., Bui, H., Spofford, C., & Alper, H. S. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1311970111 · Cited by 197 · 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
Leandro, M. J., Gonçalves, P. M., & Spencer‐Martins, I. (2006) · Biochemical Journal · doi:10.1042/bj20051465 · Cited by 168 · see citing works
Young, E. M., Poucher, A., Comer, A. D., Bailey, A. S., & Alper, H. S. (2011) · Applied and Environmental Microbiology · doi:10.1128/aem.02651-10 · Cited by 165 · see citing works
Henderson, P. J. F., & Maiden, M. C. J. (1990) · Philosophical transactions of the Royal Society of London. Series B, Biological sciences · doi:10.1098/rstb.1990.0020 · Cited by 159 · see citing works
Subtil, T., & Boles, E. (2012) · Biotechnology for Biofuels · doi:10.1186/1754-6834-5-14 · Cited by 158 · see citing works
Self-citationAffinity of glucose transport in Saccharomyces cerevisiae is modulated during growth on glucose
Walsh, M. C., Smits, H. P., Scholte, M. E., & DAM, K. V. (1994) · Journal of Bacteriology · doi:10.1128/jb.176.4.953-958.1994 · Cited by 154 · see citing works
Properties of the sugar carrier in baker's yeast
Kotyk, A. (1967) · Folia Microbiologica · doi:10.1007/bf02896872 · Cited by 146 · see citing works
Liang, H., & Gaber, R. F. (1996) · Molecular Biology of the Cell · doi:10.1091/mbc.7.12.1953 · Cited by 139 · see citing works
Young, E. M., Comer, A. D., Huang, H., & Alper, H. S. (2012) · Metabolic Engineering · doi:10.1016/j.ymben.2012.03.004 · Cited by 138 · see citing works
Weierstall, T., Hollenberg, C. P., & Boles, E. (1999) · Molecular Microbiology · doi:10.1046/j.1365-2958.1999.01224.x · Cited by 137 · see citing works
Self-citationStructural basis for substrate transport in the GLUT-homology family of monosaccharide transporters
Quistgaard, E. M., Löw, C., Moberg, P., Tresaugues, L., & Nordlund, P. (2013) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.2569 · Cited by 136 · see citing works
Comparison of heterologous xylose transporters in recombinant Saccharomyces cerevisiae
Runquist, D., Hahn‐Hägerdal, B., & Rådström, P. (2010) · Biotechnology for Biofuels · doi:10.1186/1754-6834-3-5 · Cited by 134 · see citing works
Crystal structure of a glucose/H + symporter and its mechanism of action
Iancu, C. V., Zamoon, J., Woo, S. B., Aleshin, A. E., & Choe, J. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1311485110 · Cited by 132 · see citing works
Katahira, S., Ito, M., Takema, H., Fujita, Y., Tanino, T., Tanaka, T., Fukuda, H., & Kondo, A. (2008) · Enzyme and Microbial Technology · doi:10.1016/j.enzmictec.2008.03.001 · Cited by 130 · see citing works
Runquist, D., Fonseca, C., Rådström, P., Spencer‐Martins, I., & Hahn‐Hägerdal, B. (2008) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-008-1773-y · Cited by 121 · see citing works
Du, J., Li, S., & Zhao, H. (2010) · Molecular BioSystems · doi:10.1039/c0mb00007h · Cited by 121 · 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
Kinetic studies on glucose and xylose transport in Saccharomyces cerevisiae
W.-J., L., M.-D., K., Ryu, Y. W., Bisson, L. F., & J.-H., S. (2002) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-002-1085-6 · Cited by 116 · see citing works
Properties of the sugar carrier in baker's yeast
Kotyk, A. (1965) · Folia Microbiologica · doi:10.1007/bf02869838 · Cited by 98 · see citing works
Transport of hemicellulose monomers in the xylose-fermenting yeastCandida shehatae
Lucas, C., & van Uden, N. O. P. (1986) · Applied Microbiology and Biotechnology · doi:10.1007/bf02346066 · Cited by 97 · see citing works
Control of xylose consumption by xylose transport in recombinant Saccharomyces cerevisiae
Gárdonyi, M., Jeppsson, M., Lidén, G., Gorwa‐Grauslund, M. F., & Hahn‐Hägerdal, B. (2003) · Biotechnology and Bioengineering · doi:10.1002/bit.10631 · Cited by 92 · see citing works
Parachin, N. S., Bergdahl, B. M., van Niel, E. W. J., & Gorwa‐Grauslund, M. F. (2011) · Metabolic Engineering · doi:10.1016/j.ymben.2011.05.005 · Cited by 87 · see citing works
Proton-linked D-xylose transport in Escherichia coli
Lam, V. M. S., Daruwalla, K. R., Henderson, P. J. F., & Jones-Mortimer, M. C. (1980) · Journal of Bacteriology · doi:10.1128/jb.143.1.396-402.1980 · Cited by 85 · see citing works
Transport and Utilization of Hexoses and Pentoses in the Halotolerant Yeast Debaryomyces hansenii
Nobre, A., Lucas, C., & Leão, C. (1999) · Applied and Environmental Microbiology · doi:10.1128/aem.65.8.3594-3598.1999 · Cited by 78 · see citing works
Carter, Z., & Delneri, D. (2010) · Yeast · doi:10.1002/yea.1774 · Cited by 76 · see citing works
High capacity xylose transport in Candida intermedia PYCC 4715
Gárdonyi, M., OSTERBERG, M., Rodrigues, C., Spencer‐Martins, I., & Hähn‐Hägerdal, B. (2003) · FEMS Yeast Research · doi:10.1111/j.1567-1364.2003.tb00137.x · Cited by 65 · see citing works
Isobutanol production from d -xylose by recombinantSaccharomyces cerevisiae
Brat, D., & Boles, E. (2012) · FEMS Yeast Research · doi:10.1111/1567-1364.12028 · Cited by 58 · see citing works
Self-citationDelgenès, J. P., Moletta, R., & Navarro, J. M. (1989) · Biotechnology and Bioengineering · doi:10.1002/bit.260340314 · Cited by 39 · see citing works
Fermentation ofd-xylose,d-glucose andl-arabinose mixture byPichia stipitis Y 7124: sugar tolerance
Delgenès, J., Moletta, R., & Navarro, J. M. (1988) · Applied Microbiology and Biotechnology · doi:10.1007/bf00939300 · Cited by 35 · see citing works
Tanino, T., Ito, T., Ogino, C., Ohmura, N., Ohshima, T., & Kondo, A. (2012) · Journal of Bioscience and Bioengineering · doi:10.1016/j.jbiosc.2012.03.004 · Cited by 24 · see citing works
Identification of a Key Residue Determining Substrate Affinity in the Yeast Glucose Transporter Hxt7
Kasahara, T., & Kasahara, M. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.149716 · Cited by 24 · see citing works
This is about the in and the out
Henderson, P. J. F., & Baldwin, S. A. (2013) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.2604 · Cited by 23 · see citing works
Kasahara, T., Shimogawara, K., & Kasahara, M. (2011) · Biochemistry · doi:10.1021/bi200958s · Cited by 22 · see citing works
Delgenès, J., Moletta, R., & Navarro, J. M. (1988) · Applied Microbiology and Biotechnology · doi:10.1007/bf00251695 · Cited by 10 · see citing works
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Liao, J. C., Mi, L., Pontrelli, S., & Luo, S. (2016) · Nature Reviews Microbiology · doi:10.1038/nrmicro.2016.32 · Cited by 597 · see citing works
Synthetic Biology Tools to Engineer Microbial Communities for Biotechnology
McCarty, N. S., & Ledesma‐Amaro, R. (2018) · Trends in biotechnology · doi:10.1016/j.tibtech.2018.11.002 · Cited by 585 · see citing works
Cellulosic ethanol production: Progress, challenges and strategies for solutions
Liu, C., Xiao, Y., Xia, X., Zhao, X., Peng, L., Srinophakun, P., & Bai, F. (2019) · Biotechnology Advances · doi:10.1016/j.biotechadv.2019.03.002 · Cited by 418 · 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
Structure and mechanism of the mammalian fructose transporter GLUT5
Nomura, N., Verdon, G., Kang, H. J., Shimamura, T., Nomura, Y., Sonoda, Y., Hussien, S. A., Qureshi, A. A., Coincon, M., Sato, Y., et al. (2015) · Nature · doi:10.1038/nature14909 · Cited by 240 · see citing works
Metabolic engineering of Yarrowia lipolytica to produce chemicals and fuels from xylose
Ledesma‐Amaro, R., Lazar, Z., Rakicka, M., Guo, Z., Fouchard, F., Coq, A.-M. C.-L., & Nicaud, J. (2016) · Metabolic Engineering · doi:10.1016/j.ymben.2016.07.001 · Cited by 234 · see citing works
Rollin, J. A., del Campo, J. S. M., Myung, S., Sun, F., You, C., Bakovic, A., Castro, R., Chandrayan, S. K., Wu, C.-H., Adams, M. W. W., et al. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1417719112 · Cited by 232 · see citing works
Metabolic Engineering for Expanding the Substrate Range of Yarrowia lipolytica
Ledesma‐Amaro, R., & Nicaud, J. (2016) · Trends in biotechnology · doi:10.1016/j.tibtech.2016.04.010 · Cited by 227 · 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
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Volk, M., Tran, V. G., Tan, S., Mishra, S., Fatma, Z., Boob, A. G., Li, H., Xue, P., Martin, T. A., & Zhao, H. (2022) · Chemical Reviews · doi:10.1021/acs.chemrev.2c00403 · Cited by 204 · see citing works
Challenges and prospects of xylitol production with whole cell bio-catalysis: A review
Dasgupta, D., Bandhu, S., Adhikari, D. K., & Ghosh, D. (2017) · Microbiological Research · doi:10.1016/j.micres.2016.12.012 · Cited by 199 · see citing works
Biobased organic acids production by metabolically engineered microorganisms
Chen, Y., & Nielsen, J. (2015) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2015.11.004 · Cited by 174 · see citing works
Simplified CRISPR-Cas genome editing for Saccharomyces cerevisiae
Generoso, W. C., Gottardi, M., Oreb, M., & Boles, E. (2016) · Journal of Microbiological Methods · doi:10.1016/j.mimet.2016.06.020 · Cited by 168 · see citing works
Self-citationMans, 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
Pandiyan, K., Singh, A., Singh, S., Saxena, A. K., & Nain, L. (2019) · Renewable Energy · doi:10.1016/j.renene.2018.08.049 · Cited by 166 · see citing works
Production of biofuels and chemicals from xylose using native and engineered yeast strains
Kwak, S., Jo, J.-H., Yun, E. J., Jin, Y., & Seo, J. (2018) · Biotechnology Advances · doi:10.1016/j.biotechadv.2018.12.003 · Cited by 163 · 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
Hernández-Pérez, A. F., de Arruda, P. V., Sene, L., da Silva, S. S., Chandel, A. K., & Felipe, M. D. G. D. A. (2019) · Critical Reviews in Biotechnology · doi:10.1080/07388551.2019.1640658 · Cited by 159 · see citing works
Lignocellulosic conversion into value-added products: A review
Haldar, D., & Purkait, M. K. (2019) · Process Biochemistry · doi:10.1016/j.procbio.2019.10.001 · Cited by 156 · see citing works
Narisetty, V., Cox, R., Bommareddy, R. R., Agrawal, D., Ahmạd, E., Pant, K. K., Chandel, A. K., Bhatia, S. K., Kumar, D., Binod, P., et al. (2021) · Sustainable Energy & Fuels · doi:10.1039/d1se00927c · Cited by 136 · see citing works
Ruchała, J., Kurylenko, O. O., Dmytruk, K. V., & Sibirny, A. А. (2019) · Journal of Industrial Microbiology & Biotechnology · doi:10.1007/s10295-019-02242-x · Cited by 132 · see citing works
Nijland, J. G., Shin, H. Y., de Jong, R. M., de Waal, P. P., Klaassen, P., & Driessen, A. J. M. (2014) · Biotechnology for Biofuels · doi:10.1186/s13068-014-0168-9 · 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
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
Harnessing xylose pathways for biofuels production
Li, X., Chen, Y., & Nielsen, J. (2019) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2019.01.006 · Cited by 116 · see citing works
François, J., Alkım, C., & Morin, N. (2020) · Biotechnology for Biofuels · doi:10.1186/s13068-020-01744-6 · Cited by 115 · see citing works
Engineering strategies to optimize lignocellulosic biorefineries
Long, B., Zhang, F., Dai, S. Y., Foston, M. B., Tang, Y., & Yuan, J. S. (2024) · Nature Reviews Bioengineering · doi:10.1038/s44222-024-00247-5 · Cited by 114 · 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
Wess, J., Brinek, M., & Boles, E. (2019) · Biotechnology for Biofuels · doi:10.1186/s13068-019-1486-8 · Cited by 103 · see citing works
Self-citationTran, 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
Lane, S., Xu, H., Oh, E. J., Kim, H., Lesmana, A., Jeong, D., Zhang, G.-C., Tsai, C., Jin, Y., & Kim, S. R. (2018) · Scientific Reports · doi:10.1038/s41598-018-20804-4 · Cited by 98 · see citing works
Protzko, R. J., Latimer, L. N., Martinho, Z., de Reus, E., Seibert, T., Benz, J. P., & Dueber, J. E. (2018) · Nature Communications · doi:10.1038/s41467-018-07589-w · Cited by 96 · see citing works
Li, Y., Wang, M., Chen, Y., Wang, M., Fan, L., & Tan, T. (2017) · Scientific Reports · doi:10.1038/srep43875 · Cited by 95 · see citing works
An artificial transport metabolon facilitates improved substrate utilization in yeast
Thomik, T., Wittig, I., Choe, J., Boles, E., & Oreb, M. (2017) · Nature Chemical Biology · doi:10.1038/nchembio.2457 · Cited by 94 · see citing works
Self-citationNogueira, K. M. V., de Paula, R. G., Antoniêto, A. C. C., dos Reis, T. F., Carraro, C. B., Silva, A. C., Almeida, F. B. D. R., Vargas-Rechia, C. G., Goldman, G. H., & Silva, R. N. (2018) · Biotechnology for Biofuels · doi:10.1186/s13068-018-1084-1 · Cited by 93 · see citing works
Mixed carbon substrates: a necessary nuisance or a missed opportunity?
Liu, N., Santala, S., & Stephanopoulos, G. N. (2019) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2019.07.003 · Cited by 93 · see citing works
Wang, C., Bao, X., Li, Y., Jiao, C., Hou, J., Zhang, Q., Zhang, W., Liu, W., & Shen, Y. (2015) · Metabolic Engineering · doi:10.1016/j.ymben.2015.04.007 · Cited by 92 · see citing works
Sloothaak, J., Tamayo‐Ramos, J. A., Odoni, D. I., Laothanachareon, T., Derntl, C., Mach-Aigner, A. R., dos Santos, V. A. P. M., & Schaap, P. J. (2016) · Biotechnology for Biofuels · doi:10.1186/s13068-016-0564-4 · Cited by 92 · see citing works
Recent Developments in Lignocellulosic Biofuels, a Renewable Source of Bioenergy
Rai, A. K., Al Makishah, N. H., Wen, Z., Gupta, G., Pandit, S., & Prasad, R. (2022) · Fermentation · doi:10.3390/fermentation8040161 · Cited by 90 · see citing works
Converting Sugars to Biofuels: Ethanol and Beyond
Kang, A., & Lee, T. S. (2015) · Bioengineering · doi:10.3390/bioengineering2040184 · Cited by 90 · 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
Activating and Elucidating Metabolism of Complex Sugars in Yarrowia lipolytica
Ryu, S., Hipp, J., & Trinh, C. T. (2015) · Applied and Environmental Microbiology · doi:10.1128/aem.03582-15 · Cited by 89 · see citing works
Scaling up xylitol bioproduction: Challenges to achieve a profitable bioprocess
Queiroz, S. D. S., Jofre, F. M., Mussatto, S. I., & Felipe, M. D. G. D. A. (2021) · Renewable and Sustainable Energy Reviews · doi:10.1016/j.rser.2021.111789 · Cited by 88 · 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
Schadeweg, V., & Boles, E. (2016) · Biotechnology for Biofuels · doi:10.1186/s13068-016-0456-7 · Cited by 82 · see citing works
Self-citationJordan, P., Choe, J., Boles, E., & Oreb, M. (2016) · Scientific Reports · doi:10.1038/srep23502 · Cited by 82 · see citing works
Self-citationEnabling glucose/xylose co-transport in yeast through the directed evolution of a sugar transporter
Li, H., Schmitz, O., & Alper, H. S. (2016) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-016-7879-8 · Cited by 82 · see citing works
Wang, L. F., York, S. W., Ingram, L. O., & Shanmugam, K. T. (2018) · Bioresource Technology · doi:10.1016/j.biortech.2018.11.016 · Cited by 82 · see citing works
Transporter Engineering for Microbial Manufacturing
Zhu, Y. L., Zhou, C. X., Wang, Y., & Li, C. (2020) · Biotechnology Journal · doi:10.1002/biot.201900494 · Cited by 81 · see citing works
Shin, H. Y., Nijland, J. G., de Waal, P. P., de Jong, R. M., Klaassen, P., & Driessen, A. J. M. (2015) · Biotechnology for Biofuels · doi:10.1186/s13068-015-0360-6 · Cited by 79 · see citing works
Hua, Y., Wang, J., Zhu, Y., Zhang, B., Kong, X., Li, W., Wang, D., & Hong, J. (2019) · Microbial Cell Factories · doi:10.1186/s12934-019-1068-2 · Cited by 79 · see citing works
Zhang, K., Lu, X., Li, Y., Jiang, X., Liu, L., & Wang, H. (2019) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-019-09620-6 · Cited by 78 · 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
Metabolic engineering for improved production of ethanol by Corynebacterium glutamicum
Jojima, T., Noburyu, R., Sasaki, M., Tajima, T., Suda, M., Yukawa, H., & Inui, M. (2014) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-014-6223-4 · Cited by 75 · see citing works
dos Reis, T. F., de Lima, P. B. A., Parachin, N. S., Mingossi, F. B., Oliveira, J., Ries, L. N. A., & Goldman, G. H. (2016) · Biotechnology for Biofuels · doi:10.1186/s13068-016-0611-1 · Cited by 75 · 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
Brückner, C., Oreb, M., Kunze, G., Boles, E., & Tripp, J. (2018) · FEMS Yeast Research · doi:10.1093/femsyr/foy017 · Cited by 72 · see citing works
Self-citationWang, M., Li, S., & Zhao, H. (2015) · Biotechnology and Bioengineering · doi:10.1002/bit.25676 · Cited by 69 · see citing works
De novo biosynthesis of trans-cinnamic acid derivatives in Saccharomyces cerevisiae
Gottardi, M., Knudsen, J. D., Prado, L., Oreb, M., Branduardi, P., & Boles, E. (2017) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-017-8220-x · Cited by 69 · see citing works
Self-citationIntegrating Systems and Synthetic Biology to Understand and Engineer Microbiomes
Leggieri, P. A., Liu, Y., Hayes, M. M., Connors, B., Seppälä, S., O’Malley, M., & Venturelli, O. S. (2021) · Annual Review of Biomedical Engineering · doi:10.1146/annurev-bioeng-082120-022836 · Cited by 68 · see citing works
Wang, C., Bao, X., Li, Y., Jiao, C., Hou, J., Zhang, Q., Zhang, W., Liu, W., & Shen, Y. (2015) · Data in Brief · doi:10.1016/j.dib.2015.05.005 · Cited by 68 · see citing works
Engineering Sugar Utilization and Microbial Tolerance toward Lignocellulose Conversion
Nieves, L. M., Panyon, L. A., & Wang, X. (2015) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2015.00017 · Cited by 67 · see citing works
Zhang, B., Zhang, J., Wang, D., Han, R., Ding, R., Gao, X., Sun, L., & Hong, J. (2016) · Bioresource Technology · doi:10.1016/j.biortech.2016.05.068 · Cited by 67 · see citing works
Schadeweg, V., & Boles, E. (2016) · Biotechnology for Biofuels · doi:10.1186/s13068-016-0673-0 · Cited by 66 · see citing works
Self-citationMicrobial conversion of xylose into useful bioproducts
Jagtap, S. S., & Rao, C. V. (2018) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-018-9294-9 · Cited by 66 · see citing works
d ‐Xylose consumption by nonrecombinant Saccharomyces cerevisiae : A review
Lagos, M. A. P., Ortiz, J. P. D., Velásquez, M., & Stambuk, B. U. (2019) · Yeast · doi:10.1002/yea.3429 · Cited by 65 · 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
Renewable fuels from biomass: Technical hurdles and economic assessment of biological routes
Klein‐Marcuschamer, D., & Blanch, H. W. (2015) · AIChE Journal · doi:10.1002/aic.14755 · Cited by 64 · see citing works
Seike, T., Kobayashi, Y., Sahara, T., Ohgiya, S., Kamagata, Y., & Fujimori, K. E. (2019) · Biotechnology for Biofuels · doi:10.1186/s13068-019-1474-z · Cited by 63 · see citing works
Nijland, J. G., Vos, E. P. P., Shin, H. Y., de Waal, P. P., Klaassen, P., & Driessen, A. J. M. (2016) · Biotechnology for Biofuels · doi:10.1186/s13068-016-0573-3 · Cited by 61 · see citing works
Directed evolution of xylose specific transporters to facilitate glucose‐xylose co‐utilization
Wang, M., Yu, C., & Zhao, H. (2015) · Biotechnology and Bioengineering · doi:10.1002/bit.25724 · Cited by 60 · 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
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
Co-utilization of carbon sources in microorganisms for the bioproduction of chemicals
Ma, Q., Yi, J., Tang, Y., Geng, Z., Zhang, C., Sun, W., Liu, Z., Xiong, W., Wu, H., & Xie, X. (2024) · Biotechnology Advances · doi:10.1016/j.biotechadv.2024.108380 · Cited by 58 · see citing works
Zou, X., Yang, J., Xu, T., Guo, M., Li, Z., & Li, Y. (2015) · Process Biochemistry · doi:10.1016/j.procbio.2015.11.018 · Cited by 58 · 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
Zhang, L., Liu, Q., Ge, Y., Li, L., Gao, C., Xu, P., & Ma, C. (2015) · Green Chemistry · doi:10.1039/c5gc01638j · 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
Metabolic Engineering Strategies for Co-Utilization of Carbon Sources in Microbes
Wu, Y., Shen, X., Yuan, Q., & Yan, Y. (2016) · Bioengineering · doi:10.3390/bioengineering3010010 · Cited by 55 · see citing works
Transporter engineering in biomass utilization by yeast
Hara, K. Y., Kobayashi, J., Yamada, R., Sasaki, D., Kuriya, Y., Hirono-Hara, Y., Ishii, J., Araki, M., & Kondo, A. (2017) · FEMS Yeast Research · doi:10.1093/femsyr/fox061 · Cited by 55 · 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
Utilizing yeasts for the conversion of renewable feedstocks to sugar alcohols - a review
Erian, A. M., & Sauer, M. (2021) · Bioresource Technology · doi:10.1016/j.biortech.2021.126296 · Cited by 55 · see citing works
Sun, L., & Jin, Y. (2020) · Biotechnology Journal · doi:10.1002/biot.202000142 · Cited by 54 · see citing works
Metabolic engineering for the utilization of carbohydrate portions of lignocellulosic biomass
Kim, J., Hwang, S., & Lee, S. (2021) · Metabolic Engineering · doi:10.1016/j.ymben.2021.10.002 · Cited by 54 · see citing works
Teo, W. S., & Chang, M. W. (2014) · Biotechnology Journal · doi:10.1002/biot.201400159 · Cited by 53 · see citing works
Ryu, S., & Trinh, C. T. (2017) · Applied and Environmental Microbiology · doi:10.1128/aem.02146-17 · Cited by 53 · see citing works
Xylose transport in yeast for lignocellulosic ethanol production: Current status
Sharma, N. K., Behera, S., Arora, R., Kumar, S., & Sani, R. K. (2017) · Journal of Bioscience and Bioengineering · doi:10.1016/j.jbiosc.2017.10.006 · Cited by 50 · see citing works
Improved Xylose Metabolism by a CYC8 Mutant of Saccharomyces cerevisiae
Nijland, J. G., Shin, H. Y., Boender, L. G. M., de Waal, P. P., Klaassen, P., & Driessen, A. J. M. (2017) · Applied and Environmental Microbiology · doi:10.1128/aem.00095-17 · Cited by 49 · see citing works
Xiao, Q., Ma, F., Li, Y., Yu, H., Li, C., & Zhang, X. (2017) · Frontiers in Microbiology · doi:10.3389/fmicb.2017.00480 · Cited by 49 · 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
Assessing Glucose Uptake through the Yeast Hexose Transporter 1 (Hxt1)
Roy, A., Dement, A. D., Cho, K. H., & Kim, J. (2015) · PLoS ONE · doi:10.1371/journal.pone.0121985 · 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
Jiang, Y., Shen, Y., Gu, L., Wang, Z., Su, N., Niu, K., Guo, W., Hou, S., Bao, X., Tian, C., et al. (2020) · Journal of Agricultural and Food Chemistry · doi:10.1021/acs.jafc.9b07113 · 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
Bracher, J. M., Verhoeven, M. D., Wisselink, H. W., Crimi, B., Nijland, J. G., Driessen, A. J. M., Klaassen, P., van Maris, A. J. A., Daran, J.-M. G., & Pronk, J. T. (2018) · Biotechnology for Biofuels · doi:10.1186/s13068-018-1047-6 · Cited by 47 · see citing works
Yukawa, T., Bamba, T., Guirimand, G. G. Y., Matsuda, M., Hasunuma, T., & Kondo, A. (2020) · Biotechnology and Bioengineering · doi:10.1002/bit.27560 · Cited by 46 · see citing works
- Authors
- Farwick, A., Bruder, S., Schadeweg, V., Oreb, M., & Boles, E.
- Affiliations
- Goethe University Frankfurt (DE)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2014-03-24
- Volume
- 111
- Issue
- 14
- Pages
- 5159-5164
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC3986176
- OpenAlex
- W2118069954
- Cited by
- 298
- References
- 54
- Citations by year
- 2026: 20 · 2025: 12 · 2024: 17 · 2023: 20 · 2022: 25 · 2021: 35 · 2020: 28 · 2019: 26 · 2018: 26 · 2017: 35 · 2016: 26 · 2015: 22 · 2014: 6
- FWCI
- 12.16
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
- Physical Sciences › Engineering › Biomedical Engineering › Biofuel production and bioconversion
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Microbial Metabolic Engineering and Bioproduction
- Keywords
- hexose transporters, GAL2, XylE, sugar specificity, competitive inhibition, lignocellulosic biomass, Saccharomyces cerevisiae
- MeSH terms
- Biological Transport, Glucose, Hydrolysis, Models, Molecular, Monosaccharide Transport Proteins, Saccharomyces cerevisiae, Xylose, Protein Engineering, Mutagenesis, Site-Directed
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