The bright frontiers of microbial metabolic optogenetics

Wegner, Scott A.; Barocio-Galindo, Rachel M.; Avalos, José L.

doi:10.1016/j.cbpa.2022.102207

The bright frontiers of microbial metabolic optogenetics

Journal Article · Sun Sep 11 00:00:00 EDT 2022 · Current Opinion in Chemical Biology

DOI:https://doi.org/10.1016/j.cbpa.2022.102207· OSTI ID:1900138

Wegner, Scott A. ^[1]; Barocio-Galindo, Rachel M. ^[2]; ^[2]

Princeton Univ., NJ (United States); Princeton University
Princeton Univ., NJ (United States)

In recent years, light-responsive systems from the field of optogenetics have been applied to several areas of metabolic engineering with remarkable success. By taking advantage of light's high tunability, reversibility, and orthogonality to host endogenous processes, optogenetic systems have enabled unprecedented dynamical controls of microbial fermentations for chemical production, metabolic flux analysis, and population compositions in co-cultures. In this article, we share our opinions on the current state of this new field of metabolic optogenetics. Furthermore, we make the case that it will continue to impact metabolic engineering in increasingly new directions, with the potential to challenge existing paradigms for metabolic pathway and strain optimization as well as bioreactor operation.

View Accepted Manuscript (DOE)

Research Organization:: Princeton Univ., NJ (United States)

Sponsoring Organization:: National Institutes of Health; USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: SC0019363; SC0022155

OSTI ID:: 1900138

Alternate ID(s):: OSTI ID: 1962168

Journal Information:: Current Opinion in Chemical Biology, Journal Name: Current Opinion in Chemical Biology Vol. 71; ISSN 1367-5931

Publisher:: ElsevierCopyright Statement

Country of Publication:: United States

Language:: English

References (63)

Synthetic Biological Approaches for Optogenetics and Tools for Transcriptional Light‐Control in Bacteria Baumschlager, Armin; Khammash, Mustafa Advanced Biology, Vol. 5, Issue 5 https://doi.org/10.1002/adbi.202000256	journal	February 2021
Synthetic Biology Driven Biosynthesis of Unnatural Tropolone Sesquiterpenoids Schotte, Carsten; Li, Lei; Wibberg, Daniel Angewandte Chemie International Edition, Vol. 59, Issue 52 https://doi.org/10.1002/anie.202009914	journal	October 2020
Effect of precise control of flux ratio between the glycolytic pathways on mevalonate production in Escherichia coli Kamata, Kentaro; Toya, Yoshihiro; Shimizu, Hiroshi Biotechnology and Bioengineering, Vol. 116, Issue 5 https://doi.org/10.1002/bit.26923	journal	February 2019
Light‐inducible flux control of triosephosphate isomerase on glycolysis in Escherichia coli Senoo, Sachie; Tandar, Sebastian Tommi; Kitamura, Sayaka Biotechnology and Bioengineering, Vol. 116, Issue 12 https://doi.org/10.1002/bit.27148	journal	September 2019
A yeast optogenetic toolkit (yOTK) for gene expression control in Saccharomyces cerevisiae An‐adirekkun, Jidapas (My); Stewart, Cameron J.; Geller, Stephanie H. Biotechnology and Bioengineering, Vol. 117, Issue 3 https://doi.org/10.1002/bit.27234	journal	December 2019
A Miniaturized Escherichia coli Green Light Sensor with High Dynamic Range Ong, Nicholas T.; Tabor, Jeffrey J. ChemBioChem, Vol. 19, Issue 12 https://doi.org/10.1002/cbic.201800007	journal	March 2018
A light-controlled cell lysis system in bacteria Wang, Geyi; Lu, Xin; Zhu, Yisha Journal of Industrial Microbiology and Biotechnology, Vol. 45, Issue 6 https://doi.org/10.1007/s10295-018-2034-4	journal	June 2018
Optogenetic tools for microbial synthetic biology Chia, Natalie; Lee, Sang Yup; Tong, Yaojun Biotechnology Advances, Vol. 59 https://doi.org/10.1016/j.biotechadv.2022.107953	journal	October 2022
A bright future: optogenetics to dissect the spatiotemporal control of cell behavior Goglia, Alexander G.; Toettcher, Jared E. Current Opinion in Chemical Biology, Vol. 48 https://doi.org/10.1016/j.cbpa.2018.11.010	journal	February 2019
Multivariate modular metabolic engineering for pathway and strain optimization Biggs, Bradley Walters; De Paepe, Brecht; Santos, Christine Nicole S. Current Opinion in Biotechnology, Vol. 29 https://doi.org/10.1016/j.copbio.2014.05.005	journal	October 2014
Engineering metabolism through dynamic control Venayak, Naveen; Anesiadis, Nikolaos; Cluett, William R. Current Opinion in Biotechnology, Vol. 34 https://doi.org/10.1016/j.copbio.2014.12.022	journal	August 2015
Current and future modalities of dynamic control in metabolic engineering Lalwani, Makoto A.; Zhao, Evan M.; Avalos, José L. Current Opinion in Biotechnology, Vol. 52 https://doi.org/10.1016/j.copbio.2018.02.007	journal	August 2018
Optogenetics and biosensors set the stage for metabolic cybergenetics Carrasco-López, César; García-Echauri, Sergio A.; Kichuk, Therese Current Opinion in Biotechnology, Vol. 65 https://doi.org/10.1016/j.copbio.2020.07.012	journal	October 2020
Metabolic engineering and synthetic biology of plant natural products – A minireview Birchfield, Aaron S.; McIntosh, Cecilia A. Current Plant Biology, Vol. 24 https://doi.org/10.1016/j.cpb.2020.100163	journal	December 2020
Recent advances in metabolic engineering–integration of in silico design and experimental analysis of metabolic pathways Shimizu, Hiroshi; Toya, Yoshihiro Journal of Bioscience and Bioengineering, Vol. 132, Issue 5 https://doi.org/10.1016/j.jbiosc.2021.08.002	journal	November 2021
From Dusk till Dawn: One-Plasmid Systems for Light-Regulated Gene Expression Ohlendorf, Robert; Vidavski, Roee R.; Eldar, Avigdor Journal of Molecular Biology, Vol. 416, Issue 4 https://doi.org/10.1016/j.jmb.2012.01.001	journal	March 2012
Metabolic Burden: Cornerstones in Synthetic Biology and Metabolic Engineering Applications Wu, Gang; Yan, Qiang; Jones, J. Andrew Trends in Biotechnology, Vol. 34, Issue 8 https://doi.org/10.1016/j.tibtech.2016.02.010	journal	August 2016
Modular Metabolic Engineering for Biobased Chemical Production Lu, Hongyuan; Villada, Juan C.; Lee, Patrick K. H. Trends in Biotechnology, Vol. 37, Issue 2 https://doi.org/10.1016/j.tibtech.2018.07.003	journal	February 2019
Experimental and computational optimization of an Escherichia coli co-culture for the efficient production of flavonoids Jones, J. Andrew; Vernacchio, Victoria R.; Sinkoe, Andrew L. Metabolic Engineering, Vol. 35 https://doi.org/10.1016/j.ymben.2016.01.006	journal	May 2016
Optogenetic switch for controlling the central metabolic flux of Escherichia coli Tandar, Sebastian Tommi; Senoo, Sachie; Toya, Yoshihiro Metabolic Engineering, Vol. 55 https://doi.org/10.1016/j.ymben.2019.06.002	journal	September 2019
Design and Characterization of Rapid Optogenetic Circuits for Dynamic Control in Yeast Metabolic Engineering Zhao, Evan M.; Lalwani, Makoto A.; Lovelett, Robert J. ACS Synthetic Biology, Vol. 9, Issue 12 https://doi.org/10.1021/acssynbio.0c00305	journal	November 2020
Engineering an Optogenetic CRISPRi Platform for Improved Chemical Production Wu, Peiling; Chen, Yufen; Liu, Mingyu ACS Synthetic Biology, Vol. 10, Issue 1 https://doi.org/10.1021/acssynbio.0c00488	journal	December 2020
Optogenetic Amplification Circuits for Light-Induced Metabolic Control Zhao, Evan M.; Lalwani, Makoto A.; Chen, Jhong-Min ACS Synthetic Biology, Vol. 10, Issue 5 https://doi.org/10.1021/acssynbio.0c00642	journal	April 2021
Optogenetic Control of Microbial Consortia Populations for Chemical Production Lalwani, Makoto A.; Kawabe, Hinako; Mays, Rebecca L. ACS Synthetic Biology, Vol. 10, Issue 8 https://doi.org/10.1021/acssynbio.1c00182	journal	August 2021
The Neurospora crassa Inducible Q System Enables Simultaneous Optogenetic Amplification and Inversion in Saccharomyces cerevisiae for Bidirectional Control of Gene Expression Lalwani, Makoto A.; Zhao, Evan M.; Wegner, Scott A. ACS Synthetic Biology, Vol. 10, Issue 8 https://doi.org/10.1021/acssynbio.1c00229	journal	August 2021
Dynamic Blue Light-Inducible T7 RNA Polymerases (Opto-T7RNAPs) for Precise Spatiotemporal Gene Expression Control Baumschlager, Armin; Aoki, Stephanie K.; Khammash, Mustafa ACS Synthetic Biology, Vol. 6, Issue 11 https://doi.org/10.1021/acssynbio.7b00169	journal	October 2017
Optogenetic Control of Heterologous Metabolism in E. coli Raghavan, Adhithi R.; Salim, Kevin; Yadav, Vikramaditya G. ACS Synthetic Biology, Vol. 9, Issue 9 https://doi.org/10.1021/acssynbio.9b00454	journal	August 2020
Optogenetic regulation of engineered cellular metabolism for microbial chemical production Zhao, Evan M.; Zhang, Yanfei; Mehl, Justin Nature, Vol. 555, Issue 7698 https://doi.org/10.1038/nature26141	journal	March 2018
Distributing a metabolic pathway among a microbial consortium enhances production of natural products Zhou, Kang; Qiao, Kangjian; Edgar, Steven Nature Biotechnology, Vol. 33, Issue 4 https://doi.org/10.1038/nbt.3095	journal	January 2015
Precise, automated control of conditions for high-throughput growth of yeast and bacteria with eVOLVER Wong, Brandon G.; Mancuso, Christopher P.; Kiriakov, Szilvia Nature Biotechnology, Vol. 36, Issue 7 https://doi.org/10.1038/nbt.4151	journal	June 2018
An optogenetic gene expression system with rapid activation and deactivation kinetics Motta-Mena, Laura B.; Reade, Anna; Mallory, Michael J. Nature Chemical Biology, Vol. 10, Issue 3 https://doi.org/10.1038/nchembio.1430	journal	January 2014
Engineering RGB color vision into Escherichia coli Fernandez-Rodriguez, Jesus; Moser, Felix; Song, Miryoung Nature Chemical Biology, Vol. 13, Issue 7 https://doi.org/10.1038/nchembio.2390	journal	May 2017
Automated optogenetic feedback control for precise and robust regulation of gene expression and cell growth Milias-Argeitis, Andreas; Rullan, Marc; Aoki, Stephanie K. Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms12546	journal	August 2016
Shaping bacterial population behavior through computer-interfaced control of individual cells Chait, Remy; Ruess, Jakob; Bergmiller, Tobias Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/s41467-017-01683-1	journal	November 2017
Industrial brewing yeast engineered for the production of primary flavor determinants in hopped beer Denby, Charles M.; Li, Rachel A.; Vu, Van T. Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-03293-x	journal	March 2018
Pulsatile inputs achieve tunable attenuation of gene expression variability and graded multi-gene regulation Benzinger, Dirk; Khammash, Mustafa Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-05882-2	journal	August 2018
A genetically encoded single-wavelength sensor for imaging cytosolic and cell surface ATP Lobas, Mark A.; Tao, Rongkun; Nagai, Jun Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-08441-5	journal	February 2019
Optogenetic control of protein binding using light-switchable nanobodies Gil, Agnieszka A.; Carrasco-López, César; Zhu, Liyuan Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-17836-8	journal	August 2020
Development of light-responsive protein binding in the monobody non-immunoglobulin scaffold Carrasco-López, César; Zhao, Evan M.; Gil, Agnieszka A. Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-17837-7	journal	August 2020
A light tunable differentiation system for the creation and control of consortia in yeast Aditya, Chetan; Bertaux, François; Batt, Gregory Nature Communications, Vol. 12, Issue 1 https://doi.org/10.1038/s41467-021-26129-7	journal	October 2021
Unnatural biosynthesis by an engineered microorganism with heterologously expressed natural enzymes and an artificial metalloenzyme Huang, Jing; Liu, Zhennan; Bloomer, Brandon J. Nature Chemistry, Vol. 13, Issue 12 https://doi.org/10.1038/s41557-021-00801-3	journal	October 2021
Reconstructing organisms in silico: genome-scale models and their emerging applications Fang, Xin; Lloyd, Colton J.; Palsson, Bernhard O. Nature Reviews Microbiology, Vol. 18, Issue 12 https://doi.org/10.1038/s41579-020-00440-4	journal	September 2020
Light-based control of metabolic flux through assembly of synthetic organelles Zhao, Evan M.; Suek, Nathan; Wilson, Maxwell Z. Nature Chemical Biology, Vol. 15, Issue 6 https://doi.org/10.1038/s41589-019-0284-8	journal	May 2019
Optogenetic control of the lac operon for bacterial chemical and protein production Lalwani, Makoto A.; Ip, Samantha S.; Carrasco-López, César Nature Chemical Biology, Vol. 17, Issue 1 https://doi.org/10.1038/s41589-020-0639-1	journal	September 2020
Engineering AraC to make it responsive to light instead of arabinose Romano, Edoardo; Baumschlager, Armin; Akmeriç, Emir Bora Nature Chemical Biology, Vol. 17, Issue 7 https://doi.org/10.1038/s41589-021-00787-6	journal	April 2021
High-throughput multicolor optogenetics in microwell plates Bugaj, Lukasz J.; Lim, Wendell A. Nature Protocols, Vol. 14, Issue 7 https://doi.org/10.1038/s41596-019-0178-y	journal	June 2019
An open-hardware platform for optogenetics and photobiology Gerhardt, Karl P.; Olson, Evan J.; Castillo-Hair, Sebastian M. Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep35363	journal	November 2016
Real-time optogenetic control of intracellular protein concentration in microbial cell cultures Melendez, Justin; Patel, Michael; Oakes, Benjamin L. Integrative Biology, Vol. 6, Issue 3 https://doi.org/10.1039/c3ib40102b	journal	January 2014
Cyanobacteriochrome CcaS is the green light receptor that induces the expression of phycobilisome linker protein Hirose, Y.; Shimada, T.; Narikawa, R. Proceedings of the National Academy of Sciences, Vol. 105, Issue 28 https://doi.org/10.1073/pnas.0801826105	journal	July 2008
Genetically encoded sensors enable real-time observation of metabolite production Rogers, Jameson K.; Church, George M. Proceedings of the National Academy of Sciences, Vol. 113, Issue 9 https://doi.org/10.1073/pnas.1600375113	journal	February 2016
Development of an autonomous and bifunctional quorum-sensing circuit for metabolic flux control in engineered Escherichia coli Dinh, Christina V.; Prather, Kristala L. J. Proceedings of the National Academy of Sciences, Vol. 116, Issue 51 https://doi.org/10.1073/pnas.1911144116	journal	December 2019
PhiReX: a programmable and red light-regulated protein expression switch for yeast Hochrein, Lena; Machens, Fabian; Messerschmidt, Katrin Nucleic Acids Research, Vol. 45, Issue 15 https://doi.org/10.1093/nar/gkx610	journal	July 2017
Building a biofoundry Holowko, Maciej B.; Frow, Emma K.; Reid, Janet C. Synthetic Biology, Vol. 6, Issue 1 https://doi.org/10.1093/synbio/ysaa026	journal	December 2020
Dynamic Control of Metabolism Ni, Cynthia; Dinh, Christina V.; Prather, Kristala L. J. Annual Review of Chemical and Biomolecular Engineering, Vol. 12, Issue 1 https://doi.org/10.1146/annurev-chembioeng-091720-125738	journal	June 2021
Optogenetics Illuminates Applications in Microbial Engineering Hoffman, Shannon M.; Tang, Allison Y.; Avalos, José L. Annual Review of Chemical and Biomolecular Engineering, Vol. 13, Issue 1 https://doi.org/10.1146/annurev-chembioeng-092120-092340	journal	June 2022
Engineered microbial biosensors based on bacterial two-component systems as synthetic biotechnology platforms in bioremediation and biorefinery Ravikumar, Sambandam; Baylon, Mary Grace; Park, Si Jae Microbial Cell Factories, Vol. 16, Issue 1 https://doi.org/10.1186/s12934-017-0675-z	journal	April 2017
Engineering microbial consortia by division of labor Roell, Garrett W.; Zha, Jian; Carr, Rhiannon R. Microbial Cell Factories, Vol. 18, Issue 1 https://doi.org/10.1186/s12934-019-1083-3	journal	February 2019
Engineering metabolite-responsive transcriptional factors to sense small molecules in eukaryotes: current state and perspectives Wan, Xia; Marsafari, Monireh; Xu, Peng Microbial Cell Factories, Vol. 18, Issue 1 https://doi.org/10.1186/s12934-019-1111-3	journal	March 2019
In situ characterisation and manipulation of biological systems with Chi.Bio Steel, Harrison; Habgood, Robert; Kelly, Ciarán L. PLOS Biology, Vol. 18, Issue 7 https://doi.org/10.1371/journal.pbio.3000794	journal	July 2020
Design, Optimization and Application of Small Molecule Biosensor in Metabolic Engineering Liu, Yang; Liu, Ye; Wang, Meng Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.02012	journal	October 2017
Modular and Molecular Optimization of a LOV (Light–Oxygen–Voltage)-Based Optogenetic Switch in Yeast Romero, Andrés; Rojas, Vicente; Delgado, Verónica International Journal of Molecular Sciences, Vol. 22, Issue 16 https://doi.org/10.3390/ijms22168538	journal	August 2021
A highly responsive pyruvate sensor reveals pathway-regulatory role of the mitochondrial pyruvate carrier MPC Arce-Molina, Robinson; Cortés-Molina, Francisca; Sandoval, Pamela Y. eLife, Vol. 9 https://doi.org/10.7554/eLife.53917	journal	March 2020
A single-chain and fast-responding light-inducible Cre recombinase as a novel optogenetic switch Duplus-Bottin, Hélène; Spichty, Martin; Triqueneaux, Gérard eLife, Vol. 10 https://doi.org/10.7554/eLife.61268	journal	February 2021

Similar Records

Optogenetics Illuminates Applications in Microbial Engineering

Journal Article · Tue Mar 22 20:00:00 EDT 2022 · Annual Review of Chemical and Biomolecular Engineering · OSTI ID:1900143

Optogenetics and biosensors set the stage for metabolic cybergenetics

Journal Article · Fri Sep 11 20:00:00 EDT 2020 · Current Opinion in Biotechnology · OSTI ID:1853115

Light-Controlled Fermentations for Microbial Chemical and Protein Production

Journal Article · Mon Mar 21 20:00:00 EDT 2022 · Journal of Visualized Experiments · OSTI ID:1900140

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
60 APPLIED LIFE SCIENCES
Biosensors
Control
Cybergenetics
DBTL
Design build test learn cycle
Dynamic control of microbial fermentations
MMME
Metabolic engineering
Multivariate modular metabolic engineering
Optogenetics

The bright frontiers of microbial metabolic optogenetics

Citation Formats

References (63)

Similar Records

Related Subjects