skip to main content
DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Bioprinting microbial communities to examine interspecies interactions in time and space

Abstract

Bioprinting experiments have emerged as an approach for studying complex cellular interactions in the context of spatial structure, ranging from intracellular networks to interspecies interactions in communities. Despite the progress made in developing and optimizing computational modeling parameters to recapitulate these interactions in silico, experimental verification of model predictions in vitro is often elusive, due to the limits of common laboratory culturing methods, especially at the micro- and nanoscale. In this work, micro-scale bioprinting was used to evaluate the spatiotemporal effects of metabolite sharing between partners in an artificial syntrophic consortium consisting of Salmonella enterica serovar Typhimurium and Escherichia coli. Micro-colonies of these bacteria were patterned at increasing spatial separation distances, in the presence of competitor or cooperator strains. Growth of the consortium members was evaluated and compared to predictions generated by a bacterial growth modeling platform known as Computation of Microbial Ecosystems in Time and Space (COMETS). In close agreement with simulation, experimental metabolite sharing between micro-colonies exhibited strong distance-dependency. When bioprinted micro-colonies were confronted with one-way or two-way diffusion barriers, such as the intervention of cooperative or competitive bacteria, experimental results showed that spatial positioning of the barriers critically influences metabolite sharing between consortium members. These results weremore » generally predicted by simulation in COMETS. Our data demonstrate the utility of micro-scale bioprinting to experimentally test which aspects of predictive microbial growth models hold at this spatial scale, and for a range of synthetic biology applications.« less

Authors:
ORCiD logo; ; ; ; ;
Publication Date:
Research Org.:
Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States)
Sponsoring Org.:
USDOE National Nuclear Security Administration (NNSA)
OSTI Identifier:
1462578
Alternate Identifier(s):
OSTI ID: 1600880
Report Number(s):
LLNL-JRNL-754585
Journal ID: ISSN 2057-1976
Grant/Contract Number:  
AC52-07NA27344; DC0006731
Resource Type:
Published Article
Journal Name:
Biomedical Physics & Engineering Express
Additional Journal Information:
Journal Name: Biomedical Physics & Engineering Express Journal Volume: 4 Journal Issue: 5; Journal ID: ISSN 2057-1976
Publisher:
IOP Publishing
Country of Publication:
Country unknown/Code not available
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Hynes, William F., Chacón, Jeremy, Segrè, Daniel, Marx, Christopher J., Cady, Nathaniel C., and Harcombe, William R. Bioprinting microbial communities to examine interspecies interactions in time and space. Country unknown/Code not available: N. p., 2018. Web. doi:10.1088/2057-1976/aad544.
Hynes, William F., Chacón, Jeremy, Segrè, Daniel, Marx, Christopher J., Cady, Nathaniel C., & Harcombe, William R. Bioprinting microbial communities to examine interspecies interactions in time and space. Country unknown/Code not available. doi:https://doi.org/10.1088/2057-1976/aad544
Hynes, William F., Chacón, Jeremy, Segrè, Daniel, Marx, Christopher J., Cady, Nathaniel C., and Harcombe, William R. Thu . "Bioprinting microbial communities to examine interspecies interactions in time and space". Country unknown/Code not available. doi:https://doi.org/10.1088/2057-1976/aad544.
@article{osti_1462578,
title = {Bioprinting microbial communities to examine interspecies interactions in time and space},
author = {Hynes, William F. and Chacón, Jeremy and Segrè, Daniel and Marx, Christopher J. and Cady, Nathaniel C. and Harcombe, William R.},
abstractNote = {Bioprinting experiments have emerged as an approach for studying complex cellular interactions in the context of spatial structure, ranging from intracellular networks to interspecies interactions in communities. Despite the progress made in developing and optimizing computational modeling parameters to recapitulate these interactions in silico, experimental verification of model predictions in vitro is often elusive, due to the limits of common laboratory culturing methods, especially at the micro- and nanoscale. In this work, micro-scale bioprinting was used to evaluate the spatiotemporal effects of metabolite sharing between partners in an artificial syntrophic consortium consisting of Salmonella enterica serovar Typhimurium and Escherichia coli. Micro-colonies of these bacteria were patterned at increasing spatial separation distances, in the presence of competitor or cooperator strains. Growth of the consortium members was evaluated and compared to predictions generated by a bacterial growth modeling platform known as Computation of Microbial Ecosystems in Time and Space (COMETS). In close agreement with simulation, experimental metabolite sharing between micro-colonies exhibited strong distance-dependency. When bioprinted micro-colonies were confronted with one-way or two-way diffusion barriers, such as the intervention of cooperative or competitive bacteria, experimental results showed that spatial positioning of the barriers critically influences metabolite sharing between consortium members. These results were generally predicted by simulation in COMETS. Our data demonstrate the utility of micro-scale bioprinting to experimentally test which aspects of predictive microbial growth models hold at this spatial scale, and for a range of synthetic biology applications.},
doi = {10.1088/2057-1976/aad544},
journal = {Biomedical Physics & Engineering Express},
number = 5,
volume = 4,
place = {Country unknown/Code not available},
year = {2018},
month = {8}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
DOI: https://doi.org/10.1088/2057-1976/aad544

Save / Share:

Works referenced in this record:

A comprehensive genome‐scale reconstruction of Escherichia coli metabolism—2011
journal, January 2011

  • Orth, Jeffrey D.; Conrad, Tom M.; Na, Jessica
  • Molecular Systems Biology, Vol. 7, Issue 1
  • DOI: 10.1038/msb.2011.65

Controlling laser-induced jet formation for bioprinting mesenchymal stem cells with high viability and high resolution
journal, September 2014


Generation of mesoscopic patterns of viable Escherichia coli by ambient laser transfer
journal, January 2002


Constraint-based analysis of metabolic capacity of Salmonella typhimurium during host-pathogen interaction
journal, January 2009

  • Raghunathan, Anu; Reed, Jennifer; Shin, Sookil
  • BMC Systems Biology, Vol. 3, Issue 1
  • DOI: 10.1186/1752-0509-3-38

Engineered bidirectional communication mediates a consensus in a microbial biofilm consortium
journal, October 2007

  • Brenner, K.; Karig, D. K.; Weiss, R.
  • Proceedings of the National Academy of Sciences, Vol. 104, Issue 44
  • DOI: 10.1073/pnas.0704256104

Defined spatial structure stabilizes a synthetic multispecies bacterial community
journal, November 2008

  • Kim, H. J.; Boedicker, J. Q.; Choi, J. W.
  • Proceedings of the National Academy of Sciences, Vol. 105, Issue 47
  • DOI: 10.1073/pnas.0807935105

Bacterial Small-Molecule Signaling Pathways
journal, February 2006


A hydrogel bioink toolkit for mimicking native tissue biochemical and mechanical properties in bioprinted tissue constructs
journal, October 2015


What is microbial community ecology?
journal, August 2009


Thermal Inkjet Printing in Tissue Engineering and Regenerative Medicine
journal, May 2012

  • Cui, Xiaofeng; Boland, Thomas; D. D'Lima, Darryl
  • Recent Patents on Drug Delivery & Formulation, Vol. 6, Issue 2
  • DOI: 10.2174/187221112800672949

Metabolic modeling of a mutualistic microbial community
journal, January 2007

  • Stolyar, Sergey; Van Dien, Steve; Hillesland, Kristina Linnea
  • Molecular Systems Biology, Vol. 3, Issue 1
  • DOI: 10.1038/msb4100131

Metabolic Resource Allocation in Individual Microbes Determines Ecosystem Interactions and Spatial Dynamics
journal, May 2014


Printing Multistrain Bacterial Patterns with a Piezoelectric Inkjet Printer
journal, July 2007


The spatial and metabolic basis of colony size variation
journal, January 2018

  • Chacón, Jeremy M.; Möbius, Wolfram; Harcombe, William R.
  • The ISME Journal, Vol. 12, Issue 3
  • DOI: 10.1038/s41396-017-0038-0

Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants the Keio collection
journal, February 2006

  • Baba, Tomoya; Ara, Takeshi; Hasegawa, Miki
  • Molecular Systems Biology, Vol. 2, Article No. 2006.0008
  • DOI: 10.1038/msb4100050

Local dispersal promotes biodiversity in a real-life game of rock–paper–scissors
journal, July 2002

  • Kerr, Benjamin; Riley, Margaret A.; Feldman, Marcus W.
  • Nature, Vol. 418, Issue 6894
  • DOI: 10.1038/nature00823

Stoichiometric flux balance models quantitatively predict growth and metabolic by-product secretion in wild-type Escherichia coli W3110.
journal, January 1994


Development of an Optimized Medium, Strain and High-Throughput Culturing Methods for Methylobacterium extorquens
journal, April 2013


Engineering microbial consortia: a new frontier in synthetic biology
journal, September 2008


Biomimicry of quorum sensing using bacterial lifecycle model
journal, May 2013


Calibration and analysis of genome-based models for microbial ecology
journal, October 2015


COOPERATIVE ORGANIZATION OF BACTERIAL COLONIES: From Genotype to Morphotype
journal, October 1998


A computational exploration of bacterial metabolic diversity identifying metabolic interactions and growth-efficient strain communities
journal, January 2011

  • Tzamali, Eleftheria; Poirazi, Panayiota; Tollis, Ioannis G.
  • BMC Systems Biology, Vol. 5, Issue 1
  • DOI: 10.1186/1752-0509-5-167

A genome-scale metabolic flux model of Escherichia coli K–12 derived from the EcoCyc database
journal, January 2014

  • Weaver, Daniel S.; Keseler, Ingrid M.; Mackie, Amanda
  • BMC Systems Biology, Vol. 8, Issue 1
  • DOI: 10.1186/1752-0509-8-79

Engineering ecosystems and synthetic ecologies
journal, January 2012

  • Mee, Michael T.; Wang, Harris H.
  • Molecular BioSystems, Vol. 8, Issue 10
  • DOI: 10.1039/c2mb25133g

Construction of high-density bacterial colony arrays and patterns by the ink-jet method
journal, January 2003

  • Xu, Tao; Petridou, Sevastioni; Lee, Eric H.
  • Biotechnology and Bioengineering, Vol. 85, Issue 1
  • DOI: 10.1002/bit.10768

Dynamic Flux Balance Analysis of Diauxic Growth in Escherichia coli
journal, September 2002


Biological laser printing of genetically modified Escherichia coli for biosensor applications
journal, September 2004


Novel Cooperation Experimentally Evolved Between Species
journal, February 2010


Adding biotic complexity alters the metabolic benefits of mutualism: SELECTION FOR MUTUALISM IN A COMMUNITY CONTEXT
journal, June 2016

  • Harcombe, William R.; Betts, Alex; Shapiro, Jason W.
  • Evolution, Vol. 70, Issue 8
  • DOI: 10.1111/evo.12973

Linking Molecular and Population Processes in Mathematical Models of Quorum Sensing
journal, July 2013


Designing microarray phantoms for hyperspectral imaging validation
journal, January 2012

  • Clarke, Matthew L.; Lee, Ji Youn; Samarov, Daniel V.
  • Biomedical Optics Express, Vol. 3, Issue 6
  • DOI: 10.1364/BOE.3.001291

Single Cell Isolation of Bacteria from Microbial Fuel Cells and Potomac River Sediment
journal, March 2010

  • Ringeisen, B. R.; Lizewski, S. E.; Fitzgerald, L. A.
  • Electroanalysis, Vol. 22, Issue 7-8
  • DOI: 10.1002/elan.200880012

Adult rat retinal ganglion cells and glia can be printed by piezoelectric inkjet printing
journal, December 2013


BSim: An Agent-Based Tool for Modeling Bacterial Populations in Systems and Synthetic Biology
journal, August 2012


Laser engineering of microbial systems
journal, April 2018

  • Yusupov, V. I.; Gorlenko, M. V.; Cheptsov, V. S.
  • Laser Physics Letters, Vol. 15, Issue 6
  • DOI: 10.1088/1612-202X/aab5ef

Developmental Design of Synthetic Bacterial Architectures by Morphogenetic Engineering
journal, June 2016


Navigating through models of chemotaxis
journal, February 2008


    Works referencing / citing this record:

    Tepidiforma bonchosmolovskayae gen. nov., sp. nov., a moderately thermophilic Chloroflexi bacterium from a Chukotka hot spring (Arctic, Russia), representing a novel class, Tepidiformia, which includes the previously uncultivated lineage OLB14
    journal, February 2020

    • Kochetkova, Tatiana V.; Zayulina, Kseniya S.; Zhigarkov, Vyacheslav S.
    • International Journal of Systematic and Evolutionary Microbiology, Vol. 70, Issue 2
    • DOI: 10.1099/ijsem.0.003902