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Title: Assessing electrogenetic activation via a network model of biological signal propagation

Abstract

Introduction: Molecular communication is the transfer of information encoded by molecular structure and activity. We examine molecular communication within bacterial consortia as cells with diverse biosynthetic capabilities can be assembled for enhanced function. Their coordination, both in terms of engineered genetic circuits within individual cells as well as their population-scale functions, is needed to ensure robust performance. We have suggested that “electrogenetics,” the use of electronics to activate specific genetic circuits, is a means by which electronic devices can mediate molecular communication, ultimately enabling programmable control. Methods: Here, we have developed a graphical network model for dynamically assessing electronic and molecular signal propagation schemes wherein nodes represent individual cells, and their edges represent communication channels by which signaling molecules are transferred. We utilize graph properties such as edge dynamics and graph topology to interrogate the signaling dynamics of specific engineered bacterial consortia. Results: We were able to recapitulate previous experimental systems with our model. In addition, we found that networks with more distinct subpopulations (high network modularity) propagated signals more slowly than randomized networks, while strategic arrangement of subpopulations with respect to the inducer source (an electrode) can increase signal output and outperform otherwise homogeneous networks. Discussion: We developed thismore » model to better understand our previous experimental results, but also to enable future designs wherein subpopulation composition, genetic circuits, and spatial configurations can be varied to tune performance. We suggest that this work may provide insight into the signaling which occurs in synthetically assembled systems as well as native microbial communities.« less

Authors:
; ; ; ;
Publication Date:
Sponsoring Org.:
USDOE
OSTI Identifier:
2317716
Grant/Contract Number:  
BER#SCW1710
Resource Type:
Published Article
Journal Name:
Frontiers in Systems Biology
Additional Journal Information:
Journal Name: Frontiers in Systems Biology Journal Volume: 4; Journal ID: ISSN 2674-0702
Publisher:
Frontiers Media SA
Country of Publication:
Switzerland
Language:
English

Citation Formats

Chun, Kayla, VanArsdale, Eric, May, Elebeoba, Payne, Gregory F., and Bentley, William E. Assessing electrogenetic activation via a network model of biological signal propagation. Switzerland: N. p., 2024. Web. doi:10.3389/fsysb.2024.1291293.
Chun, Kayla, VanArsdale, Eric, May, Elebeoba, Payne, Gregory F., & Bentley, William E. Assessing electrogenetic activation via a network model of biological signal propagation. Switzerland. https://doi.org/10.3389/fsysb.2024.1291293
Chun, Kayla, VanArsdale, Eric, May, Elebeoba, Payne, Gregory F., and Bentley, William E. Fri . "Assessing electrogenetic activation via a network model of biological signal propagation". Switzerland. https://doi.org/10.3389/fsysb.2024.1291293.
@article{osti_2317716,
title = {Assessing electrogenetic activation via a network model of biological signal propagation},
author = {Chun, Kayla and VanArsdale, Eric and May, Elebeoba and Payne, Gregory F. and Bentley, William E.},
abstractNote = {Introduction: Molecular communication is the transfer of information encoded by molecular structure and activity. We examine molecular communication within bacterial consortia as cells with diverse biosynthetic capabilities can be assembled for enhanced function. Their coordination, both in terms of engineered genetic circuits within individual cells as well as their population-scale functions, is needed to ensure robust performance. We have suggested that “electrogenetics,” the use of electronics to activate specific genetic circuits, is a means by which electronic devices can mediate molecular communication, ultimately enabling programmable control. Methods: Here, we have developed a graphical network model for dynamically assessing electronic and molecular signal propagation schemes wherein nodes represent individual cells, and their edges represent communication channels by which signaling molecules are transferred. We utilize graph properties such as edge dynamics and graph topology to interrogate the signaling dynamics of specific engineered bacterial consortia. Results: We were able to recapitulate previous experimental systems with our model. In addition, we found that networks with more distinct subpopulations (high network modularity) propagated signals more slowly than randomized networks, while strategic arrangement of subpopulations with respect to the inducer source (an electrode) can increase signal output and outperform otherwise homogeneous networks. Discussion: We developed this model to better understand our previous experimental results, but also to enable future designs wherein subpopulation composition, genetic circuits, and spatial configurations can be varied to tune performance. We suggest that this work may provide insight into the signaling which occurs in synthetically assembled systems as well as native microbial communities.},
doi = {10.3389/fsysb.2024.1291293},
journal = {Frontiers in Systems Biology},
number = ,
volume = 4,
place = {Switzerland},
year = {Fri Mar 01 00:00:00 EST 2024},
month = {Fri Mar 01 00:00:00 EST 2024}
}

Works referenced in this record:

Development of a Quorum-Sensing Based Circuit for Control of Coculture Population Composition in a Naringenin Production System
journal, February 2020

  • Dinh, Christina V.; Chen, Xingyu; Prather, Kristala L. J.
  • ACS Synthetic Biology, Vol. 9, Issue 3
  • DOI: 10.1021/acssynbio.9b00451

Microbial production of valuable chemicals by modular co-culture strategy
journal, November 2022

  • Zhao, Shuo; Li, Fangfang; Yang, Fan
  • World Journal of Microbiology and Biotechnology, Vol. 39, Issue 1
  • DOI: 10.1007/s11274-022-03447-6

Network science
journal, March 2013

  • Barabási, Albert-László
  • Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences, Vol. 371, Issue 1987
  • DOI: 10.1098/rsta.2012.0375

Engineering bacterial motility towards hydrogen-peroxide
journal, May 2018


Redox Is a Global Biodevice Information Processing Modality
journal, July 2019


A First Course in Network Science
journal, January 2020


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


QUORUM SENSING: Cell-to-Cell Communication in Bacteria
journal, November 2005


A de novo matrix for macroscopic living materials from bacteria
journal, September 2022


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
  • DOI: 10.1038/s41467-020-16249-x

Programming a Human Commensal Bacterium, Bacteroides thetaiotaomicron, to Sense and Respond to Stimuli in the Murine Gut Microbiota
journal, July 2015


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
  • DOI: 10.1038/ncomms14030

Fast unfolding of communities in large networks
journal, October 2008

  • Blondel, Vincent D.; Guillaume, Jean-Loup; Lambiotte, Renaud
  • Journal of Statistical Mechanics: Theory and Experiment, Vol. 2008, Issue 10
  • DOI: 10.1088/1742-5468/2008/10/p10008

Parsed synthesis of pyocyanin via co-culture enables context-dependent intercellular redox communication
journal, November 2021


Rare and localized events stabilize microbial community composition and patterns of spatial self-organization in a fluctuating environment
journal, January 2022


Network science of biological systems at different scales: A review
journal, March 2018


Engineering consortia by polymeric microbial swarmbots
journal, July 2022


Engineered probiotic Escherichia coli can eliminate and prevent Pseudomonas aeruginosa gut infection in animal models
journal, April 2017

  • Hwang, In Young; Koh, Elvin; Wong, Adison
  • Nature Communications, Vol. 8, Issue 1
  • DOI: 10.1038/ncomms15028

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
  • DOI: 10.1002/bit.28337

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


Quorum Sensing in Escherichia coli Is Signaled by AI-2/LsrR: Effects on Small RNA and Biofilm Architecture
journal, August 2007

  • Li, Jun; Attila, Can; Wang, Liang
  • Journal of Bacteriology, Vol. 189, Issue 16
  • DOI: 10.1128/JB.00014-07

Finding and evaluating community structure in networks
journal, February 2004


Redox-operated genetic switches: the SoxR and OxyR transcription factors
journal, March 2001


Spatial heterogeneity in biofilm metabolism elicited by local control of phenazine methylation
journal, October 2023

  • Evans, Christopher R.; Smiley, Marina K.; Asahara Thio, Sean
  • Proceedings of the National Academy of Sciences, Vol. 120, Issue 43
  • DOI: 10.1073/pnas.2313208120

Programmable microbial ink for 3D printing of living materials produced from genetically engineered protein nanofibers
journal, November 2021

  • Duraj-Thatte, Anna M.; Manjula-Basavanna, Avinash; Rutledge, Jarod
  • Nature Communications, Vol. 12, Issue 1
  • DOI: 10.1038/s41467-021-26791-x

Engineering the shikimate pathway for biosynthesis of molecules with pharmaceutical activities in E. coli
journal, December 2016


Multifunctional Composite Hydrogels for Bacterial Capture, Growth/Elimination, and Sensing Applications
journal, October 2022

  • Dsouza, Andrea; Constantinidou, Chrystala; Arvanitis, Theodoros N.
  • ACS Applied Materials & Interfaces, Vol. 14, Issue 42
  • DOI: 10.1021/acsami.2c08582

Quorum Sensing Desynchronization Leads to Bimodality and Patterned Behaviors
journal, April 2016


In vitro evaluation of immune responses to bacterial hydrogels for the development of living therapeutic materials
journal, October 2023


Rational design of ‘controller cells’ to manipulate protein and phenotype expression
journal, July 2015


Construction of Synthetic Microbial Consortium for Violacein Production
journal, March 2023

  • Gwon, Da-ae; Seo, Euijin; Lee, Jeong Wook
  • Biotechnology and Bioprocess Engineering, Vol. 28, Issue 6
  • DOI: 10.1007/s12257-022-0284-5

seaborn: statistical data visualization
journal, April 2021


A photolabile hydrogel for guided three-dimensional cell growth and migration
journal, March 2004

  • Luo, Ying; Shoichet, Molly S.
  • Nature Materials, Vol. 3, Issue 4
  • DOI: 10.1038/nmat1092

Phenazine production promotes antibiotic tolerance and metabolic heterogeneity in Pseudomonas aeruginosa biofilms
journal, February 2019


Directed assembly of a bacterial quorum
journal, June 2015

  • Servinsky, Matthew D.; Terrell, Jessica L.; Tsao, Chen-Yu
  • The ISME Journal, Vol. 10, Issue 1
  • DOI: 10.1038/ismej.2015.89

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

Phenazine oxidation by a distal electrode modulates biofilm morphogenesis
journal, December 2020