High‐level production of amorpha‐4,11‐diene in a two‐phase partitioning bioreactor of metabolically engineered Escherichia coli
Abstract
Reconstructing synthetic metabolic pathways in microbes holds great promise for the production of pharmaceuticals in large-scale fermentations. By recreating biosynthetic pathways in bacteria, complex molecules traditionally harvested from scarce natural resources can be produced in microbial cultures. Here we report on a strain of Escherichia coli containing a heterologous, nine-gene biosynthetic pathway for the production of the terpene amorpha-4,11-diene, a precursor to the anti-malarial drug artemisinin. Previous reports have underestimated the productivity of this strain due to the volatility of amorphadiene. Here we show that amorphadiene evaporates from a fermentor with a half-life of about 50 min. Using a condenser, we take advantage of this volatility by trapping the amorphadiene in the off-gas. Amorphadiene was positively identified using nuclear magnetic resonance spectroscopy and determined to be 89% pure as collected. We captured amorphadiene as it was produced in situ by employing a two-phase partitioning bioreactor with a dodecane organic phase. Using a previously characterized caryophyllene standard to calibrate amorphadiene production and capture, the concentration of amorphadiene produced was determined to be 0.5 g/L of culture medium. A standard of amorphadiene collected from the off-gas showed that the caryophyllene standard overestimated amorphadiene production by approximately 30%.
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Both Saccharomyces cerevisiae and Escherichia coli have been used as hosts when attempting to establish a viable recombinant microbial pathway for artemisinin biosynthesis.
“Both Saccharomyces cerevisiae [379,380] and Escherichia coli [381,382,383] have been used as hosts when attempting to establish a viable recombinant microbial pathway for the biosynthesis of artemisinin.”
From The Biosynthesis of Artemisinin (Qinghaosu) and the Phytochemistry of Artemisia annua L. (Qinghao) (2010) · cites this paper as [380]
Cites
Guzman, L., Belin, D., Carson, M. J., & Beckwith, J. (1995) · Journal of Bacteriology · doi:10.1128/jb.177.14.4121-4130.1995 · Cited by 4,942 · see citing works
Kovach, M. E., Elzer, P. H., Hill, D. S., Robertson, G. T., Farris, M. A., Roop, R. M., & Peterson, K. M. (1995) · Gene · doi:10.1016/0378-1119(95)00584-1 · Cited by 3,355 · see citing works
Engineering a mevalonate pathway in Escherichia coli for production of terpenoids
Martin, V. J. J., Pitera, D. J., Withers, S. T., Newman, J. D., & Keasling, J. D. (2003) · Nature Biotechnology · doi:10.1038/nbt833 · Cited by 1,720 · see citing works
Amann, E. P., Ochs, B., & Kj, A. (1988) · Gene · doi:10.1016/0378-1119(88)90440-4 · Cited by 1,045 · see citing works
Mechanisms of Solvent Tolerance in Gram-Negative Bacteria
Ramos, J. L., Duque, E., Gallegos, M., Godoy, P., Ramos‐González, M. I., Rojas, A., Terán, W., & Segura, A. (2002) · Annual Review of Microbiology · doi:10.1146/annurev.micro.56.012302.161038 · Cited by 792 · see citing works
Biosynthesis of Complex Polyketides in a Metabolically Engineered Strain of E. coli
Pfeifer, B. A., Admiraal, S. J., Gramajo, H. C., Cane, D. E., & Khosla, C. (2001) · Science · doi:10.1126/science.1058092 · Cited by 751 · see citing works
Recombinant expression systems in the pharmaceutical industry
Schmidt, F. R. (2004) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-004-1656-9 · Cited by 380 · see citing works
Monoterpene biosynthesis pathway construction in Escherichia coli
Carter, O. A., Peters, R. J., & Croteau, R. (2003) · Phytochemistry · doi:10.1016/s0031-9422(03)00204-8 · Cited by 157 · see citing works
Picaud, S., Olofsson, L., Brodelius, M., & Brodelius, P. E. (2005) · Archives of Biochemistry and Biophysics · doi:10.1016/j.abb.2005.02.012 · Cited by 117 · see citing works
Production of the Potent Antibacterial Polyketide Erythromycin C in Escherichia coli
Peirú, S., Menzella, H. G., Rodrı́guez, E., Carney, J. R., & Gramajo, H. C. (2005) · Applied and Environmental Microbiology · doi:10.1128/aem.71.5.2539-2547.2005 · Cited by 103 · see citing works
Janikowski, T. B., Velicogna, D., Punt, M., & Daugulis, A. J. (2002) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-002-1011-y · Cited by 96 · see citing works
Collins, L. D., & Daugulis, A. J. (1999) · Applied Microbiology and Biotechnology · doi:10.1007/s002530051531 · Cited by 93 · see citing works
Daugulis, A. J. (1997) · Current Opinion in Biotechnology · doi:10.1016/s0958-1669(97)80097-3 · Cited by 57 · see citing works
Daugulis, A. J., & Janikowski, T. B. (2002) · Biotechnology Letters · doi:10.1023/a:1015080700477 · Cited by 34 · see citing works
Current and Emerging Approaches for Natural Product Biosynthesis in Microbial Cells
Watts, K. T., Mijts, B. N., & Schmidt‐Dannert, C. (2005) · Advanced Synthesis & Catalysis · doi:10.1002/adsc.200505062 · Cited by 33 · see citing works
Muurolane Sesquiterpenes from Illicium tsangii
Ngo, K., Wong, W., & Brown, G. D. (1999) · Journal of Natural Products · doi:10.1021/np980289m · Cited by 27 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Westfall, P. J., Pitera, D. J., Lenihan, J. R., Eng, D., Woolard, F. X., Regentin, R., Horning, T., Tsuruta, H., Melis, D. J., Owens, A. E., et al. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1110740109 · Cited by 726 · see citing works
Pan, S.-Y., Zhou, S.-F., Gao, S.-H., Yu, Z., Zhang, S.-F., Tang, M.-K., Sun, J.-N., Ma, D., Han, Y., Fong, W. F., et al. (2013) · Evidence-based Complementary and Alternative Medicine · doi:10.1155/2013/627375 · Cited by 723 · see citing works
Semi-synthetic artemisinin: a model for the use of synthetic biology in pharmaceutical development
Paddon, C. J., & Keasling, J. D. (2014) · Nature Reviews Microbiology · doi:10.1038/nrmicro3240 · Cited by 675 · see citing works
Biosynthesis of Plant Isoprenoids: Perspectives for Microbial Engineering
Kirby, J., & Keasling, J. D. (2009) · Annual Review of Plant Biology · doi:10.1146/annurev.arplant.043008.091955 · Cited by 478 · see citing works
Terpenoids: Opportunities for Biosynthesis of Natural Product Drugs Using Engineered Microorganisms
Ajikumar, P. K., Tyo, K. E. J., Carlsen, S., Mucha, O., Too, H., & Stephanopoulos, G. N. (2008) · Molecular Pharmaceutics · doi:10.1021/mp700151b · Cited by 445 · see citing works
Balancing a heterologous mevalonate pathway for improved isoprenoid production in Escherichia coli
Pitera, D. J., Paddon, C. J., Newman, J. D., & Keasling, J. D. (2006) · Metabolic Engineering · doi:10.1016/j.ymben.2006.11.002 · Cited by 440 · see citing works
Synthetic biology and the development of tools for metabolic engineering
Keasling, J. D. (2012) · Metabolic Engineering · doi:10.1016/j.ymben.2012.01.004 · Cited by 430 · see citing works
Synthetic Biology for Synthetic Chemistry
Keasling, J. D. (2008) · ACS Chemical Biology · doi:10.1021/cb7002434 · Cited by 409 · see citing works
Production of isoprenoid pharmaceuticals by engineered microbes
Chang, M. C. Y., & Keasling, J. D. (2006) · Nature Chemical Biology · doi:10.1038/nchembio836 · Cited by 388 · see citing works
Advanced biofuel production in microbes
Peralta‐Yahya, P., & Keasling, J. D. (2010) · Biotechnology Journal · doi:10.1002/biot.200900220 · Cited by 389 · see citing works
Engineering Escherichia coli for production of functionalized terpenoids using plant P450s
Chang, M. C. Y., Eachus, R. A., Trieu, W., Ro, D.-K., & Keasling, J. D. (2007) · Nature Chemical Biology · doi:10.1038/nchembio875 · Cited by 364 · see citing works
Self-citationTsuruta, H., Paddon, C. J., Eng, D., Lenihan, J. R., Horning, T., Anthony, L. C., Regentin, R., Keasling, J. D., Renninger, N. S., & Newman, J. D. (2009) · PLoS ONE · doi:10.1371/journal.pone.0004489 · Cited by 364 · see citing works
The Biosynthesis of Artemisinin (Qinghaosu) and the Phytochemistry of Artemisia annua L. (Qinghao)
Brown, G. D. (2010) · Molecules · doi:10.3390/molecules15117603 · Cited by 363 · see citing works
Fermentation-enabled wellness foods: A fresh perspective
Xiang, H., Sun‐Waterhouse, D., Waterhouse, G. I. N., Cui, C., & Ruan, Z. (2019) · Food Science and Human Wellness · doi:10.1016/j.fshw.2019.08.003 · Cited by 364 · see citing works
Methylerythritol Phosphate Pathway of Isoprenoid Biosynthesis
Zhao, L., Chang, W., Xiao, Y., Liu, H., & Liu, P. (2013) · Annual Review of Biochemistry · doi:10.1146/annurev-biochem-052010-100934 · Cited by 356 · see citing works
The potential of the mevalonate pathway for enhanced isoprenoid production
Liao, P., Hemmerlin, A., Bach, T. J., & Chye, M. (2016) · Biotechnology Advances · doi:10.1016/j.biotechadv.2016.03.005 · Cited by 332 · see citing works
The future of metabolic engineering and synthetic biology: Towards a systematic practice
Yadav, V. G., Mey, M. D., Lim, C. G., Ajikumar, P. K., & Stephanopoulos, G. N. (2012) · Metabolic Engineering · doi:10.1016/j.ymben.2012.02.001 · Cited by 323 · see citing works
Anthony, J. R., Anthony, L. C., Nowroozi, F., Kwon, G., Newman, J. D., & Keasling, J. D. (2009) · Metabolic Engineering · doi:10.1016/j.ymben.2008.07.007 · Cited by 292 · see citing works
Davies, F. K., Work, V. H., Beliaev, A. S., & Posewitz, M. C. (2014) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2014.00021 · Cited by 273 · see citing works
Antiviral Lead Compounds from Marine Sponges
Sagar, S., Kaur, M., & Minneman, K. P. (2010) · Marine Drugs · doi:10.3390/md8102619 · Cited by 263 · see citing works
Scalcinati, G., Knuf, C., Partow, S., Chen, Y., Maury, J., Schalk, M., Daviet, L., Nielsen, J., & Siewers, V. (2012) · Metabolic Engineering · doi:10.1016/j.ymben.2012.01.007 · Cited by 253 · see citing works
Asadollahi, M. A., Maury, J., Møller, K., Nielsen, K. F., Schalk, M., Clark, A., & Nielsen, J. (2007) · Biotechnology and Bioengineering · doi:10.1002/bit.21581 · Cited by 242 · see citing works
Lennen, R. M., Braden, D. J., West, R. M., Dumesic, J. A., & Pfleger, B. F. (2010) · Biotechnology and Bioengineering · doi:10.1002/bit.22660 · Cited by 238 · see citing works
Metabolic engineering of Saccharomyces cerevisiae for production of ginsenosides
Dai, Z., Liu, Y., Zhang, X., Shi, M., Wang, B., Wang, D., Huang, L., & Zhang, X. (2013) · Metabolic Engineering · doi:10.1016/j.ymben.2013.10.004 · Cited by 236 · see citing works
Huang, W., Wang, Y., Tian, W., Cui, X., Tu, P., Li, J., Shi, S., & Liu, X. (2022) · Antibiotics · doi:10.3390/antibiotics11101380 · Cited by 256 · see citing works
Metabolic engineering for plant natural product biosynthesis in microbes
Chemler, J. A., & Koffas, M. A. G. (2008) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2008.10.011 · Cited by 222 · see citing works
Asadollahi, M. A., Maury, J., Patil, K. R., Schalk, M., Clark, A., & Nielsen, J. (2009) · Metabolic Engineering · doi:10.1016/j.ymben.2009.07.001 · Cited by 213 · see citing works
Morrone, D. J., Lowry, L., Determan, M. K., Hershey, D. M., Xu, M., & Peters, R. J. (2009) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-009-2219-x · Cited by 211 · see citing works
Production of the sesquiterpenoid (+)-nootkatone by metabolic engineering of Pichia pastoris
Wriessnegger, T., Augustin, P., Engleder, M., Leitner, E., Müller, M., Kaluzna, I. A., Schürmann, M., Mink, D., Zellnig, G., Schwab, H., et al. (2014) · Metabolic Engineering · doi:10.1016/j.ymben.2014.04.001 · Cited by 203 · see citing works
Ro, D.-K., Ouellet, M., Paradise, E. M., Burd, H., Eng, D., Paddon, C. J., Newman, J. D., & Keasling, J. D. (2008) · BMC Biotechnology · doi:10.1186/1472-6750-8-83 · Cited by 197 · see citing works
Self-citationBrennan, T. C. R., Turner, C., Krömer, J. O., & Nielsen, L. K. (2012) · Biotechnology and Bioengineering · doi:10.1002/bit.24536 · Cited by 193 · see citing works
Chen, X., Gao, C., Guo, L., Hu, G., Luo, Q., Liu, J., Nielsen, J., Chen, J., & Liu, L. (2017) · Chemical Reviews · doi:10.1021/acs.chemrev.6b00804 · Cited by 193 · see citing works
Dietrich, J. A., Yoshikuni, Y., Fisher, K. J., Woolard, F. X., Ockey, D., McPhee, D. J., Renninger, N. S., Chang, M. C. Y., Baker, D., & Keasling, J. D. (2009) · ACS Chemical Biology · doi:10.1021/cb900006h · Cited by 186 · see citing works
Isoprenoid drugs, biofuels, and Chemicals–Artemisinin, farnesene, and beyond
George, K. W., Alonso-Gutierrez, J., Keasling, J. D., & Lee, T. S. (2015) · Advances in biochemical engineering, biotechnology · doi:10.1007/10_2014_288 · Cited by 185 · see citing works
Self-citationToward a Biosynthetic Route to Sclareol and Amber Odorants
Schalk, M., Pastore, L., Mirata, M. A., Khim, S., Schouwey, M., Deguerry, F., Pineda, V., Rocci, L., & Daviet, L. (2012) · Journal of the American Chemical Society · doi:10.1021/ja307404u · Cited by 183 · see citing works
Özaydın, B., Burd, H., Lee, T. S., & Keasling, J. D. (2012) · Metabolic Engineering · doi:10.1016/j.ymben.2012.07.010 · Cited by 182 · see citing works
The Sound of Silence: Activating Silent Biosynthetic Gene Clusters in Marine Microorganisms
Reen, F. J., Romano, S., Dobson, A. D. W., & O’Gara, F. (2015) · Marine Drugs · doi:10.3390/md13084754 · Cited by 180 · see citing works
Cuesta, S., Knopper, L., van der Wielen, L. A. M., & Cuellar, M. C. (2018) · Biofuels Bioproducts and Biorefining · doi:10.1002/bbb.1949 · Cited by 175 · see citing works
Enhancing Production of Bio-Isoprene Using Hybrid MVA Pathway and Isoprene Synthase in E. coli
Yang, J., Xian, M., Su, S., Zhao, G., Nie, Q., Jiang, X., Zheng, Y., & Liu, W. (2012) · PLoS ONE · doi:10.1371/journal.pone.0033509 · Cited by 174 · see citing works
Advances in in-situ product recovery (ISPR) in whole cell biotechnology during the last decade
Hecke, W. V., Kaur, G., & Wever, H. D. (2014) · Biotechnology Advances · doi:10.1016/j.biotechadv.2014.07.003 · Cited by 164 · see citing works
Optimization of a heterologous mevalonate pathway through the use of variant HMG-CoA reductases
Ma, S. M., Garcia, D. E., Redding‐Johanson, A. M., Friedland, G. D., Chan, R., Batth, T. S., Haliburton, J. R., Chivian, D. C., Keasling, J. D., Petzold, C. J., et al. (2011) · Metabolic Engineering · doi:10.1016/j.ymben.2011.07.001 · Cited by 161 · see citing works
Metabolic engineering for the high-yield production of isoprenoid-based C5 alcohols in E. coli
George, K. W., Thompson, M. G., Kang, A., Baidoo, E. E. K., Wang, G., Chan, L. J. G., Adams, P. D., Petzold, C. J., Keasling, J. D., & Lee, T. S. (2015) · Scientific Reports · doi:10.1038/srep11128 · Cited by 153 · see citing works
Towards efficient terpenoid biosynthesis: manipulating IPP and DMAPP supply
Wang, Q., Quan, S., & Xiao, H. (2019) · Bioresources and Bioprocessing · doi:10.1186/s40643-019-0242-z · Cited by 152 · see citing works
Paradise, E. M., Kirby, J., Chan, R., & Keasling, J. D. (2008) · Biotechnology and Bioengineering · doi:10.1002/bit.21766 · Cited by 148 · see citing works
Synthetic Biology Goes Cell-Free
Tinafar, A., Jaenes, K., & Pardee, K. (2019) · BMC Biology · doi:10.1186/s12915-019-0685-x · Cited by 142 · see citing works
Survey of artemisinin production by diverse Artemisia species in northern Pakistan
Mannan, A., Ahmed, I., Arshad, W., Asim, M., Qureshi, R. A., Hussain, I., & Mirza, B. (2010) · Malaria Journal · doi:10.1186/1475-2875-9-310 · Cited by 141 · see citing works
Guo, Y., Dong, J., Zhou, T., Auxillos, J., Li, T., Zhang, W., Wang, L., Shen, Y., Luo, Y., Zheng, Y., et al. (2015) · Nucleic Acids Research · doi:10.1093/nar/gkv464 · Cited by 135 · see citing works
Metabolic engineering of volatile isoprenoids in plants and microbes
Vickers, C. E., Bongers, M., Liu, Q., Delatte, T., & Bouwmeester, H. J. (2014) · Plant Cell & Environment · doi:10.1111/pce.12316 · Cited by 130 · see citing works
Willrodt, C., David, C., Cornelissen, S., Bühler, B., Julsing, M. K., & Schmid, A. (2014) · Biotechnology Journal · doi:10.1002/biot.201400023 · Cited by 125 · see citing works
Jervis, A. J., Carbonell, P., Vinaixa, M., Dunstan, M. S., Hollywood, K. A., Robinson, C., Rattray, N. J. W., Yan, C., Swainston, N., Currin, A., et al. (2018) · ACS Synthetic Biology · doi:10.1021/acssynbio.8b00398 · Cited by 121 · see citing works
Microbial production of isoprenoids
Chandran, S. S., Kealey, J. T., & Reeves, C. D. (2011) · Process Biochemistry · doi:10.1016/j.procbio.2011.05.012 · Cited by 121 · see citing works
Kennedy, J., Marchesi, J. R., & Dobson, A. D. W. (2007) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-007-0875-2 · Cited by 119 · see citing works
Metabolic Engineering of Microorganisms for the Production of Natural Compounds
Park, S. Y., Yang, D., Ha, S. H., & Lee, S. Y. (2017) · Advanced Biosystems · doi:10.1002/adbi.201700190 · Cited by 116 · see citing works
Alternative metabolic pathways and strategies to high-titre terpenoid production in Escherichia coli
Rinaldi, M. A., Ferraz, C. A., & Scrutton, N. S. (2021) · Natural Product Reports · doi:10.1039/d1np00025j · Cited by 117 · see citing works
Farnesol production from Escherichia coli by harnessing the exogenous mevalonate pathway
Wang, C., Yoon, S., Shah, A. A., Chung, Y., Kim, J., Choi, E., Keasling, J. D., & Kim, S.-W. (2010) · Biotechnology and Bioengineering · doi:10.1002/bit.22831 · Cited by 115 · see citing works
Metabolic pathway optimization using ribosome binding site variants and combinatorial gene assembly
Nowroozi, F. F., Baidoo, E. E. K., Ermakov, S., Redding‐Johanson, A. M., Batth, T. S., Petzold, C. J., & Keasling, J. D. (2013) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-013-5361-4 · Cited by 105 · see citing works
Biosynthesis of monoterpenoid and sesquiterpenoid as natural flavors and fragrances
Jiang, H., & Wang, X. (2023) · Biotechnology Advances · doi:10.1016/j.biotechadv.2023.108151 · Cited by 105 · see citing works
Navale, G. R., Dharne, M. S., & Shinde, S. S. (2021) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-020-11040-w · Cited by 102 · see citing works
Shaw, J. J., Berbasova, T., Sasaki, T., Jefferson‐George, K., Spakowicz, D. J., Dunican, B. F., Portero, C. E., Narváez‐Trujillo, A., & Strobel, S. A. (2015) · Journal of Biological Chemistry · doi:10.1074/jbc.m114.636159 · Cited by 95 · see citing works
Wang, C., Zada, B., Wei, G., & Kim, S.-W. (2017) · Bioresource Technology · doi:10.1016/j.biortech.2017.05.168 · Cited by 92 · see citing works
Monoterpene production by the carotenogenic yeast Rhodosporidium toruloides
Zhuang, X., Kilian, O., Monroe, E. A., Ito, M., Tran-Gyamfi, M. B., Liu, F., Davis, R., Mirsiaghi, M., Sundstrom, E. R., Pray, T. R., et al. (2019) · Microbial Cell Factories · doi:10.1186/s12934-019-1099-8 · Cited by 92 · see citing works
Current prospects for the production of coenzyme Q10 in microbes
Cluis, C. P., Burja, A. M., & Martin, V. J. J. (2007) · Trends in biotechnology · doi:10.1016/j.tibtech.2007.08.008 · Cited by 92 · see citing works
Metabolic engineering of microorganisms for isoprenoid production
Kirby, J., & Keasling, J. D. (2008) · Natural Product Reports · doi:10.1039/b802939c · Cited by 91 · see citing works
Living between two worlds: two-phase culture systems for producing plant secondary metabolites
Malik, S., Mirjalili, M. H., Fett‐Neto, A. G., Mazzafera, P., & Bonfill, M. (2012) · Critical Reviews in Biotechnology · doi:10.3109/07388551.2012.659173 · Cited by 90 · see citing works
Production of artemisinin by genetically-modified microbes
Zeng, Q.-P., Qiu, F., & Yuan, L. (2007) · Biotechnology Letters · doi:10.1007/s10529-007-9596-y · Cited by 87 · see citing works
Short-chain ketone production by engineered polyketide synthases in Streptomyces albus
Yuzawa, S., Mirsiaghi, M., Jocic, R., Fujii, T., Masson, F., Benites, V. T., Baidoo, E. E. K., Sundstrom, E. R., Tanjore, D., Pray, T. R., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-07040-0 · Cited by 88 · see citing works
Ding, M., Yan, H.-F., Li, L., Zhai, F., Shang, L., Yin, Z., & Yuan, Y. (2014) · PLoS ONE · doi:10.1371/journal.pone.0109348 · Cited by 88 · see citing works
Lenihan, J. R., Tsuruta, H., Diola, D., Renninger, N. S., & Regentin, R. (2008) · Biotechnology Progress · doi:10.1002/btpr.27 · Cited by 85 · 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
Harada, H., Yu, F., Okamoto, S., Kuzuyama, T., Utsumi, R., & Misawa, N. (2008) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-008-1724-7 · Cited by 79 · see citing works
Microbial biosynthesis of medicinally important plant secondary metabolites
Song, M., Kim, E. J., Kim, E., Rathwell, K., Nam, S., & Yoon, Y. J. (2014) · Natural Product Reports · doi:10.1039/c4np00057a · Cited by 78 · see citing works
Han, G. H., Kim, S. K., Yoon, P. K.-S., Kang, Y., Kim, B. S., Fu, Y., Jung, H.-C., Jung, H. C., Lee, D.-H., Kim, S.-W., et al. (2016) · Microbial Cell Factories · doi:10.1186/s12934-016-0588-2 · Cited by 72 · see citing works
Zhang, C., Chen, X., Zou, R., Zhou, K., Stephanopoulos, G. N., & Too, H. (2013) · PLoS ONE · doi:10.1371/journal.pone.0075164 · Cited by 66 · see citing works
From Plant to Yeast—Advances in Biosynthesis of Artemisinin
Zhao, L., Zhu, Y., Jia, H., Han, Y., Zheng, X., Wang, M., & Feng, W. (2022) · Molecules · doi:10.3390/molecules27206888 · Cited by 64 · see citing works
2,2-Diphenyl-1-picrylhydrazyl as a screening tool for recombinant monoterpene biosynthesis
Behrendorff, J. B. Y. H., Vickers, C. E., Chrysanthopoulos, P. K., & Nielsen, L. K. (2013) · Microbial Cell Factories · doi:10.1186/1475-2859-12-76 · Cited by 64 · see citing works
Novel trends for producing plant triterpenoids in yeast
Sun, W., Qin, L., Xue, H., Yu, Y., Ma, Y., Wang, Y., & Li, C. (2019) · Critical Reviews in Biotechnology · doi:10.1080/07388551.2019.1608503 · Cited by 63 · see citing works
Biology by design: reduction and synthesis of cellular components and behaviour
Marguet, P., Balagadde, F., Tan, C., & You, L. (2007) · Journal of The Royal Society Interface · doi:10.1098/rsif.2006.0206 · Cited by 63 · see citing works
Metabolic Engineering of Plant Secondary Products: Which Way Forward?
Miralpeix, B., Rischer, H., Häkkinen, S. T., Ritala, A., Seppänen‐Laakso, T., Oksman‐Caldentey, K., Capell, T., & Christou, P. (2013) · Current Pharmaceutical Design · doi:10.2174/1381612811319310016 · Cited by 61 · see citing works
A concise review on Artemisia annua L.: A major source of diverse medicinal compounds
Soni, R., Shankar, G., Mukhopadhyay, P., & Gupta, V. (2022) · Industrial Crops and Products · doi:10.1016/j.indcrop.2022.115072 · Cited by 62 · see citing works
Muangphrom, P., Seki, H., Fukushima, E. O., & Muranaka, T. (2016) · Journal of Natural Medicines · doi:10.1007/s11418-016-1008-y · Cited by 59 · see citing works
Zha, W., An, T., Li, T., Zhu, J., Gao, K., Sun, Z., Xu, W., Lin, P., & Zi, J. (2020) · ACS Synthetic Biology · doi:10.1021/acssynbio.9b00479 · Cited by 59 · see citing works
Metabolic engineering strategies for sesquiterpene production in microorganism
Liu, C., Xue, K., Yang, Y., Liu, X., Li, Y., Lee, T. S., Bai, Z., & Tan, T. (2021) · Critical Reviews in Biotechnology · doi:10.1080/07388551.2021.1924112 · Cited by 58 · see citing works
Analysis of heterologous taxadiene production in K- and B-derived Escherichia coli
Boghigian, B. A., Salas, D., Ajikumar, P. K., Stephanopoulos, G. N., & Pfeifer, B. A. (2011) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-011-3528-4 · Cited by 57 · see citing works
Perspectives and limits of engineering the isoprenoid metabolism in heterologous hosts
Muntendam, R., Melillo, E., Rydén, A., & Kayser, O. (2009) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-009-2150-1 · Cited by 56 · see citing works
Comparing in situ removal strategies for improving styrene bioproduction
McKenna, R., Moya, L., McDaniel, M., & Nielsen, D. R. (2014) · Bioprocess and Biosystems Engineering · doi:10.1007/s00449-014-1255-9 · Cited by 57 · see citing works
Novel approaches and achievements in biosynthesis of functional isoprenoids in Escherichia coli
Harada, H., & Misawa, N. (2009) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-009-2166-6 · Cited by 56 · see citing works
Butler, M. S., & Newman, D. J. (2007) · Birkhäuser Basel eBooks · doi:10.1007/978-3-7643-8117-2_1 · Cited by 55 · see citing works
Metabolic engineering of Bacillus subtilis for terpenoid production
Guan, Z., Xue, D., Abdallah, I. I., Dijkshoorn, L., Setroikromo, R., Lv, G., & Quax, W. J. (2015) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-015-6950-1 · Cited by 54 · see citing works
Exploiting Hydrogenophaga pseudoflava for aerobic syngas-based production of chemicals
Grenz, S., Baumann, P. T., Rückert, C., Nebel, B. A., Siebert, D. K., Schwentner, A., Eikmanns, B. J., Hauer, B., Kalinowski, J., Takors, R., et al. (2019) · Metabolic Engineering · doi:10.1016/j.ymben.2019.07.006 · Cited by 52 · see citing works
Yu, F., Okamoto, S., Harada, H., Yamasaki, K., Misawa, N., & Utsumi, R. (2010) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-010-0506-4 · Cited by 52 · see citing works
Systems Metabolic Engineering of Escherichia coli
Choi, K., Shin, J., Cho, J. S., Yang, D., & Lee, S. (2016) · EcoSal Plus · doi:10.1128/ecosalplus.esp-0010-2015 · Cited by 43 · see citing works
High-throughput screening for high-efficiency small-molecule biosynthesis
Rienzo, M., Jackson, S. J., Chao, L. K., Leaf, T. A., Schmidt, T. J., Navidi, A. H., Nadler, D. C., Ohler, M., & Leavell, M. D. (2020) · Metabolic Engineering · doi:10.1016/j.ymben.2020.09.004 · Cited by 50 · see citing works
Synthetic biology approaches in drug discovery and pharmaceutical biotechnology
Neumann, H., & Neumann‐Staubitz, P. (2010) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-010-2578-3 · Cited by 49 · see citing works
Polymer Selection for Biphenyl Degradation in a Solid-Liquid Two-Phase Partitioning Bioreactor
Rehmann, L., Sun, B., & Daugulis, A. J. (2007) · Biotechnology Progress · doi:10.1002/bp0700962 · Cited by 47 · see citing works
Modular biomanufacturing for a sustainable production of terpenoid-based insect deterrents
Mischko, W., Hirte, M., Roehrer, S., Engelhardt, H., Mehlmer, N., Minceva, M., & Brück, T. (2018) · Green Chemistry · doi:10.1039/c8gc00434j · Cited by 45 · see citing works
Dietsch, M., Behle, A., Westhoff, P., & Axmann, I. M. I. (2021) · Metabolic Engineering Communications · doi:10.1016/j.mec.2021.e00178 · Cited by 44 · see citing works
Current and Emerging Options for Taxol Production
Li, Y., Zhang, G., & Pfeifer, B. A. (2014) · Advances in biochemical engineering, biotechnology · doi:10.1007/10_2014_292 · Cited by 44 · see citing works
Jha, P., Ram, M., Khan, M. A., Kiran, U., Mahmooduzzafar, M., & Abdin, M. Z. (2011) · Industrial Crops and Products · doi:10.1016/j.indcrop.2010.12.011 · Cited by 44 · see citing works
Sun, Z., Meng, H., Li, J., Wang, J., Li, Q., Wang, Y., & Zhang, Y. (2014) · PLoS ONE · doi:10.1371/journal.pone.0112615 · Cited by 43 · see citing works
Hussain, M. H., Hong, Q., Zaman, W. Q., Mohsin, A., Wei, Y., Zhang, N., Fang, H., Wang, Z., Hang, H., Zhuang, Y., et al. (2021) · Synthetic and Systems Biotechnology · doi:10.1016/j.synbio.2021.04.001 · Cited by 42 · see citing works
- Authors
- Newman, J. D., Marshall, J., Chang, M., Nowroozi, F., Paradise, E., Pitera, D., Newman, K. L., & Keasling, J. D.
- Affiliations
- University of California, Berkeley (US)
- Lawrence Berkeley National Laboratory (US)
- Corresponding author
- Keasling, Jay D.
- Venue
- Biotechnology and Bioengineering
- Publisher
- Wiley
- Published
- 2006-07-28
- Volume
- 95
- Issue
- 4
- Pages
- 684-691
- ISSN
- 0006-3592 (ISSN-L)
- 1097-0290
- OpenAlex
- W2070190792
- Cited by
- 257
- References
- 16
- Citations by year
- 2026: 3 · 2025: 5 · 2024: 6 · 2023: 3 · 2022: 8 · 2021: 15 · 2020: 11 · 2019: 19 · 2018: 17 · 2017: 6 · 2016: 13 · 2015: 14 · 2014: 22 · 2013: 18 · 2012: 26
- FWCI
- 5.84
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Biotechnology and Bioengineering (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (1r41ai061936-01)
- National Institute of Allergy and Infectious Diseases (5 R41 AI061936-02)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Microbial Metabolic Engineering and Bioproduction
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Plant biochemistry and biosynthesis
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Biotechnology › Biochemical and biochemical processes
- Keywords
- terpene biosynthesis, Escherichia coli, metabolic engineering, two-phase partitioning bioreactor, n-dodecane
- MeSH terms
- Polycyclic Sesquiterpenes, Antimalarials, Escherichia coli, Fermentation, Gases, Half-Life, Sesquiterpenes, Terpenes, Volatilization, Bioreactors, Artemisinins
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