Designing Metabolic Division of Labor in Microbial Communities
Abstract
ABSTRACT Microbes face a trade-off between being metabolically independent and relying on neighboring organisms for the supply of some essential metabolites. This balance of conflicting strategies affects microbial community structure and dynamics, with important implications for microbiome research and synthetic ecology. A “gedanken” (thought) experiment to investigate this trade-off would involve monitoring the rise of mutual dependence as the number of metabolic reactions allowed in an organism is increasingly constrained. The expectation is that below a certain number of reactions, no individual organism would be able to grow in isolation and cross-feeding partnerships and division of labor would emerge. We implemented this idealized experiment using in silico genome-scale models. In particular, we used mixed-integer linear programming to identify trade-off solutions in communities of Escherichia coli strains. The strategies that we found revealed a large space of opportunities in nuanced and nonintuitive metabolic division of labor, including, for example, splitting the tricarboxylic acid (TCA) cycle into two separate halves. The systematic computation of possible solutions in division of labor for 1-, 2-, and 3-strain consortia resulted in a rich and complex landscape. This landscape displayed a nonlinear boundary, indicating that the loss of an intracellular reaction was not necessarily compensated formore »
- Publication Date:
- Research Org.:
- Boston Univ., MA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC)
- OSTI Identifier:
- 1505658
- Alternate Identifier(s):
- OSTI ID: 1610773
- Grant/Contract Number:
- SC0004962; SC0012627
- Resource Type:
- Published Article
- Journal Name:
- mSystems
- Additional Journal Information:
- Journal Name: mSystems Journal Volume: 4 Journal Issue: 2; Journal ID: ISSN 2379-5077
- Publisher:
- American Society for Microbiology
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Microbiology
Citation Formats
Thommes, Meghan, Wang, Taiyao, Zhao, Qi, Paschalidis, Ioannis C., Segrè, Daniel, and Dutton, ed., Rachel J. Designing Metabolic Division of Labor in Microbial Communities. United States: N. p., 2019.
Web. doi:10.1128/mSystems.00263-18.
Thommes, Meghan, Wang, Taiyao, Zhao, Qi, Paschalidis, Ioannis C., Segrè, Daniel, & Dutton, ed., Rachel J. Designing Metabolic Division of Labor in Microbial Communities. United States. https://doi.org/10.1128/mSystems.00263-18
Thommes, Meghan, Wang, Taiyao, Zhao, Qi, Paschalidis, Ioannis C., Segrè, Daniel, and Dutton, ed., Rachel J. Tue .
"Designing Metabolic Division of Labor in Microbial Communities". United States. https://doi.org/10.1128/mSystems.00263-18.
@article{osti_1505658,
title = {Designing Metabolic Division of Labor in Microbial Communities},
author = {Thommes, Meghan and Wang, Taiyao and Zhao, Qi and Paschalidis, Ioannis C. and Segrè, Daniel and Dutton, ed., Rachel J.},
abstractNote = {ABSTRACT Microbes face a trade-off between being metabolically independent and relying on neighboring organisms for the supply of some essential metabolites. This balance of conflicting strategies affects microbial community structure and dynamics, with important implications for microbiome research and synthetic ecology. A “gedanken” (thought) experiment to investigate this trade-off would involve monitoring the rise of mutual dependence as the number of metabolic reactions allowed in an organism is increasingly constrained. The expectation is that below a certain number of reactions, no individual organism would be able to grow in isolation and cross-feeding partnerships and division of labor would emerge. We implemented this idealized experiment using in silico genome-scale models. In particular, we used mixed-integer linear programming to identify trade-off solutions in communities of Escherichia coli strains. The strategies that we found revealed a large space of opportunities in nuanced and nonintuitive metabolic division of labor, including, for example, splitting the tricarboxylic acid (TCA) cycle into two separate halves. The systematic computation of possible solutions in division of labor for 1-, 2-, and 3-strain consortia resulted in a rich and complex landscape. This landscape displayed a nonlinear boundary, indicating that the loss of an intracellular reaction was not necessarily compensated for by a single imported metabolite. Different regions in this landscape were associated with specific solutions and patterns of exchanged metabolites. Our approach also predicts the existence of regions in this landscape where independent bacteria are viable but are outcompeted by cross-feeding pairs, providing a possible incentive for the rise of division of labor. IMPORTANCE Understanding how microbes assemble into communities is a fundamental open issue in biology, relevant to human health, metabolic engineering, and environmental sustainability. A possible mechanism for interactions of microbes is through cross-feeding, i.e., the exchange of small molecules. These metabolic exchanges may allow different microbes to specialize in distinct tasks and evolve division of labor. To systematically explore the space of possible strategies for division of labor, we applied advanced optimization algorithms to computational models of cellular metabolism. Specifically, we searched for communities able to survive under constraints (such as a limited number of reactions) that would not be sustainable by individual species. We found that predicted consortia partition metabolic pathways in ways that would be difficult to identify manually, possibly providing a competitive advantage over individual organisms. In addition to helping understand diversity in natural microbial communities, our approach could assist in the design of synthetic consortia.},
doi = {10.1128/mSystems.00263-18},
journal = {mSystems},
number = 2,
volume = 4,
place = {United States},
year = {Tue Apr 09 00:00:00 EDT 2019},
month = {Tue Apr 09 00:00:00 EDT 2019}
}
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1128/mSystems.00263-18
https://doi.org/10.1128/mSystems.00263-18
Other availability
Search WorldCat to find libraries that may hold this journal
Cited by: 62 works
Citation information provided by
Web of Science
Web of Science
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:
Networks of energetic and metabolic interactions define dynamics in microbial communities
journal, November 2015
- Embree, Mallory; Liu, Joanne K.; Al-Bassam, Mahmoud M.
- Proceedings of the National Academy of Sciences, Vol. 112, Issue 50
Ecosystems biology of microbial metabolism
journal, August 2011
- Klitgord, Niels; Segrè, Daniel
- Current Opinion in Biotechnology, Vol. 22, Issue 4
The phenomenon of microbial uncultivability
journal, October 2013
- Epstein, Ss
- Current Opinion in Microbiology, Vol. 16, Issue 5
From Cell Differentiation to Cell Collectives: Bacillus subtilis Uses Division of Labor to Migrate
journal, April 2015
- van Gestel, Jordi; Vlamakis, Hera; Kolter, Roberto
- PLOS Biology, Vol. 13, Issue 4
Environments that Induce Synthetic Microbial Ecosystems
journal, November 2010
- Klitgord, Niels; Segrè, Daniel
- PLoS Computational Biology, Vol. 6, Issue 11
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
Extreme genome reduction in symbiotic bacteria
journal, November 2011
- McCutcheon, John P.; Moran, Nancy A.
- Nature Reviews Microbiology, Vol. 10, Issue 1
Resource Availability Modulates the Cooperative and Competitive Nature of a Microbial Cross-Feeding Mutualism
journal, August 2016
- Hoek, Tim A.; Axelrod, Kevin; Biancalani, Tommaso
- PLOS Biology, Vol. 14, Issue 8
Analysis of fluorescent reporters indicates heterogeneity in glucose uptake and utilization in clonal bacterial populations
journal, January 2013
- Nikolic, Nela; Barner, Thomas; Ackermann, Martin
- BMC Microbiology, Vol. 13, Issue 1
An expanded genome-scale model of Escherichia coli K-12 (iJR904 GSM/GPR)
journal, August 2003
- Reed, Jennifer L.; Vo, Thuy D.; Schilling, Christophe H.
- Genome Biology, Vol. 4, Issue 9, p. R54
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
Metabolic Resource Allocation in Individual Microbes Determines Ecosystem Interactions and Spatial Dynamics
journal, May 2014
- Harcombe, William R.; Riehl, William J.; Dukovski, Ilija
- Cell Reports, Vol. 7, Issue 4
Functional Metabolic Map of Faecalibacterium prausnitzii, a Beneficial Human Gut Microbe
journal, July 2014
- Heinken, A.; Khan, M. T.; Paglia, G.
- Journal of Bacteriology, Vol. 196, Issue 18
Reconstruction and Use of Microbial Metabolic Networks: the Core Escherichia coli Metabolic Model as an Educational Guide
journal, September 2010
- Orth, Jeffrey D.; Palsson, Bernhard Ø.; Fleming, R. M. T.
- EcoSal Plus, Vol. 4, Issue 1
Metabolic modeling of species interaction in the human microbiome elucidates community-level assembly rules
journal, July 2013
- Levy, R.; Borenstein, E.
- Proceedings of the National Academy of Sciences, Vol. 110, Issue 31
The Black Queen Hypothesis: Evolution of Dependencies through Adaptive Gene Loss
journal, March 2012
- Morris, J. Jeffrey; Lenski, Richard E.; Zinser, Erik R.
- mBio, Vol. 3, Issue 2
Division of Labor in Biofilms: the Ecology of Cell Differentiation
journal, April 2015
- van Gestel, Jordi; Vlamakis, Hera; Kolter, Roberto
- Microbiology Spectrum, Vol. 3, Issue 2
Precise manipulation of bacterial chromosomes by conjugative assembly genome engineering
journal, September 2014
- Ma, Natalie J.; Moonan, Daniel W.; Isaacs, Farren J.
- Nature Protocols, Vol. 9, Issue 10
Engineering microbial consortia for controllable outputs
journal, March 2016
- Lindemann, Stephen R.; Bernstein, Hans C.; Song, Hyun-Seob
- The ISME Journal, Vol. 10, Issue 9
Metabolic model-based analysis of the emergence of bacterial cross-feeding via extensive gene loss
journal, June 2018
- McNally, Colin P.; Borenstein, Elhanan
- BMC Systems Biology, Vol. 12, Issue 1
Quantitative prediction of cellular metabolism with constraint-based models: the COBRA Toolbox v2.0
journal, August 2011
- Schellenberger, Jan; Que, Richard; Fleming, Ronan M. T.
- Nature Protocols, Vol. 6, Issue 9
NetCmpt: a network-based tool for calculating the metabolic competition between bacterial species
journal, July 2012
- Kreimer, Anat; Doron-Faigenboim, Adi; Borenstein, Elhanan
- Bioinformatics, Vol. 28, Issue 16
Modeling central metabolism and energy biosynthesis across microbial life
journal, August 2016
- Edirisinghe, Janaka N.; Weisenhorn, Pamela; Conrad, Neal
- BMC Genomics, Vol. 17, Issue 1
A functional perspective on phenotypic heterogeneity in microorganisms
journal, July 2015
- Ackermann, Martin
- Nature Reviews Microbiology, Vol. 13, Issue 8
Escherichia coli alpha-ketoglutarate permease is a constitutively expressed proton symporter.
journal, March 1992
- Seol, W.; Shatkin, A. J.
- Journal of Biological Chemistry, Vol. 267, Issue 9
Laboratory Evolution to Alternating Substrate Environments Yields Distinct Phenotypic and Genetic Adaptive Strategies
journal, April 2017
- Sandberg, Troy E.; Lloyd, Colton J.; Palsson, Bernhard O.
- Applied and Environmental Microbiology, Vol. 83, Issue 13
Fast growth phenotype of E. coli K-12 from adaptive laboratory evolution does not require intracellular flux rewiring
journal, November 2017
- Long, Christopher P.; Gonzalez, Jacqueline E.; Feist, Adam M.
- Metabolic Engineering, Vol. 44
Close Interspecies Interactions between Prokaryotes from Sulfureous Environments
journal, January 2011
- Müller, Johannes; Overmann, Jörg
- Frontiers in Microbiology, Vol. 2
Repeated evolution of an acetate-crossfeeding polymorphism in long-term populations of Escherichia coli
journal, July 1998
- Treves, D. S.; Manning, S.; Adams, J.
- Molecular Biology and Evolution, Vol. 15, Issue 7
Unusual cyanobacterial TCA cycles: not broken just different
journal, September 2012
- Steinhauser, Dirk; Fernie, Alisdair R.; Araújo, Wagner L.
- Trends in Plant Science, Vol. 17, Issue 9
Less is More: Selective Advantages can Explain the Prevalent loss of Biosynthetic Genes in Bacteria: Adaptive loss of Biosynthetic Genes in Bacteria
journal, July 2014
- D'Souza, Glen; Waschina, Silvio; Pande, Samay
- Evolution, Vol. 68, Issue 9
The dynamics of molecular evolution over 60,000 generations
journal, October 2017
- Good, Benjamin H.; McDonald, Michael J.; Barrick, Jeffrey E.
- Nature, Vol. 551, Issue 7678
The E. coli molecular phenotype under different growth conditions
journal, April 2017
- Caglar, Mehmet U.; Houser, John R.; Barnhart, Craig S.
- Scientific Reports, Vol. 7, Issue 1
Syntrophic exchange in synthetic microbial communities
journal, April 2014
- Mee, M. T.; Collins, J. J.; Church, G. M.
- Proceedings of the National Academy of Sciences, Vol. 111, Issue 20
Using Genome-scale Models to Predict Biological Capabilities
journal, May 2015
- O’Brien, Edward J.; Monk, Jonathan M.; Palsson, Bernhard O.
- Cell, Vol. 161, Issue 5
Microbial Community Metabolic Modeling: A Community Data-Driven Network Reconstruction: COMMUNITY DATA-DRIVEN METABOLIC NETWORK MODELING
journal, June 2016
- Henry, Christopher S.; Bernstein, Hans C.; Weisenhorn, Pamela
- Journal of Cellular Physiology, Vol. 231, Issue 11
Sampling for Metabolome Analysis of Microorganisms
journal, May 2007
- Bolten, Christoph J.; Kiefer, Patrick; Letisse, Fabien
- Analytical Chemistry, Vol. 79, Issue 10
Metabolic interactions in microbial communities: untangling the Gordian knot
journal, October 2015
- Ponomarova, Olga; Patil, Kiran Raosaheb
- Current Opinion in Microbiology, Vol. 27
Competitive resource allocation to metabolic pathways contributes to overflow metabolisms and emergent properties in cross-feeding microbial consortia
journal, February 2018
- Carlson, Ross P.; Beck, Ashley E.; Phalak, Poonam
- Biochemical Society Transactions, Vol. 46, Issue 2
Synthetic Escherichia coli consortia engineered for syntrophy demonstrate enhanced biomass productivity
journal, January 2012
- Bernstein, Hans C.; Paulson, Steven D.; Carlson, Ross P.
- Journal of Biotechnology, Vol. 157, Issue 1
Generation of genome-scale metabolic reconstructions for 773 members of the human gut microbiota
journal, November 2016
- Magnúsdóttir, Stefanía; Heinken, Almut; Kutt, Laura
- Nature Biotechnology, Vol. 35, Issue 1
Competitive and cooperative metabolic interactions in bacterial communities
journal, September 2011
- Freilich, Shiri; Zarecki, Raphy; Eilam, Omer
- Nature Communications, Vol. 2, Issue 1
Genome-driven evolutionary game theory helps understand the rise of metabolic interdependencies in microbial communities
journal, November 2017
- Zomorrodi, Ali R.; Segrè, Daniel
- Nature Communications, Vol. 8, Issue 1
Optimal allocation of metabolic functions among organisms in a microbial ecosystem
conference, December 2016
- Zhao, Qi; Segre, Daniel; Paschalidisy, Ioannis Ch.
- 2016 IEEE 55th Conference on Decision and Control (CDC)
A Programmable Escherichia coli Consortium via Tunable Symbiosis
journal, March 2012
- Kerner, Alissa; Park, Jihyang; Williams, Audra
- PLoS ONE, Vol. 7, Issue 3
Quantitative flux coupling analysis
journal, December 2018
- Tefagh, Mojtaba; Boyd, Stephen P.
- Journal of Mathematical Biology, Vol. 78, Issue 5
Managing uncertainty in metabolic network structure and improving predictions using EnsembleFBA
journal, March 2017
- Biggs, Matthew B.; Papin, Jason A.
- PLOS Computational Biology, Vol. 13, Issue 3
Variation and evolution of the citric-acid cycle: a genomic perspective
journal, July 1999
- Huynen, Martijn A.; Dandekar, Thomas; Bork, Peer
- Trends in Microbiology, Vol. 7, Issue 7
Dissecting the genetic and metabolic mechanisms of adaptation to the knockout of a major metabolic enzyme in Escherichia coli
journal, December 2017
- Long, Christopher P.; Gonzalez, Jacqueline E.; Feist, Adam M.
- Proceedings of the National Academy of Sciences, Vol. 115, Issue 1
Long-Term Experimental Evolution in Escherichia coli. XIII. Phylogenetic History of a Balanced Polymorphism
journal, June 2005
- Rozen, Daniel E.; Schneider, Dominique; Lenski, Richard E.
- Journal of Molecular Evolution, Vol. 61, Issue 2
Inferring Metabolic Mechanisms of Interaction within a Defined Gut Microbiota
journal, September 2018
- Medlock, Gregory L.; Carey, Maureen A.; McDuffie, Dennis G.
- Cell Systems, Vol. 7, Issue 3
Novel Cooperation Experimentally Evolved Between Species
journal, February 2010
- Harcombe, William
- Evolution
Tricarboxylic Acid Cycle and Glyoxylate Bypass
journal, July 2005
- Cronan, Jr., John E.; Laporte, David
- EcoSal Plus, Vol. 1, Issue 2
Design and analysis of synthetic carbon fixation pathways
journal, April 2010
- Bar-Even, A.; Noor, E.; Lewis, N. E.
- Proceedings of the National Academy of Sciences, Vol. 107, Issue 19, p. 8889-8894
Sequence homologies between proteins of bacterial phosphoenolpyruvate-dependent sugar phosphotransferase systems: identification of possible phosphate-carrying histidine residues.
journal, July 1987
- Bramley, H. F.; Kornberg, H. L.
- Proceedings of the National Academy of Sciences, Vol. 84, Issue 14
Bacterial Unculturability and the Formation of Intercellular Metabolic Networks
journal, May 2017
- Pande, Samay; Kost, Christian
- Trends in Microbiology, Vol. 25, Issue 5
Emergent cooperation in microbial metabolism
journal, January 2010
- Wintermute, Edwin H.; Silver, Pamela A.
- Molecular Systems Biology, Vol. 6, Issue 1
Metabolic Changes Associated With Adaptive Diversification in Escherichia coli
journal, February 2008
- Le Gac, Mickaël; Brazas, Michelle D.; Bertrand, Melanie
- Genetics, Vol. 178, Issue 2
Metabolic dependencies drive species co-occurrence in diverse microbial communities
journal, May 2015
- Zelezniak, Aleksej; Andrejev, Sergej; Ponomarova, Olga
- Proceedings of the National Academy of Sciences, Vol. 112, Issue 20
Oxygen-regulated gene expression in Escherichia coli: (Delivered at the 122nd Ordinary Meeting of the Society for General Microbiology, 25 March 1992)
journal, November 1992
- Guest, J. R.
- Journal of General Microbiology, Vol. 138, Issue 11
Experimental Evidence for Sympatric Ecological Diversification due to Frequency-Dependent Competition in Escherichia coli
journal, January 2004
- Friesen, Maren L.; Saxer, Gerda; Travisano, Michael
- Evolution, Vol. 58, Issue 2
Snowdrift game dynamics and facultative cheating in yeast
journal, April 2009
- Gore, Jeff; Youk, Hyun; van Oudenaarden, Alexander
- Nature, Vol. 459, Issue 7244
Stochastic Gene Expression in a Single Cell
journal, August 2002
- Elowitz, M. B.
- Science, Vol. 297, Issue 5584
BiGG Models: A platform for integrating, standardizing and sharing genome-scale models
journal, October 2015
- King, Zachary A.; Lu, Justin; Dräger, Andreas
- Nucleic Acids Research, Vol. 44, Issue D1
The Incomplete Tricarboxylic Acid Cycle in the Blue-green Alga Anabaena Variabilis
journal, March 1969
- Pearce, J.; Leach, C. K.; Carr, N. G.
- Journal of General Microbiology, Vol. 55, Issue 3
Extensive exometabolome analysis reveals extended overflow metabolism in various microorganisms
journal, January 2012
- Paczia, Nicole; Nilgen, Anke; Lehmann, Tobias
- Microbial Cell Factories, Vol. 11, Issue 1
From elementary flux modes to elementary flux vectors: Metabolic pathway analysis with arbitrary linear flux constraints
journal, April 2017
- Klamt, Steffen; Regensburger, Georg; Gerstl, Matthias P.
- PLOS Computational Biology, Vol. 13, Issue 4
Programming cells by multiplex genome engineering and accelerated evolution
journal, July 2009
- Wang, Harris H.; Isaacs, Farren J.; Carr, Peter A.
- Nature, Vol. 460, Issue 7257, p. 894-898
Metabolic division of labor in microbial systems
journal, February 2018
- Tsoi, Ryan; Wu, Feilun; Zhang, Carolyn
- Proceedings of the National Academy of Sciences, Vol. 115, Issue 10
Biotic Interactions Shape the Ecological Distributions of Staphylococcus Species
journal, October 2016
- Kastman, Erik K.; Kamelamela, Noelani; Norville, Josh W.
- mBio, Vol. 7, Issue 5
Emergent Biosynthetic Capacity in Simple Microbial Communities
journal, July 2014
- Chiu, Hsuan-Chao; Levy, Roie; Borenstein, Elhanan
- PLoS Computational Biology, Vol. 10, Issue 7
OptCom: A Multi-Level Optimization Framework for the Metabolic Modeling and Analysis of Microbial Communities
journal, February 2012
- Zomorrodi, Ali R.; Maranas, Costas D.
- PLoS Computational Biology, Vol. 8, Issue 2
Bayesian metabolic flux analysis reveals intracellular flux couplings
journal, July 2019
- Heinonen, Markus; Osmala, Maria; Mannerström, Henrik
- Bioinformatics, Vol. 35, Issue 14
Metabolic interactions between dynamic bacterial subpopulations
journal, May 2018
- Rosenthal, Adam Z.; Qi, Yutao; Hormoz, Sahand
- eLife, Vol. 7
Optknock: A bilevel programming framework for identifying gene knockout strategies for microbial strain optimization
journal, October 2003
- Burgard, Anthony P.; Pharkya, Priti; Maranas, Costas D.
- Biotechnology and Bioengineering, Vol. 84, Issue 6
Adaptive Diversification in Genes That Regulate Resource Use in Escherichia coli
journal, January 2007
- Spencer, Christine C.; Bertrand, Melanie; Travisano, Michael
- PLoS Genetics, Vol. 3, Issue 1
The PEP—pyruvate—oxaloacetate node as the switch point for carbon flux distribution in bacteria: We dedicate this paper to Rudolf K. Thauer, Director of the Max-Planck-Institute for Terrestrial Microbiology in Marburg, Germany, on the occasion of his 65th birthday
journal, September 2005
- Sauer, Uwe; Eikmanns, Bernhard J.
- FEMS Microbiology Reviews, Vol. 29, Issue 4
New approach for understanding genome variations in KEGG
journal, October 2018
- Kanehisa, Minoru; Sato, Yoko; Furumichi, Miho
- Nucleic Acids Research, Vol. 47, Issue D1
Systematic changes in gene expression patterns following adaptive evolution in yeast
journal, August 1999
- Ferea, T. L.; Botstein, D.; Brown, P. O.
- Proceedings of the National Academy of Sciences, Vol. 96, Issue 17
The Importance of Compartmentalization in Metabolic flux Models: Yeast as an Ecosystem of Organelles
conference, January 2012
- Klitgord, Niels; SegrÈ, Daniel
- Proceedings of the 9th Annual International Workshop on Bioinformatics and Systems Biology (IBSB 2009), Genome Informatics 2009
Adaptation increases the likelihood of diversification in an experimental bacterial lineage
journal, January 2008
- Spencer, C. C.; Tyerman, J.; Bertrand, M.
- Proceedings of the National Academy of Sciences, Vol. 105, Issue 5
Flux Coupling Analysis of Genome-Scale Metabolic Network Reconstructions
journal, February 2004
- Burgard, A. P.
- Genome Research, Vol. 14, Issue 2
Development and application of a differential method for reliable metabolome analysis in Escherichia coli
journal, March 2009
- Taymaz-Nikerel, Hilal; de Mey, Marjan; Ras, Cor
- Analytical Biochemistry, Vol. 386, Issue 1
Synthetic cooperation in engineered yeast populations
journal, January 2007
- Shou, W.; Ram, S.; Vilar, J. M. G.
- Proceedings of the National Academy of Sciences, Vol. 104, Issue 6
Metabolic network modeling of microbial communities: Metabolic network modeling
journal, June 2015
- Biggs, Matthew B.; Medlock, Gregory L.; Kolling, Glynis L.
- Wiley Interdisciplinary Reviews: Systems Biology and Medicine, Vol. 7, Issue 5
Community Flux Balance Analysis for Microbial Consortia at Balanced Growth
journal, May 2013
- Khandelwal, Ruchir A.; Olivier, Brett G.; Röling, Wilfred F. M.
- PLoS ONE, Vol. 8, Issue 5
Yeast Creates a Niche for Symbiotic Lactic Acid Bacteria through Nitrogen Overflow
journal, October 2017
- Ponomarova, Olga; Gabrielli, Natalia; Sévin, Daniel C.
- Cell Systems, Vol. 5, Issue 4
Microbial evolution in a simple unstructured environment: genetic differentiation in Escherichia coli.
journal, August 1994
- Rosenzweig, R. F.; Sharp, R. R.; Treves, D. S.
- Genetics, Vol. 137, Issue 4
Synthetic Ecology of Microbes: Mathematical Models and Applications
journal, February 2016
- Zomorrodi, Ali R.; Segrè, Daniel
- Journal of Molecular Biology, Vol. 428, Issue 5
Genomics and Evolution of Heritable Bacterial Symbionts
journal, December 2008
- Moran, Nancy A.; McCutcheon, John P.; Nakabachi, Atsushi
- Annual Review of Genetics, Vol. 42, Issue 1
Long‐Term Experimental Evolution in Escherichia coli . VIII. Dynamics of a Balanced Polymorphism
journal, January 2000
- Rozen, Daniel E.; Lenski, Richard E.
- The American Naturalist, Vol. 155, Issue 1
From Network Analysis to Functional Metabolic Modeling of the Human Gut Microbiota
journal, March 2018
- Bauer, Eugen; Thiele, Ines
- mSystems, Vol. 3, Issue 3
Overflow metabolism in Escherichia coli results from efficient proteome allocation
journal, December 2015
- Basan, Markus; Hui, Sheng; Okano, Hiroyuki
- Nature, Vol. 528, Issue 7580
Biogeography, Evolution, and Diversity of Epibionts in Phototrophic Consortia
journal, August 2004
- Glaeser, J.; Overmann, J.
- Applied and Environmental Microbiology, Vol. 70, Issue 8
F2C2: a fast tool for the computation of flux coupling in genome-scale metabolic networks
journal, April 2012
- Larhlimi, Abdelhalim; David, Laszlo; Selbig, Joachim
- BMC Bioinformatics, Vol. 13, Issue 1
Sugar Synthesis from CO2 in Escherichia coli
journal, June 2016
- Antonovsky, Niv; Gleizer, Shmuel; Noor, Elad
- Cell, Vol. 166, Issue 1
NetCooperate: a network-based tool for inferring host-microbe and microbe-microbe cooperation
journal, May 2015
- Levy, Roie; Carr, Rogan; Kreimer, Anat
- BMC Bioinformatics, Vol. 16, Issue 1
Multiplex Genome Engineering Using CRISPR/Cas Systems
journal, January 2013
- Cong, L.; Ran, F. A.; Cox, D.
- Science, Vol. 339, Issue 6121, p. 819-823
Evolution experiments with microorganisms: the dynamics and genetic bases of adaptation
journal, June 2003
- Elena, Santiago F.; Lenski, Richard E.
- Nature Reviews Genetics, Vol. 4, Issue 6
A challenge for 21st century molecular biology and biochemistry: what are the causes of obligate autotrophy and methanotrophy?
journal, June 2004
- Wood, Ann P.; Aurikko, Jukka P.; Kelly, Donovan P.
- FEMS Microbiology Reviews, Vol. 28, Issue 3
Building a morbidostat: an automated continuous-culture device for studying bacterial drug resistance under dynamically sustained drug inhibition
journal, February 2013
- Toprak, Erdal; Veres, Adrian; Yildiz, Sadik
- Nature Protocols, Vol. 8, Issue 3
Fitness and stability of obligate cross-feeding interactions that emerge upon gene loss in bacteria
journal, November 2013
- Pande, Samay; Merker, Holger; Bohl, Katrin
- The ISME Journal, Vol. 8, Issue 5