Optogenetics and biosensors set the stage for metabolic cybergenetics

Carrasco-López, César; García-Echauri, Sergio A.; Kichuk, Therese; Avalos, José L.

doi:10.1016/j.copbio.2020.07.012

Optogenetics and biosensors set the stage for metabolic cybergenetics

Journal Article · Sat Sep 12 00:00:00 EDT 2020 · Current Opinion in Biotechnology

DOI:https://doi.org/10.1016/j.copbio.2020.07.012· OSTI ID:1853115

^[1]; García-Echauri, Sergio A. ^[2]; Kichuk, Therese ^[2]; ^[2]

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

We report cybergenetic systems use computer interfaces to enable feed-back controls over biological processes in real time. The complex and dynamic nature of cellular metabolism makes cybergenetics attractive for controlling engineered metabolic pathways in microbial fermentations. Cybergenetics would not only create new avenues of research into cellular metabolism, it would also enable unprecedented strategies for pathway optimization and bioreactor operation and automation. Implementation of metabolic cybergenetics, however, will require new capabilities from actuators, biosensors, and control algorithms. The recent application of optogenetics in metabolic engineering, the expanding role of genetically encoded biosensors in strain development, and continued progress in control algorithms for biological processes suggest that this technology will become available in the not so distant future.

View Accepted Manuscript (DOE)

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

Sponsoring Organization:: Camille Dreyfus Teacher-Scholar Award; National Science Foundation (NSF); Pew Charitable Trusts; Princeton University SEAS; USDOE; USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: SC0019363

OSTI ID:: 1853115

Alternate ID(s):: OSTI ID: 1766086

Journal Information:: Current Opinion in Biotechnology, Journal Name: Current Opinion in Biotechnology Journal Issue: C Vol. 65; ISSN 0958-1669

Publisher:: ElsevierCopyright Statement

Country of Publication:: United States

Language:: English

References (73)

Genetically Encoded Ratiometric RNA‐Based Sensors for Quantitative Imaging of Small Molecules in Living Cells Wu, Rigumula; Karunanayake Mudiyanselage, Aruni P. K. K.; Shafiei, Fatemeh Angewandte Chemie International Edition, Vol. 58, Issue 50 https://doi.org/10.1002/anie.201911799	journal	December 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 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
Cultivation, photobioreactor design and harvesting of microalgae for biodiesel production: A critical review Chen, Chun-Yen; Yeh, Kuei-Ling; Aisyah, Rifka Bioresource Technology, Vol. 102, Issue 1 https://doi.org/10.1016/j.biortech.2010.06.159	journal	January 2011
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
Spatiotemporal Control of Intracellular Phase Transitions Using Light-Activated optoDroplets Shin, Yongdae; Berry, Joel; Pannucci, Nicole Cell, Vol. 168, Issue 1-2 https://doi.org/10.1016/j.cell.2016.11.054	journal	January 2017
Real-Time Genetic Compensation Defines the Dynamic Demands of Feedback Control Harrigan, Patrick; Madhani, Hiten D.; El-Samad, Hana Cell, Vol. 175, Issue 3 https://doi.org/10.1016/j.cell.2018.09.044	journal	October 2018
Engineering a Model Cell for Rational Tuning of GPCR Signaling Shaw, William M.; Yamauchi, Hitoshi; Mead, Jack Cell, Vol. 177, Issue 3 https://doi.org/10.1016/j.cell.2019.02.023	journal	April 2019
Protein Phase Separation Provides Long-Term Memory of Transient Spatial Stimuli Dine, Elliot; Gil, Agnieszka A.; Uribe, Giselle Cell Systems, Vol. 6, Issue 6 https://doi.org/10.1016/j.cels.2018.05.002	journal	June 2018
Self-Amplifying Pulsatile Protein Dynamics without Positive Feedback Martinez-Corral, Rosa; Raimundez, Elba; Lin, Yihan Cell Systems, Vol. 7, Issue 4 https://doi.org/10.1016/j.cels.2018.08.012	journal	October 2018
A Fluorogenic RNA-Based Sensor Activated by Metabolite-Induced RNA Dimerization Kim, Hyaeyeong; Jaffrey, Samie R. Cell Chemical Biology, Vol. 26, Issue 12 https://doi.org/10.1016/j.chembiol.2019.09.013	journal	December 2019
Biosensor-based engineering of biosynthetic pathways Rogers, Jameson K.; Taylor, Noah D.; Church, George M. Current Opinion in Biotechnology, Vol. 42 https://doi.org/10.1016/j.copbio.2016.03.005	journal	December 2016
Next generation industrial biotechnology based on extremophilic bacteria Chen, Guo-Qiang; Jiang, Xiao-Ran Current Opinion in Biotechnology, Vol. 50 https://doi.org/10.1016/j.copbio.2017.11.016	journal	April 2018
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
Custom-made transcriptional biosensors for metabolic engineering Koch, Mathilde; Pandi, Amir; Borkowski, Olivier Current Opinion in Biotechnology, Vol. 59 https://doi.org/10.1016/j.copbio.2019.02.016	journal	October 2019
Transcription factor-based biosensors and inducible systems in non-model bacteria: current progress and future directions Kim, Nancy M.; Sinnott, Riley W.; Sandoval, Nicholas R. Current Opinion in Biotechnology, Vol. 64 https://doi.org/10.1016/j.copbio.2019.09.009	journal	August 2020
RNA-based fluorescent biosensors for live cell imaging of small molecules and RNAs Su, Yichi; Hammond, Ming C. Current Opinion in Biotechnology, Vol. 63 https://doi.org/10.1016/j.copbio.2020.01.001	journal	June 2020
An evaluation of genetically encoded FRET-based biosensors for quantitative metabolite analyses in vivo Moussa, Roland; Baierl, Anna; Steffen, Victoria Journal of Biotechnology, Vol. 191 https://doi.org/10.1016/j.jbiotec.2014.07.007	journal	December 2014
Multichromatic Control of Gene Expression in Escherichia coli Tabor, Jeffrey J.; Levskaya, Anselm; Voigt, Christopher A. Journal of Molecular Biology, Vol. 405, Issue 2 https://doi.org/10.1016/j.jmb.2010.10.038	journal	January 2011
An Optogenetic Platform for Real-Time, Single-Cell Interrogation of Stochastic Transcriptional Regulation Rullan, Marc; Benzinger, Dirk; Schmidt, Gregor W. Molecular Cell, Vol. 70, Issue 4 https://doi.org/10.1016/j.molcel.2018.04.012	journal	May 2018
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
Advances in optogenetic regulation of gene expression in mammalian cells using cryptochrome 2 (CRY2) Hernández-Candia, Carmen N.; Wysoczynski, Christina L.; Tucker, Chandra L. Methods, Vol. 164-165 https://doi.org/10.1016/j.ymeth.2019.03.011	journal	July 2019
Partial Observations and Conservation Laws: Gray-Box Modeling in Biotechnology and Optogenetics Lovelett, Robert J.; Avalos, José L.; Kevrekidis, Ioannis G. Industrial & Engineering Chemistry Research, Vol. 59, Issue 6 https://doi.org/10.1021/acs.iecr.9b04507	journal	November 2019
In Vivo Real-Time Control of Gene Expression: A Comparative Analysis of Feedback Control Strategies in Yeast Fiore, Gianfranco; Perrino, Giansimone; di Bernardo, Mario ACS Synthetic Biology, Vol. 5, Issue 2 https://doi.org/10.1021/acssynbio.5b00135	journal	December 2015
Development of Transcription Factor-Based Designer Macrolide Biosensors for Metabolic Engineering and Synthetic Biology Kasey, Christian M.; Zerrad, Mounir; Li, Yiwei ACS Synthetic Biology, Vol. 7, Issue 1 https://doi.org/10.1021/acssynbio.7b00287	journal	August 2017
An Orthogonal and pH-Tunable Sensor-Selector for Muconic Acid Biosynthesis in Yeast Snoek, Tim; Romero-Suarez, David; Zhang, Jie ACS Synthetic Biology, Vol. 7, Issue 4 https://doi.org/10.1021/acssynbio.7b00439	journal	April 2018
Regulation of Gene Expression and Signaling Pathway Activity in Mammalian Cells by Automated Microfluidics Feedback Control Postiglione, Lorena; Napolitano, Sara; Pedone, Elisa ACS Synthetic Biology, Vol. 7, Issue 11 https://doi.org/10.1021/acssynbio.8b00235	journal	October 2018
A Regulatory NADH/NAD+ Redox Biosensor for Bacteria Liu, Yang; Landick, Robert; Raman, Srivatsan ACS Synthetic Biology, Vol. 8, Issue 2 https://doi.org/10.1021/acssynbio.8b00485	journal	January 2019
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
In silico feedback for in vivo regulation of a gene expression circuit Milias-Argeitis, Andreas; Summers, Sean; Stewart-Ornstein, Jacob Nature Biotechnology, Vol. 29, Issue 12 https://doi.org/10.1038/nbt.2018	journal	November 2011
Design of a dynamic sensor-regulator system for production of chemicals and fuels derived from fatty acids Zhang, Fuzhong; Carothers, James M.; Keasling, Jay D. Nature Biotechnology, Vol. 30, Issue 4 https://doi.org/10.1038/nbt.2149	journal	March 2012
FRET imaging Jares-Erijman, Elizabeth A.; Jovin, Thomas M. Nature Biotechnology, Vol. 21, Issue 11 https://doi.org/10.1038/nbt896	journal	October 2003
Engineering prokaryotic transcriptional activators as metabolite biosensors in yeast Skjoedt, Mette L.; Snoek, Tim; Kildegaard, Kanchana R. Nature Chemical Biology, Vol. 12, Issue 11 https://doi.org/10.1038/nchembio.2177	journal	September 2016
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
Ultraviolet-B-mediated induction of protein–protein interactions in mammalian cells Crefcoeur, Remco P.; Yin, Ruohe; Ulm, Roman Nature Communications, Vol. 4, Issue 1 https://doi.org/10.1038/ncomms2800	journal	April 2013
Light-based feedback for controlling intracellular signaling dynamics Toettcher, Jared E.; Gong, Delquin; Lim, Wendell A. Nature Methods, Vol. 8, Issue 10 https://doi.org/10.1038/nmeth.1700	journal	September 2011
Near-infrared light–controlled systems for gene transcription regulation, protein targeting and spectral multiplexing Redchuk, Taras A.; Kaberniuk, Andrii A.; Verkhusha, Vladislav V. Nature Protocols, Vol. 13, Issue 5 https://doi.org/10.1038/nprot.2018.022	journal	April 2018
RNA-aptamers-in-droplets (RAPID) high-throughput screening for secretory phenotypes Abatemarco, Joseph; Sarhan, Maen F.; Wagner, James M. Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/s41467-017-00425-7	journal	August 2017
Balancing a genetic toggle switch by real-time feedback control and periodic forcing Lugagne, Jean-Baptiste; Sosa Carrillo, Sebastián; Kirch, Melanie Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/s41467-017-01498-0	journal	November 2017
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
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
Optogenetic control of mRNA localization and translation in live cells Kim, Na Yeon; Lee, Sangkyu; Yu, Jeonghye Nature Cell Biology, Vol. 22, Issue 3 https://doi.org/10.1038/s41556-020-0468-1	journal	February 2020
A universal biomolecular integral feedback controller for robust perfect adaptation Aoki, Stephanie K.; Lillacci, Gabriele; Gupta, Ankit Nature, Vol. 570, Issue 7762 https://doi.org/10.1038/s41586-019-1321-1	journal	June 2019
Modular and tunable biological feedback control using a de novo protein switch Ng, Andrew H.; Nguyen, Taylor H.; Gómez-Schiavon, Mariana Nature, Vol. 572, Issue 7768 https://doi.org/10.1038/s41586-019-1425-7	journal	July 2019
De novo design of bioactive protein switches Langan, Robert A.; Boyken, Scott E.; Ng, Andrew H. Nature, Vol. 572, Issue 7768 https://doi.org/10.1038/s41586-019-1432-8	journal	July 2019
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
A blue light receptor that mediates RNA binding and translational regulation Weber, Anna M.; Kaiser, Jennifer; Ziegler, Thea Nature Chemical Biology, Vol. 15, Issue 11 https://doi.org/10.1038/s41589-019-0346-y	journal	August 2019
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
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
Long-term model predictive control of gene expression at the population and single-cell levels Uhlendorf, J.; Miermont, A.; Delaveau, T. Proceedings of the National Academy of Sciences, Vol. 109, Issue 35 https://doi.org/10.1073/pnas.1206810109	journal	August 2012
G _S Activation Is Time-limiting in Initiating Receptor-mediated Signaling Hein, Peter; Rochais, Francesca; Hoffmann, Carsten Journal of Biological Chemistry, Vol. 281, Issue 44 https://doi.org/10.1074/jbc.M606713200	journal	September 2006
Multi-chromatic control of mammalian gene expression and signaling Müller, Konrad; Engesser, Raphael; Schulz, Simon Nucleic Acids Research, Vol. 41, Issue 12 https://doi.org/10.1093/nar/gkt340	journal	April 2013
Synthetic biosensors for precise gene control and real-time monitoring of metabolites Rogers, Jameson K.; Guzman, Christopher D.; Taylor, Noah D. Nucleic Acids Research, Vol. 43, Issue 15 https://doi.org/10.1093/nar/gkv616	journal	July 2015
Synthetic control systems for high performance gene expression in mammalian cells Lillacci, Gabriele; Benenson, Yaakov; Khammash, Mustafa Nucleic Acids Research, Vol. 46, Issue 18 https://doi.org/10.1093/nar/gky795	journal	September 2018
Next-level riboswitch development—implementation of Capture-SELEX facilitates identification of a new synthetic riboswitch Boussebayle, Adrien; Torka, Daniel; Ollivaud, Sandra Nucleic Acids Research, Vol. 47, Issue 9 https://doi.org/10.1093/nar/gkz216	journal	April 2019
Evolution-guided engineering of small-molecule biosensors Snoek, Tim; Chaberski, Evan K.; Ambri, Francesca Nucleic Acids Research, Vol. 48, Issue 1 https://doi.org/10.1093/nar/gkz954	journal	November 2019
Programmable protein circuits in living cells Gao, Xiaojing J.; Chong, Lucy S.; Kim, Matthew S. Science, Vol. 361, Issue 6408 https://doi.org/10.1126/science.aat5062	journal	September 2018
At Light Speed: Advances in Optogenetic Systems for Regulating Cell Signaling and Behavior Repina, Nicole A.; Rosenbloom, Alyssa; Mukherjee, Abhirup Annual Review of Chemical and Biomolecular Engineering, Vol. 8, Issue 1 https://doi.org/10.1146/annurev-chembioeng-060816-101254	journal	June 2017
Optogenetic regulation of transcription Polesskaya, Oksana; Baranova, Ancha; Bui, Sarah BMC Neuroscience, Vol. 19, Issue S1 https://doi.org/10.1186/s12868-018-0411-6	journal	April 2018
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
Principles and applications of optogenetics in developmental biology Krueger, Daniel; Izquierdo, Emiliano; Viswanathan, Ranjith Development, Vol. 146, Issue 20 https://doi.org/10.1242/dev.175067	journal	October 2019
Two Decades of Genetically Encoded Biosensors Based on Förster Resonance Energy Transfer Terai, Kenta; Imanishi, Ayako; Li, Chunjie Cell Structure and Function, Vol. 44, Issue 2 https://doi.org/10.1247/csf.18035	journal	January 2019
In-Vivo Real-Time Control of Protein Expression from Endogenous and Synthetic Gene Networks Menolascina, Filippo; Fiore, Gianfranco; Orabona, Emanuele PLoS Computational Biology, Vol. 10, Issue 5 https://doi.org/10.1371/journal.pcbi.1003625	journal	May 2014
A novel optogenetically tunable frequency modulating oscillator Mahajan, Tarun; Rai, Kshitij PLOS ONE, Vol. 13, Issue 2 https://doi.org/10.1371/journal.pone.0183242	journal	February 2018
Dynamic control of endogenous metabolism with combinatorial logic circuits Moser, Felix; Espah Borujeni, Amin; Ghodasara, Amar N. Molecular Systems Biology, Vol. 14, Issue 11 https://doi.org/10.15252/msb.20188605	journal	November 2018
Programming Escherichia coli to function as a digital display Shin, Jonghyeon; Zhang, Shuyi; Der, Bryan S. Molecular Systems Biology, Vol. 16, Issue 3 https://doi.org/10.15252/msb.20199401	journal	March 2020
Conversion of Cytochrome P450 2D6 of Human Into a FRET-Based Tool for Real-Time Monitoring of Ajmalicine in Living Cells Ambrin, Ghazala; Ahmad, Mohammad; Alqarawi, Abdulaziz A. Frontiers in Bioengineering and Biotechnology, Vol. 7 https://doi.org/10.3389/fbioe.2019.00375	journal	November 2019
Bringing Light to Transcription: The Optogenetics Repertoire de Mena, Lorena; Rizk, Patrick; Rincon-Limas, Diego E. Frontiers in Genetics, Vol. 9 https://doi.org/10.3389/fgene.2018.00518	journal	November 2018
A general strategy to construct small molecule biosensors in eukaryotes Feng, Justin; Jester, Benjamin W.; Tinberg, Christine E. eLife, Vol. 4 https://doi.org/10.7554/eLife.10606	journal	December 2015
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

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