Redox-enabled electronic interrogation and feedback control of hierarchical and networked biological systems
Abstract
Abstract Microelectronic devices can directly communicate with biology, as electronic information can be transmitted via redox reactions within biological systems. By engineering biology’s native redox networks, we enable electronic interrogation and control of biological systems at several hierarchical levels: proteins, cells, and cell consortia. First, electro-biofabrication facilitates on-device biological component assembly. Then, electrode-actuated redox data transmission and redox-linked synthetic biology allows programming of enzyme activity and closed-loop electrogenetic control of cellular function. Specifically, horseradish peroxidase is assembled onto interdigitated electrodes where electrode-generated hydrogen peroxide controls its activity. E. coli ’s stress response regulon, oxyRS , is rewired to enable algorithm-based feedback control of gene expression, including an eCRISPR module that switches cell-cell quorum sensing communication from one autoinducer to another—creating an electronically controlled ‘bilingual’ cell. Then, these disparate redox-guided devices are wirelessly connected, enabling real-time communication and user-based control. We suggest these methodologies will help us to better understand and develop sophisticated control for biology.
- Publication Date:
- Sponsoring Org.:
- USDOE
- OSTI Identifier:
- 2248105
- Grant/Contract Number:
- BER#SCW1710
- Resource Type:
- Published Article
- Journal Name:
- Nature Communications
- Additional Journal Information:
- Journal Name: Nature Communications Journal Volume: 14 Journal Issue: 1; Journal ID: ISSN 2041-1723
- Publisher:
- Nature Publishing Group
- Country of Publication:
- United Kingdom
- Language:
- English
Citation Formats
Wang, Sally, Chen, Chen-Yu, Rzasa, John R., Tsao, Chen-Yu, Li, Jinyang, VanArsdale, Eric, Kim, Eunkyoung, Zakaria, Fauziah Rahma, Payne, Gregory F., and Bentley, William E. Redox-enabled electronic interrogation and feedback control of hierarchical and networked biological systems. United Kingdom: N. p., 2023.
Web. doi:10.1038/s41467-023-44223-w.
Wang, Sally, Chen, Chen-Yu, Rzasa, John R., Tsao, Chen-Yu, Li, Jinyang, VanArsdale, Eric, Kim, Eunkyoung, Zakaria, Fauziah Rahma, Payne, Gregory F., & Bentley, William E. Redox-enabled electronic interrogation and feedback control of hierarchical and networked biological systems. United Kingdom. https://doi.org/10.1038/s41467-023-44223-w
Wang, Sally, Chen, Chen-Yu, Rzasa, John R., Tsao, Chen-Yu, Li, Jinyang, VanArsdale, Eric, Kim, Eunkyoung, Zakaria, Fauziah Rahma, Payne, Gregory F., and Bentley, William E. Thu .
"Redox-enabled electronic interrogation and feedback control of hierarchical and networked biological systems". United Kingdom. https://doi.org/10.1038/s41467-023-44223-w.
@article{osti_2248105,
title = {Redox-enabled electronic interrogation and feedback control of hierarchical and networked biological systems},
author = {Wang, Sally and Chen, Chen-Yu and Rzasa, John R. and Tsao, Chen-Yu and Li, Jinyang and VanArsdale, Eric and Kim, Eunkyoung and Zakaria, Fauziah Rahma and Payne, Gregory F. and Bentley, William E.},
abstractNote = {Abstract Microelectronic devices can directly communicate with biology, as electronic information can be transmitted via redox reactions within biological systems. By engineering biology’s native redox networks, we enable electronic interrogation and control of biological systems at several hierarchical levels: proteins, cells, and cell consortia. First, electro-biofabrication facilitates on-device biological component assembly. Then, electrode-actuated redox data transmission and redox-linked synthetic biology allows programming of enzyme activity and closed-loop electrogenetic control of cellular function. Specifically, horseradish peroxidase is assembled onto interdigitated electrodes where electrode-generated hydrogen peroxide controls its activity. E. coli ’s stress response regulon, oxyRS , is rewired to enable algorithm-based feedback control of gene expression, including an eCRISPR module that switches cell-cell quorum sensing communication from one autoinducer to another—creating an electronically controlled ‘bilingual’ cell. Then, these disparate redox-guided devices are wirelessly connected, enabling real-time communication and user-based control. We suggest these methodologies will help us to better understand and develop sophisticated control for biology.},
doi = {10.1038/s41467-023-44223-w},
journal = {Nature Communications},
number = 1,
volume = 14,
place = {United Kingdom},
year = {Thu Dec 21 00:00:00 EST 2023},
month = {Thu Dec 21 00:00:00 EST 2023}
}
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1038/s41467-023-44223-w
https://doi.org/10.1038/s41467-023-44223-w
Other availability
Search WorldCat to find libraries that may hold this journal
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.
Works referenced in this record:
Connecting Biology to Electronics: Molecular Communication via Redox Modality
journal, October 2017
- Liu, Yi; Li, Jinyang; Tschirhart, Tanya
- Advanced Healthcare Materials, Vol. 6, Issue 24
Simple, rapidly electroassembled thiolated PEG‐based sensor interfaces enable rapid interrogation of antibody titer and glycosylation
journal, May 2021
- Motabar, Dana; Li, Jinyang; Wang, Sally
- Biotechnology and Bioengineering, Vol. 118, Issue 7
Cyclic AMP (cAMP) and cAMP Receptor Protein Influence both Synthesis and Uptake of Extracellular Autoinducer 2 in
Escherichia coli
journal, March 2005
- Wang, Liang; Hashimoto, Yoshifumi; Tsao, Chen-Yu
- Journal of Bacteriology, Vol. 187, Issue 6
Modular one-pot assembly of CRISPR arrays enables library generation and reveals factors influencing crRNA biogenesis
journal, July 2019
- Liao, Chunyu; Ttofali, Fani; Slotkowski, Rebecca A.
- Nature Communications, Vol. 10, Issue 1
Redox Electrochemistry to Interrogate and Control Biomolecular Communication
journal, September 2020
- VanArsdale, Eric; Pitzer, Juliana; Payne, Gregory F.
- iScience, Vol. 23, Issue 9
Electrogenetic cellular insulin release for real-time glycemic control in type 1 diabetic mice
journal, May 2020
- Krawczyk, Krzysztof; Xue, Shuai; Buchmann, Peter
- Science, Vol. 368, Issue 6494
T Cell-Derived Protein S Engages TAM Receptor Signaling in Dendritic Cells to Control the Magnitude of the Immune Response
journal, July 2013
- Carrera Silva, Eugenio A.; Chan, Pamela Y.; Joannas, Leonel
- Immunity, Vol. 39, Issue 1
Electronic signals are electrogenetically relayed to control cell growth and co-culture composition
journal, December 2021
- Stephens, Kristina; Zakaria, Fauziah Rahma; VanArsdale, Eric
- Metabolic Engineering Communications, Vol. 13
Nanomaterial-based biohybrid hydrogel in bioelectronics
journal, February 2023
- Shin, Minkyu; Lim, Joungpyo; An, Joohyun
- Nano Convergence, Vol. 10, Issue 1
A Coculture Based Tyrosine-Tyrosinase Electrochemical Gene Circuit for Connecting Cellular Communication with Electronic Networks
journal, March 2020
- VanArsdale, Eric; Hörnström, David; Sjöberg, Gustav
- ACS Synthetic Biology, Vol. 9, Issue 5
Real-time bioelectronic sensing of environmental contaminants
journal, November 2022
- Atkinson, Joshua T.; Su, Lin; Zhang, Xu
- Nature, Vol. 611, Issue 7936
The gut microbiota–brain axis in behaviour and brain disorders
journal, October 2020
- Morais, Livia H.; Schreiber, Henry L.; Mazmanian, Sarkis K.
- Nature Reviews Microbiology, Vol. 19, Issue 4
Oligosaccharide microarrays for high-throughput detection and specificity assignments of carbohydrate-protein interactions
journal, September 2002
- Fukui, Shigeyuki; Feizi, Ten; Galustian, Christine
- Nature Biotechnology, Vol. 20, Issue 10
An electrogenetic interface to program mammalian gene expression by direct current
journal, July 2023
- Huang, Jinbo; Xue, Shuai; Buchmann, Peter
- Nature Metabolism, Vol. 5, Issue 8
The internet of Bio-Nano things
journal, March 2015
- Akyildiz, I.; Pierobon, M.; Balasubramaniam, S.
- IEEE Communications Magazine, Vol. 53, Issue 3
Transient Electronics: Materials and Devices
journal, May 2016
- Fu, Kun Kelvin; Wang, Zhengyang; Dai, Jiaqi
- Chemistry of Materials, Vol. 28, Issue 11
Towards area‐based in vitro metabolic engineering: Assembly of Pfs enzyme onto patterned microfabricated chips
journal, September 2008
- Lewandowski, Angela T.; Bentley, William E.; Yi, Hyunmin
- Biotechnology Progress, Vol. 24, Issue 5
Electrochemical detection of nucleic acids, proteins, small molecules and cells using a DNA-nanostructure-based universal biosensing platform
journal, June 2016
- Lin, Meihua; Song, Ping; Zhou, Guobao
- Nature Protocols, Vol. 11, Issue 7
Metabolic Burden: Cornerstones in Synthetic Biology and Metabolic Engineering Applications
journal, August 2016
- Wu, Gang; Yan, Qiang; Jones, J. Andrew
- Trends in Biotechnology, Vol. 34, Issue 8
Programmable repression and activation of bacterial gene expression using an engineered CRISPR-Cas system
journal, June 2013
- Bikard, David; Jiang, Wenyan; Samai, Poulami
- Nucleic Acids Research, Vol. 41, Issue 15
Automated optogenetic feedback control for precise and robust regulation of gene expression and cell growth
journal, August 2016
- Milias-Argeitis, Andreas; Rullan, Marc; Aoki, Stephanie K.
- Nature Communications, Vol. 7, Issue 1
Bioactuators based on stimulus-responsive hydrogels and their emerging biomedical applications
journal, November 2019
- Shi, Qiang; Liu, Hao; Tang, Deding
- NPG Asia Materials, Vol. 11, Issue 1
Biofilms as Complex Differentiated Communities
journal, October 2002
- Stoodley, P.; Sauer, K.; Davies, D. G.
- Annual Review of Microbiology, Vol. 56, Issue 1
Genetically targeted magnetic control of the nervous system
journal, March 2016
- Wheeler, Michael A.; Smith, Cody J.; Ottolini, Matteo
- Nature Neuroscience, Vol. 19, Issue 5
Quorum Sensing Communication: Molecularly Connecting Cells, Their Neighbors, and Even Devices
journal, June 2020
- Wang, Sally; Payne, Gregory F.; Bentley, William E.
- Annual Review of Chemical and Biomolecular Engineering, Vol. 11, Issue 1
Electronic modulation of biochemical signal generation
journal, July 2014
- Gordonov, Tanya; Kim, Eunkyoung; Cheng, Yi
- Nature Nanotechnology, Vol. 9, Issue 8
Hydrogen peroxide‐producing electrochemical bandage controlled by a wearable potentiostat for treatment of wound infections
journal, May 2021
- Mohamed, Abdelrhman; Anoy, MD Monzurul Islam; Tibbits, Gretchen
- Biotechnology and Bioengineering, Vol. 118, Issue 7
Sensing the future of bio-informational engineering
journal, January 2021
- Dixon, Thomas A.; Williams, Thomas C.; Pretorius, Isak S.
- Nature Communications, Vol. 12, Issue 1
Bioelectronic control of a microbial community using surface-assembled electrogenetic cells to route signals
journal, March 2021
- Terrell, Jessica L.; Tschirhart, Tanya; Jahnke, Justin P.
- Nature Nanotechnology, Vol. 16, Issue 6
Electrochemical scaffold generates localized, low concentration of hydrogen peroxide that inhibits bacterial pathogens and biofilms
journal, October 2015
- Sultana, Sujala T.; Atci, Erhan; Babauta, Jerome T.
- Scientific Reports, Vol. 5, Issue 1
Smart-watch-programmed green-light-operated percutaneous control of therapeutic transgenes
journal, June 2021
- Mansouri, Maysam; Hussherr, Marie-Didiée; Strittmatter, Tobias
- Nature Communications, Vol. 12, Issue 1
Understanding and engineering electrochemically active bacteria for sustainable biotechnology
journal, March 2019
- Hirose, Atsumi; Kasai, Takuya; Koga, Ryota
- Bioresources and Bioprocessing, Vol. 6, Issue 1
Engineering bacterial motility towards hydrogen-peroxide
journal, May 2018
- Virgile, Chelsea; Hauk, Pricila; Wu, Hsuan-Chen
- PLOS ONE, Vol. 13, Issue 5
Chapter 33 Performing and Optimizing Western Blots with an Emphasis on Chemiluminescent Detection
book, November 2009
- Alegria-Schaffer, Alice; Lodge, Andrew; Vattem, Krishna
- Methods in Enzymology
Enzyme-based ultrasensitive electrochemical biosensors
journal, August 2012
- Yang, Haesik
- Current Opinion in Chemical Biology, Vol. 16, Issue 3-4
A ‘bioproduction breadboard’: programming, assembling, and actuating cellular networks
journal, December 2015
- Zargar, Amin; Payne, Gregory F.; Bentley, William E.
- Current Opinion in Biotechnology, Vol. 36
Multiplexed CRISPR technologies for gene editing and transcriptional regulation
journal, March 2020
- McCarty, Nicholas S.; Graham, Alicia E.; Studená, Lucie
- Nature Communications, Vol. 11, Issue 1
Non-lethal exposure to H2O2 boosts bacterial survival and evolvability against oxidative stress
journal, March 2020
- Rodríguez-Rojas, Alexandro; Kim, Joshua Jay; Johnston, Paul R.
- PLOS Genetics, Vol. 16, Issue 3
Redox Is a Global Biodevice Information Processing Modality
journal, July 2019
- Kim, Eunkyoung; Li, Jinyang; Kang, Mijeong
- Proceedings of the IEEE, Vol. 107, Issue 7
Electrogenetic Signal Transmission and Propagation in Coculture to Guide Production of a Small Molecule, Tyrosine
journal, February 2022
- VanArsdale, Eric; Pitzer, Juliana; Wang, Sally
- ACS Synthetic Biology, Vol. 11, Issue 2
Interactive Materials for Bidirectional Redox‐Based Communication
journal, March 2021
- Li, Jinyang; Wang, Sally P.; Zong, Guanghui
- Advanced Materials, Vol. 33, Issue 18
Transcription Factors That Defend Bacteria Against Reactive Oxygen Species
journal, October 2015
- Imlay, James A.
- Annual Review of Microbiology, Vol. 69, Issue 1
A redox-based electrogenetic CRISPR system to connect with and control biological information networks
journal, May 2020
- Bhokisham, Narendranath; VanArsdale, Eric; Stephens, Kristina T.
- Nature Communications, Vol. 11, Issue 1
Electronic control of gene expression and cell behaviour in Escherichia coli through redox signalling
journal, January 2017
- Tschirhart, Tanya; Kim, Eunkyoung; McKay, Ryan
- Nature Communications, Vol. 8, Issue 1
Generic model control of induced protein expression in high cell density cultivation of Escherichia coli using on-line GFP-fusion monitoring
journal, July 2001
- DeLisa, M.; Chae, H.; Weigand, W.
- Bioprocess and Biosystems Engineering, Vol. 24, Issue 2
Macroscale Biomolecular Electronics and Ionics
journal, September 2018
- Amdursky, Nadav; Głowacki, Eric Daniel; Meredith, Paul
- Advanced Materials, Vol. 31, Issue 3
Flexible Electrochemical Bioelectronics: The Rise of In Situ Bioanalysis
journal, August 2019
- Yu, You; Nyein, Hnin Yin Yin; Gao, Wei
- Advanced Materials, Vol. 32, Issue 15
Parsed synthesis of pyocyanin via co-culture enables context-dependent intercellular redox communication
journal, November 2021
- Chun, Kayla; Stephens, Kristina; Wang, Sally
- Microbial Cell Factories, Vol. 20, Issue 1
Electrogenetic signaling and information propagation for controlling microbial consortia via programmed lysis
journal, February 2023
- VanArsdale, Eric; Navid, Ali; Chu, Monica J.
- Biotechnology and Bioengineering, Vol. 120, Issue 5
Enhancement of recombinant protein synthesis and stability via coordinated amino acid addition
journal, March 1993
- Ramérez, Delia M.; Bentley, William E.
- Biotechnology and Bioengineering, Vol. 41, Issue 5
Quorum sensing in
Escherichia coli
,
Salmonella typhimurium
, and
Vibrio harveyi
: A new family of genes responsible for autoinducer production
journal, February 1999
- Surette, Michael G.; Miller, Melissa B.; Bassler, Bonnie L.
- Proceedings of the National Academy of Sciences, Vol. 96, Issue 4
Towards smart biomanufacturing: a perspective on recent developments in industrial measurement and monitoring technologies for bio-based production processes
journal, November 2020
- Gargalo, Carina L.; Udugama, Isuru; Pontius, Katrin
- Journal of Industrial Microbiology and Biotechnology, Vol. 47, Issue 11
A multiplexed, electrochemical interface for gene-circuit-based sensors
journal, November 2019
- Sadat Mousavi, Peivand; Smith, Sarah J.; Chen, Jenise B.
- Nature Chemistry, Vol. 12, Issue 1
Chip modularity enables molecular information access from organ-on-chip devices with quality control
journal, September 2019
- Shang, Wu; Chen, Chen-Yu; Lo, Kimberly
- Sensors and Actuators B: Chemical, Vol. 295
A Synthetic Genetic Edge Detection Program
journal, June 2009
- Tabor, Jeffrey J.; Salis, Howard M.; Simpson, Zachary Booth
- Cell, Vol. 137, Issue 7
Biofabrication with Chitosan
journal, September 2005
- Yi, Hyunmin; Wu, Li-Qun; Bentley, William E.
- Biomacromolecules, Vol. 6, Issue 6
Effect of sdiA on Biosensors of N -Acylhomoserine Lactones
journal, July 2005
- Lindsay, Amber; Ahmer, Brian M. M.
- Journal of Bacteriology, Vol. 187, Issue 14
Harnessing microbial multitrophic interactions for rhizosphere microbiome engineering
journal, December 2022
- Afridi, Muhammad Siddique; Fakhar, Ali; Kumar, Ashwani
- Microbiological Research, Vol. 265
Engineering Wired Life: Synthetic Biology for Electroactive Bacteria
journal, October 2021
- Bird, Lina J.; Kundu, Biki B.; Tschirhart, Tanya
- ACS Synthetic Biology, Vol. 10, Issue 11
Electro-Biofabrication. Coupling Electrochemical and Biomolecular Methods to Create Functional Bio-Based Hydrogels
journal, May 2023
- Liu, Yi; Kim, Eunkyoung; Lei, Miao
- Biomacromolecules, Vol. 24, Issue 6
Selective assembly and functionalization of miniaturized redox capacitor inside microdevices for microbial toxin and mammalian cell cytotoxicity analyses
journal, January 2018
- Shang, Wu; Liu, Yi; Kim, Eunkyoung
- Lab on a Chip, Vol. 18, Issue 23
Lipid raft microdomains and neurotransmitter signalling
journal, December 2006
- Allen, John A.; Halverson-Tamboli, Robyn A.; Rasenick, Mark M.
- Nature Reviews Neuroscience, Vol. 8, Issue 2
The microbiome and gut homeostasis
journal, July 2022
- Lee, Jee-Yon; Tsolis, Renée M.; Bäumler, Andreas J.
- Science, Vol. 377, Issue 6601
Toll-like receptor signalling
journal, July 2004
- Akira, Shizuo; Takeda, Kiyoshi
- Nature Reviews Immunology, Vol. 4, Issue 7
Mediated Electrochemistry to Mimic Biology's Oxidative Assembly of Functional Matrices
journal, June 2020
- Li, Jinyang; Kim, Eunkyoung; Gray, Kelsey M.
- Advanced Functional Materials, Vol. 30, Issue 30
Synthetic biology and bioelectrochemical tools for electrogenetic system engineering
journal, May 2022
- Lawrence, Joshua M.; Yin, Yutong; Bombelli, Paolo
- Science Advances, Vol. 8, Issue 18
Plasmid-encoded protein: The principal factor in the “metabolic burden” associated with recombinant bacteria
journal, March 1990
- Bentley, William E.; Mirjalili, Noushin; Andersen, Dana C.
- Biotechnology and Bioengineering, Vol. 35, Issue 7
Mediated electrochemistry for redox-based biological targeting: entangling sensing and actuation for maximizing information transfer
journal, October 2021
- Motabar, Dana; Li, Jinyang; Payne, Gregory F.
- Current Opinion in Biotechnology, Vol. 71
Feedback Control of Tryptophan Biosynthesis
journal, March 1960
- Doy, C. H.; Pittard, A. J.
- Nature, Vol. 185, Issue 4717
Quorum sensing componentry opens new lines of communication
journal, August 2022
- Wang, Sally; Payne, Gregory F.; Bentley, William E.
- The EMBO Journal, Vol. 41, Issue 18
Soil microbiomes and climate change
journal, October 2019
- Jansson, Janet K.; Hofmockel, Kirsten S.
- Nature Reviews Microbiology, Vol. 18, Issue 1
Redox-Enabled Bio-Electronics for Information Acquisition and Transmission
journal, June 2023
- Liu, Yi; Kim, Eunkyoung; Motabar, Dana
- IEEE Transactions on Molecular, Biological and Multi-Scale Communications, Vol. 9, Issue 2