A Microfluidics and Agent-Based Modeling Framework for Investigating Spatial Organization in Bacterial Colonies: The Case of Pseudomonas Aeruginosa and H1-Type VI Secretion Interactions
Abstract
The factors leading to changes in the organization of microbial assemblages at fine spatial scales are not well characterized or understood. However, they are expected to guide the succession of community development and function toward specific outcomes that could impact human health and the environment. In this study, we put forward a combined experimental and agent-based modeling framework and use it to interpret unique spatial organization patterns of H1-Type VI secretion system (T6SS) mutants of P. aeruginosa under spatial confinement. We find that key parameters, such as T6SS-mediated cell contact and lysis, spatial localization, relative species abundance, cell density and local concentrations of growth substrates and metabolites are influenced by spatial confinement. The model, written in the accessible programming language NetLogo, can be adapted to a variety of biological systems of interest and used to simulate experiments across a broad parameter space. It was implemented and run in a high-throughput mode by deploying it across multiple CPUs, with each simulation representing an individual well within a high-throughput microwell array experimental platform. The microfluidics and agent-based modeling framework we present in this paper provides an effective means by which to connect experimental studies in microbiology to model development. The work demonstratesmore »
- Authors:
- Publication Date:
- Research Org.:
- Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES); ORNL Laboratory Directed Research and Development (LDRD) Program
- OSTI Identifier:
- 1437197
- Alternate Identifier(s):
- OSTI ID: 1423048
- Grant/Contract Number:
- AC05-00OR22725
- Resource Type:
- Published Article
- Journal Name:
- Frontiers in Microbiology
- Additional Journal Information:
- Journal Name: Frontiers in Microbiology Journal Volume: 9; Journal ID: ISSN 1664-302X
- Publisher:
- Frontiers Media SA
- Country of Publication:
- Switzerland
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; 97 MATHEMATICS AND COMPUTING; agent-based modeling; Pseudomonas aeruginosa; Type VI secretion; silicon microwell arrays; microbial succession; microbial organization; spatial confinement
Citation Formats
Wilmoth, Jared L., Doak, Peter W., Timm, Andrea, Halsted, Michelle, Anderson, John D., Ginovart, Marta, Prats, Clara, Portell, Xavier, Retterer, Scott T., and Fuentes-Cabrera, Miguel. A Microfluidics and Agent-Based Modeling Framework for Investigating Spatial Organization in Bacterial Colonies: The Case of Pseudomonas Aeruginosa and H1-Type VI Secretion Interactions. Switzerland: N. p., 2018.
Web. doi:10.3389/fmicb.2018.00033.
Wilmoth, Jared L., Doak, Peter W., Timm, Andrea, Halsted, Michelle, Anderson, John D., Ginovart, Marta, Prats, Clara, Portell, Xavier, Retterer, Scott T., & Fuentes-Cabrera, Miguel. A Microfluidics and Agent-Based Modeling Framework for Investigating Spatial Organization in Bacterial Colonies: The Case of Pseudomonas Aeruginosa and H1-Type VI Secretion Interactions. Switzerland. https://doi.org/10.3389/fmicb.2018.00033
Wilmoth, Jared L., Doak, Peter W., Timm, Andrea, Halsted, Michelle, Anderson, John D., Ginovart, Marta, Prats, Clara, Portell, Xavier, Retterer, Scott T., and Fuentes-Cabrera, Miguel. Tue .
"A Microfluidics and Agent-Based Modeling Framework for Investigating Spatial Organization in Bacterial Colonies: The Case of Pseudomonas Aeruginosa and H1-Type VI Secretion Interactions". Switzerland. https://doi.org/10.3389/fmicb.2018.00033.
@article{osti_1437197,
title = {A Microfluidics and Agent-Based Modeling Framework for Investigating Spatial Organization in Bacterial Colonies: The Case of Pseudomonas Aeruginosa and H1-Type VI Secretion Interactions},
author = {Wilmoth, Jared L. and Doak, Peter W. and Timm, Andrea and Halsted, Michelle and Anderson, John D. and Ginovart, Marta and Prats, Clara and Portell, Xavier and Retterer, Scott T. and Fuentes-Cabrera, Miguel},
abstractNote = {The factors leading to changes in the organization of microbial assemblages at fine spatial scales are not well characterized or understood. However, they are expected to guide the succession of community development and function toward specific outcomes that could impact human health and the environment. In this study, we put forward a combined experimental and agent-based modeling framework and use it to interpret unique spatial organization patterns of H1-Type VI secretion system (T6SS) mutants of P. aeruginosa under spatial confinement. We find that key parameters, such as T6SS-mediated cell contact and lysis, spatial localization, relative species abundance, cell density and local concentrations of growth substrates and metabolites are influenced by spatial confinement. The model, written in the accessible programming language NetLogo, can be adapted to a variety of biological systems of interest and used to simulate experiments across a broad parameter space. It was implemented and run in a high-throughput mode by deploying it across multiple CPUs, with each simulation representing an individual well within a high-throughput microwell array experimental platform. The microfluidics and agent-based modeling framework we present in this paper provides an effective means by which to connect experimental studies in microbiology to model development. The work demonstrates progress in coupling experimental results to simulation while also highlighting potential sources of discrepancies between real-world experiments and idealized models.},
doi = {10.3389/fmicb.2018.00033},
journal = {Frontiers in Microbiology},
number = ,
volume = 9,
place = {Switzerland},
year = {Tue Feb 06 00:00:00 EST 2018},
month = {Tue Feb 06 00:00:00 EST 2018}
}
https://doi.org/10.3389/fmicb.2018.00033
Web of Science
Works referenced in this record:
Pseudomonas entomophila and Pseudomonas mendocina: Potential models for studying the bacterial type VI secretion system
journal, August 2011
- Sarris, Panagiotis F.; Scoulica, Effie V.
- Infection, Genetics and Evolution, Vol. 11, Issue 6
Superresolution Imaging of Intact Microbial Communities Reveals Molecular Architecture of Biofilm Development and Bacterial Organization
journal, February 2011
- Berk, Veysel; Fong, Nicholas; Dempsey, Graham
- Biophysical Journal, Vol. 100, Issue 3
A Virulence Locus of Pseudomonas aeruginosa Encodes a Protein Secretion Apparatus
journal, June 2006
- Mougous, J. D.
- Science, Vol. 312, Issue 5779
Toward Development of an Autonomous Network of Bacteria-Based Delivery Systems (BacteriaBots): Spatiotemporally High-Throughput Characterization of Bacterial Quorum-Sensing Response
journal, November 2014
- Sahari, Ali; Traore, Mahama A.; Stevens, Ann M.
- Analytical Chemistry, Vol. 86, Issue 23
The effect of biofilm permeability on bio-clogging of porous media
journal, December 2011
- Pintelon, Thomas R. R.; Picioreanu, Cristian; van Loosdrecht, Mark C. M.
- Biotechnology and Bioengineering, Vol. 109, Issue 4
Micropatterned culture of HepG2 spheroids using microwell chip with honeycomb-patterned polymer film
journal, October 2014
- Yamazaki, Hidekazu; Gotou, Shun; Ito, Koju
- Journal of Bioscience and Bioengineering, Vol. 118, Issue 4
Agent-based modeling of the complex life cycle of a cyanobacterium (Anabaena) in a shallow reservoir
journal, July 2008
- Hellweger, Ferdi L.; Kravchuk, Elena S.; Novotny, Vladimir
- Limnology and Oceanography, Vol. 53, Issue 4
Isolation, incubation, and parallel functional testing and identification by FISH of rare microbial single-copy cells from multi-species mixtures using the combination of chemistrode and stochastic confinement
journal, January 2009
- Liu, Weishan; Kim, Hyun Jung; Lucchetta, Elena M.
- Lab on a Chip, Vol. 9, Issue 15
The spatial organization and microbial community structure of an epilithic biofilm
journal, December 2014
- Cutler, Nick A.; Chaput, Dominique L.; Oliver, Anna E.
- FEMS Microbiology Ecology, Vol. 91, Issue 3
Killing by Type VI secretion drives genetic phase separation and correlates with increased cooperation
journal, February 2017
- McNally, Luke; Bernardy, Eryn; Thomas, Jacob
- Nature Communications, Vol. 8, Issue 1
A standard protocol for describing individual-based and agent-based models
journal, September 2006
- Grimm, Volker; Berger, Uta; Bastiansen, Finn
- Ecological Modelling, Vol. 198, Issue 1-2
A Type VI Secretion-Related Pathway in Bacteroidetes Mediates Interbacterial Antagonism
journal, August 2014
- Russell, Alistair B.; Wexler, Aaron G.; Harding, Brittany N.
- Cell Host & Microbe, Vol. 16, Issue 2
High-throughput superhydrophobic microwell arrays for investigating multifactorial stem cell niches
journal, January 2016
- Zhang, Pengfei; Zhang, Jianxiong; Bian, Shengtai
- Lab on a Chip, Vol. 16, Issue 16
Understanding the sequential activation of Type III and Type VI Secretion Systems in Salmonella typhimurium using Boolean modeling
journal, January 2013
- Das, Chandrani; Dutta, Anirban; Rajasingh, Hannah
- Gut Pathogens, Vol. 5, Issue 1
Individual-based modelling of carbon and nitrogen dynamics in soils: Parameterization and sensitivity analysis of microbial components
journal, June 2011
- Gras, Anna; Ginovart, Marta; Valls, Joaquim
- Ecological Modelling, Vol. 222, Issue 12
Evaluation of a Yersinia pestis mutant impaired in a thermoregulated type VI-like secretion system in flea, macrophage and murine models
journal, November 2009
- Robinson, Jennilee B.; Telepnev, Maxim V.; Zudina, Irina V.
- Microbial Pathogenesis, Vol. 47, Issue 5
Modeling the effect of soil meso- and macropores topology on the biodegradation of a soluble carbon substrate
journal, September 2015
- Vogel, Laure E.; Makowski, David; Garnier, Patricia
- Advances in Water Resources, Vol. 83
Spatial Organization of Microbial Biofilm Communities
journal, August 2000
- Tolker-Nielsen, T.; Molin, S.
- Microbial Ecology, Vol. 40, Issue 2
A Type VI Secretion System of Pseudomonas aeruginosa Targets a Toxin to Bacteria
journal, January 2010
- Hood, Rachel D.; Singh, Pragya; Hsu, FoSheng
- Cell Host & Microbe, Vol. 7, Issue 1
Human symbionts inject and neutralize antibacterial toxins to persist in the gut
journal, March 2016
- Wexler, Aaron G.; Bao, Yiqiao; Whitney, John C.
- Proceedings of the National Academy of Sciences, Vol. 113, Issue 13
Assembly and Tracking of Microbial Community Development within a Microwell Array Platform
journal, January 2017
- Timm, Andrea C.; Halsted, Michelle C.; Wilmoth, Jared L.
- Journal of Visualized Experiments, Issue 124
INDISIM-Paracoccus, an individual-based and thermodynamic model for a denitrifying bacterium
journal, August 2016
- Araujo Granda, Pablo; Gras, Anna; Ginovart, Marta
- Journal of Theoretical Biology, Vol. 403
Established Microbial Colonies Can Survive Type VI Secretion Assault
journal, October 2015
- Borenstein, David Bruce; Ringel, Peter; Basler, Marek
- PLOS Computational Biology, Vol. 11, Issue 10
Development of a simple static microwell array with uniform cell seeding and a chemical concentration gradient
journal, April 2017
- Yeh, S. I.; Hau, C. C.; Huang, C. J.
- Microfluidics and Nanofluidics, Vol. 21, Issue 5
Individual-based modelling of microbial activity to study mineralization of C and N and nitrification process in soil
journal, September 2005
- Ginovart, Marta; López, Daniel; Gras, Anna
- Nonlinear Analysis: Real World Applications, Vol. 6, Issue 4
One-step fabrication of three-dimensional polydimethylsiloxane peel-off microwell array for cell trapping
journal, January 2015
- Xue, Ning; Bleris, Leonidas; Lee, Jeong-Bong (JB)
- Journal of Micro/Nanolithography, MEMS, and MOEMS, Vol. 14, Issue 1
Tools for the Microbiome: Nano and Beyond
journal, December 2015
- Biteen, Julie S.; Blainey, Paul C.; Cardon, Zoe G.
- ACS Nano, Vol. 10, Issue 1
Development of transparent microwell arrays for optical monitoring and dissection of microbial communities
journal, November 2016
- Halsted, Michelle; Wilmoth, Jared L.; Briggs, Paige A.
- Journal of Vacuum Science & Technology B, Nanotechnology and Microelectronics: Materials, Processing, Measurement, and Phenomena, Vol. 34, Issue 6
BacSim, a simulator for individual-based modelling of bacterial colony growth
journal, December 1998
- Kreft, J. -U.; Booth, G.; Wimpenny, J. W. T.
- Microbiology, Vol. 144, Issue 12
INDISIM, An Individual-based Discrete Simulation Model to Study Bacterial Cultures
journal, January 2002
- Ginovart, Marta; LÓPez, Daniel; Valls, Joaquim
- Journal of Theoretical Biology, Vol. 214, Issue 2
Stochastic Assembly of Bacteria in Microwell Arrays Reveals the Importance of Confinement in Community Development
journal, May 2016
- Hansen, Ryan H.; Timm, Andrea C.; Timm, Collin M.
- PLOS ONE, Vol. 11, Issue 5
Strain competition restricts colonization of an enteric pathogen and prevents colitis
journal, July 2016
- Hecht, Aaron L.; Casterline, Benjamin W.; Earley, Zachary M.
- EMBO reports, Vol. 17, Issue 9
T6SS: The bacterial "fight club" in the host gut
journal, June 2017
- Sana, Thibault G.; Lugo, Kyler A.; Monack, Denise M.
- PLOS Pathogens, Vol. 13, Issue 6
Succession of microbial community and enhanced mechanism of a ZVI-based anaerobic granular sludge process treating chloronitrobenzenes wastewater
journal, March 2015
- Zhu, Liang; Jin, Jie; Lin, Haizhuan
- Journal of Hazardous Materials, Vol. 285
Disentangling mechanisms that mediate the balance between stochastic and deterministic processes in microbial succession
journal, March 2015
- Dini-Andreote, Francisco; Stegen, James C.; van Elsas, Jan Dirk
- Proceedings of the National Academy of Sciences, Vol. 112, Issue 11
Evolution of the CRISPR-Cas adaptive immunity systems in prokaryotes: models and observations on virus–host coevolution
journal, January 2015
- Koonin, Eugene V.; Wolf, Yuri I.
- Molecular BioSystems, Vol. 11, Issue 1
Soil microbial communities are shaped by plant-driven changes in resource availability during secondary succession
journal, December 2015
- Cline, Lauren C.; Zak, Donald R.
- Ecology, Vol. 96, Issue 12
Quantitative single-cell characterization of bacterial interactions reveals type VI secretion is a double-edged sword
journal, November 2012
- LeRoux, M.; De Leon, J. A.; Kuwada, N. J.
- Proceedings of the National Academy of Sciences, Vol. 109, Issue 48
Cell manipulation tool with combined microwell array and optical tweezers for cell isolation and deposition
journal, June 2013
- Wang, Xiaolin; Gou, Xue; Chen, Shuxun
- Journal of Micromechanics and Microengineering, Vol. 23, Issue 7
Small Molecules Modulating AHL-based Quorum Sensing to Attenuate Bacteria Virulence and Biofilms as Promising Antimicrobial Drugs
journal, December 2013
- Wang, Y.; Ma, S.
- Current Medicinal Chemistry, Vol. 21, Issue 3
The T6SSs of Pseudomonas aeruginosa Strain PAO1 and Their Effectors: Beyond Bacterial-Cell Targeting
journal, June 2016
- Sana, Thibault G.; Berni, Benjamin; Bleves, Sophie
- Frontiers in Cellular and Infection Microbiology, Vol. 6
Structure of a Peptidoglycan Amidase Effector Targeted to Gram-Negative Bacteria by the Type VI Secretion System
journal, June 2012
- Chou, Seemay; Bui, Nhat Khai; Russell, Alistair B.
- Cell Reports, Vol. 1, Issue 6
Individual-Based Modeling of Carbon and Nitrogen Dynamics in Soils: Parameterization and Sensitivity Analysis of Abiotic Components
journal, January 2010
- Gras, Anna; Ginovart, Marta; Portell, Xavier
- Soil Science, Vol. 175, Issue 8
iDynoMiCS: next-generation individual-based modelling of biofilms: iDynoMiCS for Biofilm Modelling
journal, March 2011
- Lardon, Laurent A.; Merkey, Brian V.; Martins, Sónia
- Environmental Microbiology, Vol. 13, Issue 9
Self-seeding microwell chip for the isolation and characterization of single cells
journal, January 2015
- Swennenhuis, Joost F.; Tibbe, Arjan G. J.; Stevens, Michiel
- Lab on a Chip, Vol. 15, Issue 14
The Landscape of Type VI Secretion across Human Gut Microbiomes Reveals Its Role in Community Composition
journal, September 2017
- Verster, Adrian J.; Ross, Benjamin D.; Radey, Matthew C.
- Cell Host & Microbe, Vol. 22, Issue 3
The ODD protocol: A review and first update
journal, November 2010
- Grimm, Volker; Berger, Uta; DeAngelis, Donald L.
- Ecological Modelling, Vol. 221, Issue 23
Works referencing / citing this record:
Disturbance Size Can Be Compensated for by Spatial Fragmentation in Soil Microbial Ecosystems
journal, August 2019
- König, Sara; Köhnke, Merlin C.; Firle, Anouk-Letizia
- Frontiers in Ecology and Evolution, Vol. 7
Emergent Properties of Microbial Activity in Heterogeneous Soil Microenvironments: Different Research Approaches Are Slowly Converging, Yet Major Challenges Remain
journal, August 2018
- Baveye, Philippe C.; Otten, Wilfred; Kravchenko, Alexandra
- Frontiers in Microbiology, Vol. 9
Modelización basada en agentes: canibalismo microbiano
journal, July 2019
- Ginovart, Marta; Tutusaus, Albert; Mas, M. Teresa
- Modelling in Science Education and Learning, Vol. 12, Issue 2