Electrogenetic signaling and information propagation for controlling microbial consortia via programmed lysis

VanArsdale, Eric; Navid, Ali; Chu, Monica J.; Halvorsen, Tiffany M.; Payne, Gregory F.; Jiao, Yongqin; Bentley, William E.; Yung, Mimi C.

doi:10.1002/bit.28337

Title: Electrogenetic signaling and information propagation for controlling microbial consortia via programmed lysis

Abstract

Abstract To probe signal propagation and genetic actuation in microbial consortia, we have coopted the components of both redox and quorum sensing (QS) signaling into a communication network for guiding composition by “programming” cell lysis. Here, we use an electrode to generate hydrogen peroxide as a redox cue that determines consortia composition. The oxidative stress regulon of Escherichia coli , OxyR, is employed to receive and transform this signal into a QS signal that coordinates the lysis of a subpopulation of cells. We examine a suite of information transfer modalities including “monoculture” and “transmitter‐receiver” models, as well as a series of genetic circuits that introduce time‐delays for altering information relay, thereby expanding design space. A simple mathematical model aids in developing communication schemes that accommodate the transient nature of redox signals and the “collective” attributes of QS signals. We suggest this platform methodology will be useful in understanding and controlling synthetic microbial consortia for a variety of applications, including biomanufacturing and biocontainment.

Authors:

VanArsdale, Eric ^[1]; Navid, Ali ^[2]; Chu, Monica J. ^[1]; Halvorsen, Tiffany M. ^[2]; Payne, Gregory F. ^[1]; Jiao, Yongqin ^[2];

^[1];

^[2]

Univ. of Maryland, College Park, MD (United States)
Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States)

Publication Date:: Sun Jan 29 00:00:00 EST 2023

Research Org.:: Lawrence Livermore National Laboratory (LLNL), Livermore, CA (United States)

Sponsoring Org.:: USDOE National Nuclear Security Administration (NNSA); National Science Foundation (NSF); Defense Threat Reduction Agency (DTRA); USDOE Laboratory Directed Research and Development (LDRD) Program

OSTI Identifier:: 1959519

Alternate Identifier(s):: OSTI ID: 1923934

Report Number(s):: LLNL-JRNL-841967
Journal ID: ISSN 0006-3592; 1064060

Grant/Contract Number:: AC52-07NA27344; CBET1932963; ECCS1807604; CBET1805274; MCB2227598; HDTRA1-19-1-0021; 17-ERD-013

Resource Type:: Accepted Manuscript

Journal Name:: Biotechnology and Bioengineering

Additional Journal Information:: Journal Volume: 120; Journal Issue: 5; Journal ID: ISSN 0006-3592

Publisher:: Wiley

Country of Publication:: United States

Language:: English

Subject:: 59 BASIC BIOLOGICAL SCIENCES; electrogenetic signaling; lysis protein E; quorum sensing signaling; synthetic microbial consortia

Citation Formats


                    VanArsdale, Eric, Navid, Ali, Chu, Monica J., Halvorsen, Tiffany M., Payne, Gregory F., Jiao, Yongqin, Bentley, William E., and Yung, Mimi C. Electrogenetic signaling and information propagation for controlling microbial consortia via programmed lysis.  United States: N. p., 2023. 
Web.  doi:10.1002/bit.28337.

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                    VanArsdale, Eric, Navid, Ali, Chu, Monica J., Halvorsen, Tiffany M., Payne, Gregory F., Jiao, Yongqin, Bentley, William E., & Yung, Mimi C. Electrogenetic signaling and information propagation for controlling microbial consortia via programmed lysis.  United States.  https://doi.org/10.1002/bit.28337

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                    VanArsdale, Eric, Navid, Ali, Chu, Monica J., Halvorsen, Tiffany M., Payne, Gregory F., Jiao, Yongqin, Bentley, William E., and Yung, Mimi C. Sun .  
"Electrogenetic signaling and information propagation for controlling microbial consortia via programmed lysis".  United States.  https://doi.org/10.1002/bit.28337.  https://www.osti.gov/servlets/purl/1959519.

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@article{osti_1959519,

  title        = {Electrogenetic signaling and information propagation for controlling microbial consortia via programmed lysis},

  author       = {VanArsdale, Eric and Navid, Ali and Chu, Monica J. and Halvorsen, Tiffany M. and Payne, Gregory F. and Jiao, Yongqin and Bentley, William E. and Yung, Mimi C.},

  abstractNote = {Abstract To probe signal propagation and genetic actuation in microbial consortia, we have coopted the components of both redox and quorum sensing (QS) signaling into a communication network for guiding composition by “programming” cell lysis. Here, we use an electrode to generate hydrogen peroxide as a redox cue that determines consortia composition. The oxidative stress regulon of Escherichia coli , OxyR, is employed to receive and transform this signal into a QS signal that coordinates the lysis of a subpopulation of cells. We examine a suite of information transfer modalities including “monoculture” and “transmitter‐receiver” models, as well as a series of genetic circuits that introduce time‐delays for altering information relay, thereby expanding design space. A simple mathematical model aids in developing communication schemes that accommodate the transient nature of redox signals and the “collective” attributes of QS signals. We suggest this platform methodology will be useful in understanding and controlling synthetic microbial consortia for a variety of applications, including biomanufacturing and biocontainment.},

  doi          = {10.1002/bit.28337},

  journal      = {Biotechnology and Bioengineering},

  number       = 5,

  volume       = 120,

  place        = {United States},

  year         = {Sun Jan 29 00:00:00 EST 2023},

  month        = {Sun Jan 29 00:00:00 EST 2023}

}

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Works referenced in this record:

Does efficiency sensing unify diffusion and quorum sensing?
journal, March 2007

Hense, Burkhard A.; Kuttler, Christina; Müller, Johannes
Nature Reviews Microbiology, Vol. 5, Issue 3
DOI: 10.1038/nrmicro1600

Sequestration‐based bistability enables tuning of the switching boundaries and design of a latch
journal, January 2012

Chen, David; Arkin, Adam P.
Molecular Systems Biology, Vol. 8, Issue 1
DOI: 10.1038/msb.2012.52

Structural determinants driving homoserine lactone ligand selection in the Pseudomonas aeruginosa LasR quorum-sensing receptor
journal, December 2018

McCready, Amelia R.; Paczkowski, Jon E.; Henke, Brad R.
Proceedings of the National Academy of Sciences, Vol. 116, Issue 1
DOI: 10.1073/pnas.1817239116

Fundamental trade-offs between information flow in single cells and cellular populations
journal, May 2017

Suderman, Ryan; Bachman, John A.; Smith, Adam
Proceedings of the National Academy of Sciences, Vol. 114, Issue 22
DOI: 10.1073/pnas.1615660114

Molecular communication in the rhizosphere
journal, December 2008

Faure, Denis; Vereecke, Danny; Leveau, Johan H. J.
Plant and Soil, Vol. 321, Issue 1-2
DOI: 10.1007/s11104-008-9839-2

Distributing a metabolic pathway among a microbial consortium enhances production of natural products
journal, January 2015

Zhou, Kang; Qiao, Kangjian; Edgar, Steven
Nature Biotechnology, Vol. 33, Issue 4
DOI: 10.1038/nbt.3095

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
DOI: 10.1021/acssynbio.1c00522

Bacterial quorum sensing in complex and dynamically changing environments
journal, April 2019

Mukherjee, Sampriti; Bassler, Bonnie L.
Nature Reviews Microbiology, Vol. 17, Issue 6
DOI: 10.1038/s41579-019-0186-5

Kinetic Model for Signal Binding to the Quorum Sensing Regulator LasR
journal, June 2013

Claussen, Anetta; Jakobsen, Tim; Bjarnsholt, Thomas
International Journal of Molecular Sciences, Vol. 14, Issue 7
DOI: 10.3390/ijms140713360

Engineering orthogonal synthetic timer circuits based on extracytoplasmic function σ factors
journal, July 2018

Pinto, Daniela; Vecchione, Stefano; Wu, Hao
Nucleic Acids Research, Vol. 46, Issue 14
DOI: 10.1093/nar/gky614

Bacterial Persisters and Infection: Past, Present, and Progressing
journal, September 2019

Gollan, Bridget; Grabe, Grzegorz; Michaux, Charlotte
Annual Review of Microbiology, Vol. 73, Issue 1
DOI: 10.1146/annurev-micro-020518-115650

Engineering microbial consortia by division of labor
journal, February 2019

Roell, Garrett W.; Zha, Jian; Carr, Rhiannon R.
Microbial Cell Factories, Vol. 18, Issue 1
DOI: 10.1186/s12934-019-1083-3

Comparison of Kill Switch Toxins in Plant-Beneficial Pseudomonas fluorescens Reveals Drivers of Lethality, Stability, and Escape
journal, November 2022

Halvorsen, Tiffany M.; Ricci, Dante P.; Park, Dan M.
ACS Synthetic Biology, Vol. 11, Issue 11
DOI: 10.1021/acssynbio.2c00386

Species- and site-specific genome editing in complex bacterial communities
journal, December 2021

Rubin, Benjamin E.; Diamond, Spencer; Cress, Brady F.
Nature Microbiology, Vol. 7, Issue 1
DOI: 10.1038/s41564-021-01014-7

Redox-mediated quorum sensing in plants
journal, September 2017

Fuller, Alexandra W.; Young, Phoebe; Pierce, B. Daniel
PLOS ONE, Vol. 12, Issue 9
DOI: 10.1371/journal.pone.0182655

Estimating Information Exchange Performance of Engineered Cell-to-cell Molecular Communications: A Computational Approach
conference, April 2018

Harper, Colton; Pierobon, Massimiliano; Magarini, Maurizio
IEEE INFOCOM 2018 - IEEE Conference on Computer Communications
DOI: 10.1109/INFOCOM.2018.8485834

Microbial oxidative stress response: Novel insights from environmental facultative anaerobic bacteria
journal, October 2015

Fu, Huihui; Yuan, Jie; Gao, Haichun
Archives of Biochemistry and Biophysics, Vol. 584
DOI: 10.1016/j.abb.2015.08.012

Harnessing the Potential of Killers and Altruists within the Microbial Community: A Possible Alternative to Antibiotic Therapy?
journal, November 2019

Ikryannikova, Larisa N.; Kurbatov, Leonid K.; Soond, Surinder M.
Antibiotics, Vol. 8, Issue 4
DOI: 10.3390/antibiotics8040230

Design of stable and self-regulated microbial consortia for chemical synthesis
journal, March 2022

Li, Xianglai; Zhou, Zhao; Li, Wenna
Nature Communications, Vol. 13, Issue 1
DOI: 10.1038/s41467-022-29215-6

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
DOI: 10.1016/j.mec.2021.e00176

Transporter engineering in microbial cell factories: the ins, the outs, and the in-betweens
journal, December 2020

van der Hoek, Steven A.; Borodina, Irina
Current Opinion in Biotechnology, Vol. 66
DOI: 10.1016/j.copbio.2020.08.002

Fundamental limits on the suppression of molecular fluctuations
journal, September 2010

Lestas, Ioannis; Vinnicombe, Glenn; Paulsson, Johan
Nature, Vol. 467, Issue 7312
DOI: 10.1038/nature09333

Bacterial co-culture with cell signaling translator and growth controller modules for autonomously regulated culture composition
journal, September 2019

Stephens, Kristina; Pozo, Maria; Tsao, Chen-Yu
Nature Communications, Vol. 10, Issue 1
DOI: 10.1038/s41467-019-12027-6

Real-time bioelectronic sensing of environmental contaminants
journal, November 2022

Atkinson, Joshua T.; Su, Lin; Zhang, Xu
Nature, Vol. 611, Issue 7936
DOI: 10.1038/s41586-022-05356-y

Perception and Degradation of N -Acyl Homoserine Lactone Quorum Sensing Signals by Mammalian and Plant Cells
journal, January 2011

Teplitski, Max; Mathesius, Ulrike; Rumbaugh, Kendra P.
Chemical Reviews, Vol. 111, Issue 1
DOI: 10.1021/cr100045m

The ecology of heterogeneity: soil bacterial communities and C dynamics
journal, March 2020

Nunan, Naoise; Schmidt, Hannes; Raynaud, Xavier
Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 375, Issue 1798
DOI: 10.1098/rstb.2019.0249

The internet of Bio-Nano things
journal, March 2015

Akyildiz, I.; Pierobon, M.; Balasubramaniam, S.
IEEE Communications Magazine, Vol. 53, Issue 3
DOI: 10.1109/MCOM.2015.7060516

Reductionist synthetic community approaches in root microbiome research
journal, June 2019

Liu, Yong-Xin; Qin, Yuan; Bai, Yang
Current Opinion in Microbiology, Vol. 49
DOI: 10.1016/j.mib.2019.10.010

Microbial Coculture for Flavonoid Synthesis
journal, July 2020

Xu, Peng; Marsafari, Monireh; Zha, Jian
Trends in Biotechnology, Vol. 38, Issue 7
DOI: 10.1016/j.tibtech.2020.01.008

Engineered Orthogonal Quorum Sensing Systems for Synthetic Gene Regulation in Escherichia coli
journal, April 2019

Tekel, Stefan J.; Smith, Christina L.; Lopez, Brianna
Frontiers in Bioengineering and Biotechnology, Vol. 7
DOI: 10.3389/fbioe.2019.00080

Design of orthogonal genetic switches based on a crosstalk map of σs, anti‐σs, and promoters
journal, January 2013

Rhodius, Virgil A.; Segall‐Shapiro, Thomas H.; Sharon, Brian D.
Molecular Systems Biology, Vol. 9, Issue 1
DOI: 10.1038/msb.2013.58

Genome-wide Reconstruction of OxyR and SoxRS Transcriptional Regulatory Networks under Oxidative Stress in Escherichia coli K-12 MG1655
journal, August 2015

Seo, Sang Woo; Kim, Donghyuk; Szubin, Richard
Cell Reports, Vol. 12, Issue 8
DOI: 10.1016/j.celrep.2015.07.043

Gradients and consequences of heterogeneity in biofilms
journal, February 2022

Jo, Jeanyoung; Price-Whelan, Alexa; Dietrich, Lars E. P.
Nature Reviews Microbiology, Vol. 20, Issue 10
DOI: 10.1038/s41579-022-00692-2

Electroactive microorganisms in bioelectrochemical systems
journal, March 2019

Logan, Bruce E.; Rossi, Ruggero; Ragab, Ala’a
Nature Reviews Microbiology, Vol. 17, Issue 5
DOI: 10.1038/s41579-019-0173-x

OxyS small RNA induces cell cycle arrest to allow DNA damage repair
journal, December 2017

Barshishat, Shir; Elgrably‐Weiss, Maya; Edelstein, Jonathan
The EMBO Journal, Vol. 37, Issue 3
DOI: 10.15252/embj.201797651

Design of synthetic human gut microbiome assembly and butyrate production
journal, May 2021

Clark, Ryan L.; Connors, Bryce M.; Stevenson, David M.
Nature Communications, Vol. 12, Issue 1
DOI: 10.1038/s41467-021-22938-y

Synthetic mixed-signal computation in living cells
journal, June 2016

Rubens, Jacob R.; Selvaggio, Gianluca; Lu, Timothy K.
Nature Communications, Vol. 7, Issue 1
DOI: 10.1038/ncomms11658

Bottom-Up Approaches to Synthetic Cooperation in Microbial Communities
journal, February 2019

Rodríguez Amor, Daniel; Dal Bello, Martina
Life, Vol. 9, Issue 1
DOI: 10.3390/life9010022

Utilization of microbial cocultures for converting mixed substrates to valuable bioproducts
journal, August 2022

Akdemir, Hulya; Liu, Yuxin; Zhuang, Lei
Current Opinion in Microbiology, Vol. 68
DOI: 10.1016/j.mib.2022.102157

Compartmentalized microbes and co-cultures in hydrogels for on-demand bioproduction and preservation
journal, February 2020

Johnston, Trevor G.; Yuan, Shuo-Fu; Wagner, James M.
Nature Communications, Vol. 11, Issue 1
DOI: 10.1038/s41467-020-14371-4

Is quorum sensing a side effect of diffusion sensing?
journal, August 2002

Redfield, R.
Trends in Microbiology, Vol. 10, Issue 8
DOI: 10.1016/S0966-842X(02)02400-9

Engineering of ecological niches to create stable artificial consortia for complex biotransformations
journal, April 2020

Shahab, Robert L.; Brethauer, Simone; Luterbacher, Jeremy S.
Current Opinion in Biotechnology, Vol. 62
DOI: 10.1016/j.copbio.2019.09.008

Optimisation of surface expression using the AIDA autotransporter
journal, September 2011

Gustavsson, Martin; Bäcklund, Emma; Larsson, Gen
Microbial Cell Factories, Vol. 10, Issue 1
DOI: 10.1186/1475-2859-10-72

Capacity of a Diffusion-Based Molecular Communication System With Channel Memory and Molecular Noise
journal, February 2013

Pierobon, Massimiliano; Akyildiz, Ian F.
IEEE Transactions on Information Theory, Vol. 59, Issue 2
DOI: 10.1109/TIT.2012.2219496

Origin of cooperativity in the activation of dimeric transcription factors
journal, February 2020

Welch, Martin; Brasen, Jens Christian; Workman, Christopher T.
Physical Review Research, Vol. 2, Issue 1
DOI: 10.1103/PhysRevResearch.2.013151

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
DOI: 10.1038/s41565-021-00878-4

An E. coli Cell-Free Expression Toolbox: Application to Synthetic Gene Circuits and Artificial Cells
journal, January 2012

Shin, Jonghyeon; Noireaux, Vincent
ACS Synthetic Biology, Vol. 1, Issue 1
DOI: 10.1021/sb200016s

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Title: Electrogenetic signaling and information propagation for controlling microbial consortia via programmed lysis

Abstract

Citation Formats

Does efficiency sensing unify diffusion and quorum sensing? journal, March 2007

Sequestration‐based bistability enables tuning of the switching boundaries and design of a latch journal, January 2012

Structural determinants driving homoserine lactone ligand selection in the Pseudomonas aeruginosa LasR quorum-sensing receptor journal, December 2018

Fundamental trade-offs between information flow in single cells and cellular populations journal, May 2017

Molecular communication in the rhizosphere journal, December 2008

Distributing a metabolic pathway among a microbial consortium enhances production of natural products journal, January 2015

Electrogenetic Signal Transmission and Propagation in Coculture to Guide Production of a Small Molecule, Tyrosine journal, February 2022

Bacterial quorum sensing in complex and dynamically changing environments journal, April 2019

Kinetic Model for Signal Binding to the Quorum Sensing Regulator LasR journal, June 2013

Engineering orthogonal synthetic timer circuits based on extracytoplasmic function σ factors journal, July 2018

Bacterial Persisters and Infection: Past, Present, and Progressing journal, September 2019

Engineering microbial consortia by division of labor journal, February 2019

Comparison of Kill Switch Toxins in Plant-Beneficial Pseudomonas fluorescens Reveals Drivers of Lethality, Stability, and Escape journal, November 2022

Species- and site-specific genome editing in complex bacterial communities journal, December 2021

Redox-mediated quorum sensing in plants journal, September 2017

Estimating Information Exchange Performance of Engineered Cell-to-cell Molecular Communications: A Computational Approach conference, April 2018

Microbial oxidative stress response: Novel insights from environmental facultative anaerobic bacteria journal, October 2015

Harnessing the Potential of Killers and Altruists within the Microbial Community: A Possible Alternative to Antibiotic Therapy? journal, November 2019

Design of stable and self-regulated microbial consortia for chemical synthesis journal, March 2022

Electronic signals are electrogenetically relayed to control cell growth and co-culture composition journal, December 2021

Transporter engineering in microbial cell factories: the ins, the outs, and the in-betweens journal, December 2020

Fundamental limits on the suppression of molecular fluctuations journal, September 2010

Bacterial co-culture with cell signaling translator and growth controller modules for autonomously regulated culture composition journal, September 2019

Real-time bioelectronic sensing of environmental contaminants journal, November 2022

Perception and Degradation of N -Acyl Homoserine Lactone Quorum Sensing Signals by Mammalian and Plant Cells journal, January 2011

The ecology of heterogeneity: soil bacterial communities and C dynamics journal, March 2020

The internet of Bio-Nano things journal, March 2015

Reductionist synthetic community approaches in root microbiome research journal, June 2019

Microbial Coculture for Flavonoid Synthesis journal, July 2020

Engineered Orthogonal Quorum Sensing Systems for Synthetic Gene Regulation in Escherichia coli journal, April 2019

Design of orthogonal genetic switches based on a crosstalk map of σs, anti‐σs, and promoters journal, January 2013

Genome-wide Reconstruction of OxyR and SoxRS Transcriptional Regulatory Networks under Oxidative Stress in Escherichia coli K-12 MG1655 journal, August 2015

Gradients and consequences of heterogeneity in biofilms journal, February 2022

Electroactive microorganisms in bioelectrochemical systems journal, March 2019

OxyS small RNA induces cell cycle arrest to allow DNA damage repair journal, December 2017

Design of synthetic human gut microbiome assembly and butyrate production journal, May 2021

Synthetic mixed-signal computation in living cells journal, June 2016

Bottom-Up Approaches to Synthetic Cooperation in Microbial Communities journal, February 2019

Utilization of microbial cocultures for converting mixed substrates to valuable bioproducts journal, August 2022

Compartmentalized microbes and co-cultures in hydrogels for on-demand bioproduction and preservation journal, February 2020

Is quorum sensing a side effect of diffusion sensing? journal, August 2002

Engineering of ecological niches to create stable artificial consortia for complex biotransformations journal, April 2020

Optimisation of surface expression using the AIDA autotransporter journal, September 2011

Capacity of a Diffusion-Based Molecular Communication System With Channel Memory and Molecular Noise journal, February 2013

Origin of cooperativity in the activation of dimeric transcription factors journal, February 2020

Bioelectronic control of a microbial community using surface-assembled electrogenetic cells to route signals journal, March 2021

An E. coli Cell-Free Expression Toolbox: Application to Synthetic Gene Circuits and Artificial Cells journal, January 2012

Does efficiency sensing unify diffusion and quorum sensing?
journal, March 2007

Sequestration‐based bistability enables tuning of the switching boundaries and design of a latch
journal, January 2012

Structural determinants driving homoserine lactone ligand selection in the Pseudomonas aeruginosa LasR quorum-sensing receptor
journal, December 2018

Fundamental trade-offs between information flow in single cells and cellular populations
journal, May 2017

Molecular communication in the rhizosphere
journal, December 2008

Distributing a metabolic pathway among a microbial consortium enhances production of natural products
journal, January 2015

Electrogenetic Signal Transmission and Propagation in Coculture to Guide Production of a Small Molecule, Tyrosine
journal, February 2022

Bacterial quorum sensing in complex and dynamically changing environments
journal, April 2019

Kinetic Model for Signal Binding to the Quorum Sensing Regulator LasR
journal, June 2013

Engineering orthogonal synthetic timer circuits based on extracytoplasmic function σ factors
journal, July 2018

Bacterial Persisters and Infection: Past, Present, and Progressing
journal, September 2019

Engineering microbial consortia by division of labor
journal, February 2019

Comparison of Kill Switch Toxins in Plant-Beneficial Pseudomonas fluorescens Reveals Drivers of Lethality, Stability, and Escape
journal, November 2022

Species- and site-specific genome editing in complex bacterial communities
journal, December 2021

Redox-mediated quorum sensing in plants
journal, September 2017

Estimating Information Exchange Performance of Engineered Cell-to-cell Molecular Communications: A Computational Approach
conference, April 2018

Microbial oxidative stress response: Novel insights from environmental facultative anaerobic bacteria
journal, October 2015

Harnessing the Potential of Killers and Altruists within the Microbial Community: A Possible Alternative to Antibiotic Therapy?
journal, November 2019

Design of stable and self-regulated microbial consortia for chemical synthesis
journal, March 2022

Electronic signals are electrogenetically relayed to control cell growth and co-culture composition
journal, December 2021

Transporter engineering in microbial cell factories: the ins, the outs, and the in-betweens
journal, December 2020

Fundamental limits on the suppression of molecular fluctuations
journal, September 2010

Bacterial co-culture with cell signaling translator and growth controller modules for autonomously regulated culture composition
journal, September 2019

Real-time bioelectronic sensing of environmental contaminants
journal, November 2022

Perception and Degradation of N -Acyl Homoserine Lactone Quorum Sensing Signals by Mammalian and Plant Cells
journal, January 2011

The ecology of heterogeneity: soil bacterial communities and C dynamics
journal, March 2020

The internet of Bio-Nano things
journal, March 2015

Reductionist synthetic community approaches in root microbiome research
journal, June 2019

Microbial Coculture for Flavonoid Synthesis
journal, July 2020

Engineered Orthogonal Quorum Sensing Systems for Synthetic Gene Regulation in Escherichia coli
journal, April 2019

Design of orthogonal genetic switches based on a crosstalk map of σs, anti‐σs, and promoters
journal, January 2013

Genome-wide Reconstruction of OxyR and SoxRS Transcriptional Regulatory Networks under Oxidative Stress in Escherichia coli K-12 MG1655
journal, August 2015

Gradients and consequences of heterogeneity in biofilms
journal, February 2022

Electroactive microorganisms in bioelectrochemical systems
journal, March 2019

OxyS small RNA induces cell cycle arrest to allow DNA damage repair
journal, December 2017

Design of synthetic human gut microbiome assembly and butyrate production
journal, May 2021

Synthetic mixed-signal computation in living cells
journal, June 2016

Bottom-Up Approaches to Synthetic Cooperation in Microbial Communities
journal, February 2019

Utilization of microbial cocultures for converting mixed substrates to valuable bioproducts
journal, August 2022

Compartmentalized microbes and co-cultures in hydrogels for on-demand bioproduction and preservation
journal, February 2020

Is quorum sensing a side effect of diffusion sensing?
journal, August 2002

Engineering of ecological niches to create stable artificial consortia for complex biotransformations
journal, April 2020

Optimisation of surface expression using the AIDA autotransporter
journal, September 2011

Capacity of a Diffusion-Based Molecular Communication System With Channel Memory and Molecular Noise
journal, February 2013

Origin of cooperativity in the activation of dimeric transcription factors
journal, February 2020

Bioelectronic control of a microbial community using surface-assembled electrogenetic cells to route signals
journal, March 2021

An E. coli Cell-Free Expression Toolbox: Application to Synthetic Gene Circuits and Artificial Cells
journal, January 2012