Dynamic regulation of metabolic flux in engineered bacteria using a pathway-independent quorum-sensing circuit

Apoorv Gupta; Irene M Brockman Reizman; Christopher R Reisch; Kristala L J Prather

doi:10.1038/nbt.3796

journal article Feb 13, 2017

Dynamic regulation of metabolic flux in engineered bacteria using a pathway-independent quorum-sensing circuit

Apoorv Gupta Irene M Brockman Reizman

Christopher R Reisch Kristala L J Prather

Nature Biotechnology Vol. 35 No. 3 pp. 273-279 · Springer Science and Business Media LLC

View at Publisher Save 10.1038/nbt.3796

Topics

No keywords indexed for this article. Browse by subject →

References

47

[1]

Alper, H., Miyaoku, K. & Stephanopoulos, G. Construction of lycopene-overproducing E. coli strains by combining systematic and combinatorial gene knockout targets. Nat. Biotechnol. 23, 612–616 (2005). 10.1038/nbt1083

[2]

Biggs, B.W., De Paepe, B., Santos, C.N.S., De Mey, M. & Kumaran Ajikumar, P. Multivariate modular metabolic engineering for pathway and strain optimization. Curr. Opin. Biotechnol. 29, 156–162 (2014). 10.1016/j.copbio.2014.05.005

[3]

Holtz, W.J. & Keasling, J.D. Engineering static and dynamic control of synthetic pathways. Cell 140, 19–23 (2010). 10.1016/j.cell.2009.12.029

[4]

Moon, T.S., Yoon, S.-H., Lanza, A.M., Roy-Mayhew, J.D. & Prather, K.L.J. Production of glucaric acid from a synthetic pathway in recombinant Escherichia coli. Appl. Environ. Microbiol. 75, 589–595 (2009). 10.1128/aem.00973-08

[5]

Rodrigues, A.L. et al. Systems metabolic engineering of Escherichia coli for production of the antitumor drugs violacein and deoxyviolacein. Metab. Eng. 20, 29–41 (2013). 10.1016/j.ymben.2013.08.004

[6]

Martin, V.J.J., Pitera, D.J., Withers, S.T., Newman, J.D. & Keasling, J.D. Engineering a mevalonate pathway in Escherichia coli for production of terpenoids. Nat. Biotechnol. 21, 796–802 (2003). 10.1038/nbt833

[7]

Just-in-time transcription program in metabolic pathways

Alon Zaslaver, Avi E Mayo, Revital Rosenberg et al.

Nature Genetics 2004 10.1038/ng1348

[8]

Farmer, W.R. & Liao, J.C. Improving lycopene production in Escherichia coli by engineering metabolic control. Nat. Biotechnol. 18, 533–537 (2000). 10.1038/75398

[9]

Dahl, R.H. et al. Engineering dynamic pathway regulation using stress-response promoters. Nat. Biotechnol. 31, 1039–1046 (2013). 10.1038/nbt.2689

[10]

Zhou, L.-B. & Zeng, A.-P. Exploring lysine riboswitch for metabolic flux control and improvement of L-lysine synthesis in Corynebacterium glutamicum. ACS Synth. Biol. 4, 729–734 (2015). 10.1021/sb500332c

[11]

Cardinale, S. & Arkin, A.P. Contextualizing context for synthetic biology--identifying causes of failure of synthetic biological systems. Biotechnol. J. 7, 856–866 (2012). 10.1002/biot.201200085

[12]

Van Dien, S. From the first drop to the first truckload: commercialization of microbial processes for renewable chemicals. Curr. Opin. Biotechnol. 24, 1061–1068 (2013). 10.1016/j.copbio.2013.03.002

[13]

Weber, W. & Fussenegger, M. Inducible product gene expression technology tailored to bioprocess engineering. Curr. Opin. Biotechnol. 18, 399–410 (2007). 10.1016/j.copbio.2007.09.002

[14]

Soma, Y. & Hanai, T. Self-induced metabolic state switching by a tunable cell density sensor for microbial isopropanol production. Metab. Eng. 30, 7–15 (2015). 10.1016/j.ymben.2015.04.005

[15]

Tsao, C.Y., Hooshangi, S., Wu, H.C., Valdes, J.J. & Bentley, W.E. Autonomous induction of recombinant proteins by minimally rewiring native quorum sensing regulon of E. coli. Metab. Eng. 12, 291–297 (2010). 10.1016/j.ymben.2010.01.002

[16]

Solomon, K.V., Moon, T.S., Ma, B., Sanders, T.M. & Prather, K.L.J. Tuning primary metabolism for heterologous pathway productivity. ACS Synth. Biol. 2, 126–135 (2013). 10.1021/sb300055e

[17]

Brockman, I.M. & Prather, K.L.J. Dynamic knockdown of E. coli central metabolism for redirecting fluxes of primary metabolites. Metab. Eng. 28, 104–113 (2015). 10.1016/j.ymben.2014.12.005

[18]

Juminaga, D. et al. Modular engineering of L-tyrosine production in Escherichia coli. Appl. Environ. Microbiol. 78, 89–98 (2012). 10.1128/aem.06017-11

[19]

Saeidi, N. et al. Engineering microbes to sense and eradicate Pseudomonas aeruginosa, a human pathogen. Mol. Syst. Biol. 7, 521 (2011). 10.1038/msb.2011.55

[20]

Balagaddé, F.K. et al. A synthetic Escherichia coli predator-prey ecosystem. Mol. Syst. Biol. 4, 187 (2008). 10.1038/msb.2008.24

[21]

Minogue, T.D., Wehland-von Trebra, M., Bernhard, F. & von Bodman, S.B. The autoregulatory role of EsaR, a quorum-sensing regulator in Pantoea stewartii ssp. stewartii: evidence for a repressor function. Mol. Microbiol. 44, 1625–1635 (2002). 10.1046/j.1365-2958.2002.02987.x

[22]

Mutalik, V.K. et al. Precise and reliable gene expression via standard transcription and translation initiation elements. Nat. Methods 10, 354–360 (2013). 10.1038/nmeth.2404

[23]

BioFAB. Biofab Data Access Client (BioFAB, 2012).

[24]

Hansen, C.A., Dean, A.B., Draths, K.M. & Frost, J.W. Synthesis of 1,2,3,4-Tetrahydroxybenzene from D-glucose: exploiting myo-Inositol as a precursor to aromatic chemicals. J. Am. Chem. Soc. 121, 3799–3800 (1999). 10.1021/ja9840293

[25]

Werpy, T. et al. Top value added chemicals from biomass volume I—results of screening for potential candidates from sugars and synthesis gas (US Department of Energy, Washington, DC, 2004). 10.2172/15008859

[26]

Yamaoka, M., Osawa, S., Morinaga, T., Takenaka, S. & Yoshida, K. A cell factory of Bacillus subtilis engineered for the simple bioconversion of myo-inositol to scyllo-inositol, a potential therapeutic agent for Alzheimer's disease. Microb. Cell Fact. 10, 69 (2011). 10.1186/1475-2859-10-69

[27]

Moser, F. et al. Genetic circuit performance under conditions relevant for industrial bioreactors. ACS Synth. Biol. 1, 555–564 (2012). 10.1021/sb3000832

[28]

Reizman, I.M.B. et al. Improvement of glucaric acid production in E. coli via dynamic control of metabolic fluxes. Metab. Eng. Commun. 2, 109–116 (2015). 10.1016/j.meteno.2015.09.002

[29]

Evolution-guided optimization of biosynthetic pathways

Srivatsan Raman, Jameson K. Rogers, Noah D. Taylor et al.

Proceedings of the National Academy of Sciences 2014 10.1073/pnas.1409523111

[30]

Draths, K.M., Knop, D.R. & Frost, J.W. Shikimic acid and quinic acid: replacing isolation from plant sources with recombinant microbial biocatalysis. J. Am. Chem. Soc. 121, 1603–1604 (1999). 10.1021/ja9830243

[31]

Kim, C.U. et al. Influenza neuraminidase inhibitors possessing a novel hydrophobic interaction in the enzyme active site: design, synthesis, and structural analysis of carbocyclic sialic acid analogues with potent anti-influenza activity. J. Am. Chem. Soc. 119, 681–690 (1997). 10.1021/ja963036t

[32]

Way, J.C. & Davis, J.H. Methods and molecules for yield improvement involving metabolic engineering. US Patent Application No. 13/322,383 (2010).

[33]

Chen, K. et al. Deletion of the aroK gene is essential for high shikimic acid accumulation through the shikimate pathway in E. coli. Bioresour. Technol. 119, 141–147 (2012). 10.1016/j.biortech.2012.05.100

[34]

Xu, P., Li, L., Zhang, F., Stephanopoulos, G. & Koffas, M. Improving fatty acids production by engineering dynamic pathway regulation and metabolic control. Proc. Natl. Acad. Sci. USA 111, 11299–11304 (2014). 10.1073/pnas.1406401111

[35]

Pfleger, B.F., Pitera, D.J., Newman, J.D., Martin, V.J.J. & Keasling, J.D. Microbial sensors for small molecules: development of a mevalonate biosensor. Metab. Eng. 9, 30–38 (2007). 10.1016/j.ymben.2006.08.002

[36]

Protein production by auto-induction in high-density shaking cultures

F. William Studier

Protein Expression and Purification 2005 10.1016/j.pep.2005.01.016

[37]

Wang, G. et al. Integration of microbial kinetics and fluid dynamics toward model-driven scale-up of industrial bioprocesses. Eng. Life Sci. 15, 20–29 (2015). 10.1002/elsc.201400172

[38]

Brockman, I.M. & Prather, K.L.J. Dynamic metabolic engineering: new strategies for developing responsive cell factories. Biotechnol. J. 10, 1360–1369 (2015). 10.1002/biot.201400422

[39]

Venayak, N., Anesiadis, N., Cluett, W.R. & Mahadevan, R. Engineering metabolism through dynamic control. Curr. Opin. Biotechnol. 34, 142–152 (2015). 10.1016/j.copbio.2014.12.022

[40]

McNerney, M.P., Watstein, D.M. & Styczynski, M.P. Precision metabolic engineering: the design of responsive, selective, and controllable metabolic systems. Metab. Eng. 31, 123–131 (2015). 10.1016/j.ymben.2015.06.011

[41]

Shong, J., Huang, Y.-M., Bystroff, C. & Collins, C.H. Directed evolution of the quorum-sensing regulator EsaR for increased signal sensitivity. ACS Chem. Biol. 8, 789–795 (2013). 10.1021/cb3006402

[42]

St-Pierre, F. et al. One-step cloning and chromosomal integration of DNA. ACS Synth. Biol. 2, 537–541 (2013). 10.1021/sb400021j

[43]

Site-specific chromosomal integration of large synthetic constructs

Thomas E. Kuhlman, Edward C. Cox

Nucleic Acids Research 2010 10.1093/nar/gkp1193

[44]

Shong, J. & Collins, C.H. Engineering the esaR promoter for tunable quorum sensing- dependent gene expression. ACS Synth. Biol. 2, 568–575 (2013). 10.1021/sb4000433

[45]

Construction of Escherichia coli K‐12 in‐frame, single‐gene knockout mutants: the Keio collection

Tomoya Baba, Takeshi Ara, Miki Hasegawa et al.

Molecular Systems Biology 2006 10.1038/msb4100050

[46]

Reisch, C.R. & Prather, K.L.J. The no-SCAR (Scarless Cas9 Assisted Recombineering) system for genome editing in Escherichia coli. Sci. Rep. 5, 15096 (2015). 10.1038/srep15096

[47]

Salis, H.M. The ribosome binding site calculator. Methods Enzymol. 498, 19–42 (2011). 10.1016/b978-0-12-385120-8.00002-4

Cited By

463

Shifting the detection range of cell biosensors toward high concentrations using ligand-related exporters for applications

Jiawei Li, Ziqing Qin · 2025

Trends in Biotechnology

High-level and -yield orotic acid production in Escherichia coli through systematic modular engineering and “Chaos to Order Cycles” fermentation

Changgeng Li, Tangen Shi · 2024

Bioresource Technology

Engineering quorum sensing-based genetic circuits enhances growth and productivity robustness of industrial E. coli at low pH

Xiaofang Yan, Anqi Bu · 2024

Microbial Cell Factories

Cybergenetics: Theory and Applications of Genetic Control Systems

Mustafa H. Khammash · 2022

Proceedings of the IEEE

From Microbial Communities to Distributed Computing Systems

Behzad D. Karkaria, Neythen J. Treloar · 2020

Frontiers in Bioengineering and Bio...

Engineering microbial pathways for production of bio-based chemicals from lignocellulosic sugars: current status and perspectives

Jean Marie Francois, Ceren Alkim · 2020

Biotechnology for Biofuels

Quorum Sensing System Used as a Tool in Metabolic Engineering

Chang Ge, Huakang Sheng · 2020

Biotechnology Journal

Developing a pathway-independent and full-autonomous global resource allocation strategy to dynamically switching phenotypic states

Junjun Wu, Meijiao Bao · 2020

Nature Communications

Developing an endogenous quorum-sensing based CRISPRi circuit for autonomous and tunable dynamic regulation of multiple targets in Streptomyces

Jinzhong Tian, Gaohua Yang · 2020

Nucleic Acids Research

Synthetic genetic circuits for programmable biological functionalities

Peng-Fei Xia, Hua Ling · 2019

Biotechnology Advances

Layered dynamic regulation for improving metabolic pathway productivity in Escherichia coli

Stephanie J. Doong, Apoorv Gupta · 2018

Proceedings of the National Academy...

Sensor-regulator and RNAi based bifunctional dynamic control network for engineered microbial synthesis

Yaping Yang, Yuheng Lin · 2018

Nature Communications

Metrics

463

Citations

47

References

Details

Published: Feb 13, 2017
Vol/Issue: 35(3)
Pages: 273-279
License: View

Authors

A

Apoorv Gupta

I

Irene M Brockman Reizman

Cite This Article

Apoorv Gupta, Irene M Brockman Reizman, Christopher R Reisch, et al. (2017). Dynamic regulation of metabolic flux in engineered bacteria using a pathway-independent quorum-sensing circuit. Nature Biotechnology, 35(3), 273-279. https://doi.org/10.1038/nbt.3796

Dynamic regulation of metabolic flux in engineered bacteria using a pathway-independent quorum-sensing circuit

You May Also Like