Cooperation in microbial communities and their biotechnological applications

Cavaliere, Matteo; Feng, Song; Soyer, Orkun S.; Jiménez, José I.

doi:10.1111/1462-2920.13767

Title: Cooperation in microbial communities and their biotechnological applications

Journal Article · Wed Apr 26 00:00:00 EDT 2017 · Environmental Microbiology

DOI:https://doi.org/10.1111/1462-2920.13767· OSTI ID:1359990

Cavaliere, Matteo ^[1]; Feng, Song ^[2]; Soyer, Orkun S. ^[3]; Jiménez, José I. ^[4]

School of Informatics, BBSRC/EPSRC/MRC Synthetic Biology Research Centre, University of Edinburgh, Edinburgh EH8 9AB UK
Center for Nonlinear Studies, Theoretical Division (T-6), Los Alamos National Laboratory, Los Alamos NM 87545 USA
School of Life Sciences, BBSRC/EPSRC Warwick Integrative Synthetic Biology Centre, University of Warwick, Coventry CV4 7AL UK
Faculty of Health and Medical Sciences, University of Surrey, Guildford GU2 7XH UK

Microbial communities are increasingly utilized in biotechnology. Efficiency and productivity in many of these applications depends on the presence of cooperative interactions between members of the community. Two key processes underlying these interactions are the production of public goods and metabolic cross-feeding, which can be understood in the general framework of ecological and evolutionary (eco-evo) dynamics. In this review, we illustrate the relevance of cooperative interactions in microbial biotechnological processes, discuss their mechanistic origins and analyse their evolutionary resilience. Cooperative behaviours can be damaged by the emergence of ‘cheating’ cells that benefit from the cooperative interactions but do not contribute to them. Despite this, cooperative interactions can be stabilized by spatial segregation, by the presence of feedbacks between the evolutionary dynamics and the ecology of the community, by the role of regulatory systems coupled to the environmental conditions and by the action of horizontal gene transfer. Cooperative interactions enrich microbial communities with a higher degree of robustness against environmental stress and can facilitate the evolution of more complex traits. Therefore, the evolutionary resilience of microbial communities and their ability to constraint detrimental mutants should be considered to design robust biotechnological applications.

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Research Organization:: Los Alamos National Laboratory (LANL), Los Alamos, NM (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: XWJX00/3000FENG; AC52-06NA25396

OSTI ID:: 1359990

Alternate ID(s):: OSTI ID: 1359991; OSTI ID: 1625849

Journal Information:: Environmental Microbiology, Journal Name: Environmental Microbiology; ISSN 1462-2912

Publisher:: WileyCopyright Statement

Country of Publication:: United Kingdom

Language:: English

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Cited by: 93 works

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References (110)

Marine crude-oil biodegradation: a central role for interspecies interactions McGenity, Terry J.; Folwell, Benjamin D.; McKew, Boyd A. Aquatic Biosystems, Vol. 8, Issue 1 https://doi.org/10.1186/2046-9063-8-10	journal	January 2012
Availability of public goods shapes the evolution of competing metabolic strategies Bachmann, H.; Fischlechner, M.; Rabbers, I. Proceedings of the National Academy of Sciences, Vol. 110, Issue 35 https://doi.org/10.1073/pnas.1308523110	journal	August 2013
Shifts in growth strategies reflect tradeoffs in cellular economics Molenaar, Douwe; van Berlo, Rogier; de Ridder, Dick Molecular Systems Biology, Vol. 5, Issue 1 https://doi.org/10.1038/msb.2009.82	journal	January 2009
Distributing a metabolic pathway among a microbial consortium enhances production of natural products Zhou, Kang; Qiao, Kangjian; Edgar, Steven Nature Biotechnology, Vol. 33, Issue 4 https://doi.org/10.1038/nbt.3095	journal	January 2015
Microbial cell individuality and the underlying sources of heterogeneity Avery, Simon V. Nature Reviews Microbiology, Vol. 4, Issue 8 https://doi.org/10.1038/nrmicro1460	journal	August 2006
Social evolution theory for microorganisms West, Stuart A.; Griffin, Ashleigh S.; Gardner, Andy Nature Reviews Microbiology, Vol. 4, Issue 8 https://doi.org/10.1038/nrmicro1461	journal	August 2006
Plastic waste as a novel substrate for industrial biotechnology: Plastic waste as substrate for biotechnology Wierckx, Nick; Prieto, M. Auxiliadora; Pomposiello, Pablo Microbial Biotechnology, Vol. 8, Issue 6 https://doi.org/10.1111/1751-7915.12312	journal	August 2015
Effect of high loading on substrate utilization kinetics and microbial community structure in super fast submerged membrane bioreactor Sözen, S.; Çokgör, E. U.; Teksoy Başaran, S. Bioresource Technology, Vol. 159 https://doi.org/10.1016/j.biortech.2014.02.003	journal	May 2014
Metabolic Resource Allocation in Individual Microbes Determines Ecosystem Interactions and Spatial Dynamics Harcombe, William R.; Riehl, William J.; Dukovski, Ilija Cell Reports, Vol. 7, Issue 4 https://doi.org/10.1016/j.celrep.2014.03.070	journal	May 2014
Metabolic co-dependence gives rise to collective oscillations within biofilms Liu, Jintao; Prindle, Arthur; Humphries, Jacqueline Nature, Vol. 523, Issue 7562 https://doi.org/10.1038/nature14660	journal	July 2015
Molecular and functional analysis of the TOL plasmid pWWO from Pseudomonas putida and cloning of genes for the entire regulated aromatic ring meta cleavage pathway. Franklin, F. C.; Bagdasarian, M.; Bagdasarian, M. M. Proceedings of the National Academy of Sciences, Vol. 78, Issue 12 https://doi.org/10.1073/pnas.78.12.7458	journal	December 1981
Range expansion promotes cooperation in an experimental microbial metapopulation Datta, M. S.; Korolev, K. S.; Cvijovic, I. Proceedings of the National Academy of Sciences, Vol. 110, Issue 18 https://doi.org/10.1073/pnas.1217517110	journal	April 2013
Ecological public goods games: Cooperation and bifurcation Hauert, Christoph; Wakano, Joe Yuichiro; Doebeli, Michael Theoretical Population Biology, Vol. 73, Issue 2 https://doi.org/10.1016/j.tpb.2007.11.007	journal	March 2008
Self-organized patchiness facilitates survival in a cooperatively growing Bacillus subtilis population Ratzke, Christoph; Gore, Jeff Nature Microbiology, Vol. 1, Issue 5 https://doi.org/10.1038/nmicrobiol.2016.22	journal	March 2016
Quorum sensing protects bacterial co-operation from exploitation by cheats Allen, Richard C.; McNally, Luke; Popat, Roman The ISME Journal, Vol. 10, Issue 7 https://doi.org/10.1038/ismej.2015.232	journal	January 2016
Horizontal Gene Transfer of the Secretome Drives the Evolution of Bacterial Cooperation and Virulence Nogueira, Teresa; Rankin, Daniel J.; Touchon, Marie Current Biology, Vol. 19, Issue 20 https://doi.org/10.1016/j.cub.2009.08.056	journal	November 2009
Diversity and dynamics of microbial communities in engineered environments and their implications for process stability Briones, Aurelio; Raskin, Lutgarde Current Opinion in Biotechnology, Vol. 14, Issue 3 https://doi.org/10.1016/S0958-1669(03)00065-X	journal	June 2003
Cooperation driven by mutations in multi-person Prisoner's Dilemma Eriksson, Anders; Lindgren, Kristian Journal of Theoretical Biology, Vol. 232, Issue 3 https://doi.org/10.1016/j.jtbi.2004.08.020	journal	February 2005
Eco-evolutionary feedbacks can rescue cooperation in microbial populations Moreno-Fenoll, Clara; Cavaliere, Matteo; Martínez-García, Esteban Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/srep42561	journal	February 2017
Simpson's Paradox in a Synthetic Microbial System Chuang, J. S.; Rivoire, O.; Leibler, S. Science, Vol. 323, Issue 5911 https://doi.org/10.1126/science.1166739	journal	January 2009
Thermodynamics of hydrogen metabolism in methanogenic cocultures degrading ethanol or lactate Seitz, H. -J.; Schink, B.; Conrad, R. FEMS Microbiology Letters, Vol. 55, Issue 2 https://doi.org/10.1111/j.1574-6968.1988.tb13918.x	journal	October 1988
Engineering microbial consortia for controllable outputs Lindemann, Stephen R.; Bernstein, Hans C.; Song, Hyun-Seob The ISME Journal, Vol. 10, Issue 9 https://doi.org/10.1038/ismej.2016.26	journal	March 2016
Glycolytic strategy as a tradeoff between energy yield and protein cost Flamholz, A.; Noor, E.; Bar-Even, A. Proceedings of the National Academy of Sciences, Vol. 110, Issue 24 https://doi.org/10.1073/pnas.1215283110	journal	April 2013
Evolutionary Ecology of Microorganisms: From the Tamed to the Wild Lennon, Jay T.; Denef, Vincent J. Manual of Environmental Microbiology https://doi.org/10.1128/9781555818821.ch4.1.2	book	September 2015
The role of interactions, sessile growth, and nutrient amendments on the degradative efficiency of a microbial consortium Wolfaardt, G. M.; Lawrence, J. R.; Robarts, R. D. Canadian Journal of Microbiology, Vol. 40, Issue 5 https://doi.org/10.1139/m94-055	journal	May 1994
Linking thermodynamics and kinetics to assess pathway reversibility in anaerobic bioprocesses González-Cabaleiro, Rebeca; Lema, Juan M.; Rodríguez, Jorge Energy & Environmental Science, Vol. 6, Issue 12 https://doi.org/10.1039/c3ee42754d	journal	January 2013
Competitive fates of bacterial social parasites: persistence and self–induced extinction of Myxococcus xanthus cheaters Fiegna, Francesca; Velicer, Gregory J. Proceedings of the Royal Society of London. Series B: Biological Sciences, Vol. 270, Issue 1523 https://doi.org/10.1098/rspb.2003.2387	journal	July 2003
The private life of environmental bacteria: pollutant biodegradation at the single cell level: Phenotypic diversification of environmental bacteria Nikel, Pablo Iván; Silva-Rocha, Rafael; Benedetti, Ilaria Environmental Microbiology, Vol. 16, Issue 3 https://doi.org/10.1111/1462-2920.12360	journal	January 2014
Self-destructive cooperation mediated by phenotypic noise Ackermann, Martin; Stecher, Bärbel; Freed, Nikki E. Nature, Vol. 454, Issue 7207 https://doi.org/10.1038/nature07067	journal	August 2008
Extracellular Lipase and Protease Production from a Model Drinking Water Bacterial Community Is Functionally Robust to Absence of Individual Members Willsey, Graham G.; Wargo, Matthew J. PLOS ONE, Vol. 10, Issue 11 https://doi.org/10.1371/journal.pone.0143617	journal	November 2015
Horizontal gene transfer in osmotrophs: playing with public goods Richards, Thomas A.; Talbot, Nicholas J. Nature Reviews Microbiology, Vol. 11, Issue 10 https://doi.org/10.1038/nrmicro3108	journal	September 2013
Microbial syntrophy: interaction for the common good Morris, Brandon E. L.; Henneberger, Ruth; Huber, Harald FEMS Microbiology Reviews, Vol. 37, Issue 3 https://doi.org/10.1111/1574-6976.12019	journal	May 2013
Evolutionary game theory: Theoretical concepts and applications to microbial communities Frey, Erwin Physica A: Statistical Mechanics and its Applications, Vol. 389, Issue 20 https://doi.org/10.1016/j.physa.2010.02.047	journal	October 2010
Design and characterization of synthetic fungal-bacterial consortia for direct production of isobutanol from cellulosic biomass Minty, Jeremy J.; Singer, Marc E.; Scholz, Scott A. Proceedings of the National Academy of Sciences, Vol. 110, Issue 36 https://doi.org/10.1073/pnas.1218447110	journal	August 2013
Evolutionary Dynamics of Biological Games Nowak, M. A. Science, Vol. 303, Issue 5659 https://doi.org/10.1126/science.1093411	journal	February 2004
Biodegradation of Oil Tank Bottom Sludge using Microbial Consortia Gallego, José Luis R.; García-Martínez, María Jesús; Llamas, Juan F. Biodegradation, Vol. 18, Issue 3 https://doi.org/10.1007/s10532-006-9061-y	journal	July 2006
Collective sensing and collective responses in quorum-sensing bacteria Popat, R.; Cornforth, D. M.; McNally, L. Journal of The Royal Society Interface, Vol. 12, Issue 103 https://doi.org/10.1098/rsif.2014.0882	journal	February 2015
On the Origin of Cooperation Pennisi, E. Science, Vol. 325, Issue 5945 https://doi.org/10.1126/science.325_1196	journal	September 2009
Release of ecologically relevant metabolites by the cyanobacterium S ynechococcus elongatus CCMP 1631 : Metabolomics of Fiore, Cara L.; Longnecker, Krista; Kido Soule, Melissa C. Environmental Microbiology, Vol. 17, Issue 10 https://doi.org/10.1111/1462-2920.12899	journal	July 2015
Evolutionary game theory using agent-based methods Adami, Christoph; Schossau, Jory; Hintze, Arend Physics of Life Reviews, Vol. 19 https://doi.org/10.1016/j.plrev.2016.08.015	journal	December 2016
Anaerobic Degradation of Lactate by Syntrophic Associations of Methanosarcina barkeri and Desulfovibrio Species and Effect of H2 on Acetate Degradation McInerney, Michael J.; Bryant, Marvin P. Applied and Environmental Microbiology, Vol. 41, Issue 2 https://doi.org/10.1128/AEM.41.2.346-354.1981	journal	January 1981
Economics of membrane occupancy and respiro‐fermentation Zhuang, Kai; Vemuri, Goutham N.; Mahadevan, Radhakrishnan Molecular Systems Biology, Vol. 7, Issue 1 https://doi.org/10.1038/msb.2011.34	journal	January 2011
Interspecies bacterial interactions in biofilms James, G. A.; Beaudette, L.; Costerton, J. W. Journal of Industrial Microbiology, Vol. 15, Issue 4 https://doi.org/10.1007/BF01569978	journal	October 1995
Mechanisms of Action of the Maltogenic α-Amylase of Byssochlamys Fulva Doyle, EvelynM; Noone, AgnesM; Kelly, CatherineT Enzyme and Microbial Technology, Vol. 22, Issue 7 https://doi.org/10.1016/S0141-0229(97)00267-6	journal	May 1998
Stochasticity of TOL plasmid catabolic promoters sets a bimodal expression regime in Pseudomonas putida mt-2 exposed to m- xylene : Stochasticity in expression of catabolic pathways Silva-Rocha, Rafael; de Lorenzo, Víctor Molecular Microbiology, Vol. 86, Issue 1 https://doi.org/10.1111/j.1365-2958.2012.08184.x	journal	August 2012
Strategies of microbial cheater control Travisano, Michael; Velicer, Gregory J. Trends in Microbiology, Vol. 12, Issue 2 https://doi.org/10.1016/j.tim.2003.12.009	journal	February 2004
Segregating metabolic processes into different microbial cells accelerates the consumption of inhibitory substrates Lilja, Elin E.; Johnson, David R. The ISME Journal, Vol. 10, Issue 7 https://doi.org/10.1038/ismej.2015.243	journal	January 2016
The Social Lives of Microbes West, Stuart A.; Diggle, Stephen P.; Buckling, Angus Annual Review of Ecology, Evolution, and Systematics, Vol. 38, Issue 1 https://doi.org/10.1146/annurev.ecolsys.38.091206.095740	journal	December 2007
Snowdrift game dynamics and facultative cheating in yeast Gore, Jeff; Youk, Hyun; van Oudenaarden, Alexander Nature, Vol. 459, Issue 7244 https://doi.org/10.1038/nature07921	journal	April 2009
Redox balance is key to explaining full vs. partial switching to low-yield metabolism van Hoek, Milan JA; Merks, Roeland MH BMC Systems Biology, Vol. 6, Issue 1 https://doi.org/10.1186/1752-0509-6-22	journal	January 2012
Origin and analysis of microbial population heterogeneity in bioprocesses Müller, Susann; Harms, Hauke; Bley, Thomas Current Opinion in Biotechnology, Vol. 21, Issue 1 https://doi.org/10.1016/j.copbio.2010.01.002	journal	February 2010
What traits are carried on mobile genetic elements, and why? Rankin, D. J.; Rocha, E. P. C.; Brown, S. P. Heredity, Vol. 106, Issue 1 https://doi.org/10.1038/hdy.2010.24	journal	March 2010
Spatial structure, cooperation and competition in biofilms Nadell, Carey D.; Drescher, Knut; Foster, Kevin R. Nature Reviews Microbiology, Vol. 14, Issue 9 https://doi.org/10.1038/nrmicro.2016.84	journal	July 2016
Spatial Population Expansion Promotes the Evolution of Cooperation in an Experimental Prisoner’s Dilemma Van Dyken, J. David; Müller, Melanie J. I.; Mack, Keenan M. L. Current Biology, Vol. 23, Issue 10 https://doi.org/10.1016/j.cub.2013.04.026	journal	May 2013
Extensive exometabolome analysis reveals extended overflow metabolism in various microorganisms Paczia, Nicole; Nilgen, Anke; Lehmann, Tobias Microbial Cell Factories, Vol. 11, Issue 1 https://doi.org/10.1186/1475-2859-11-122	journal	January 2012
Energetics of Syntrophic Propionate Oxidation in Defined Batch and Chemostat Cocultures Scholten, J. C. M.; Conrad, R. Applied and Environmental Microbiology, Vol. 66, Issue 7 https://doi.org/10.1128/AEM.66.7.2934-2942.2000	journal	July 2000
Biodegradable Polymers for the Environment Gross, R. A. Science, Vol. 297, Issue 5582 https://doi.org/10.1126/science.297.5582.803	journal	August 2002
Cellulose Degradation by Oxidative Enzymes Dimarogona, Maria; Topakas, Evangelos; Christakopoulos, Paul Computational and Structural Biotechnology Journal, Vol. 2, Issue 3 https://doi.org/10.5936/csbj.201209015	journal	September 2012
Engineering synthetic bacterial consortia for enhanced desulfurization and revalorization of oil sulfur compounds Martínez, Igor; Mohamed, Magdy El-Said; Rozas, Daniel Metabolic Engineering, Vol. 35 https://doi.org/10.1016/j.ymben.2016.01.005	journal	May 2016
Distributed biological computation with multicellular engineered networks Regot, Sergi; Macia, Javier; Conde, Núria Nature, Vol. 469, Issue 7329 https://doi.org/10.1038/nature09679	journal	December 2010
Calibration and analysis of genome-based models for microbial ecology Louca, Stilianos; Doebeli, Michael eLife, Vol. 4 https://doi.org/10.7554/eLife.08208	journal	October 2015
Evolution of Cross‐Feeding in Microbial Populations Pfeiffer, Thomas; Bonhoeffer, Sebastian The American Naturalist, Vol. 163, Issue 6 https://doi.org/10.1086/383593	journal	June 2004
Studies on α-amylase formation by Bacillus subtilis Coleman, G.; Elliott, Wh Biochemical Journal, Vol. 83, Issue 2 https://doi.org/10.1042/bj0830256	journal	May 1962
Increased production of α-amylase from Thermomyces lanuginosus by the addition of Tween 80 Arnesen, Steen; Havn Eriksen, Susanne; Olsen, J. ørgen Enzyme and Microbial Technology, Vol. 23, Issue 3-4 https://doi.org/10.1016/S0141-0229(98)00040-4	journal	August 1998
Field applications of genetically engineered microorganisms for bioremediation processes Sayler, Gary S.; Ripp, Steven Current Opinion in Biotechnology, Vol. 11, Issue 3 https://doi.org/10.1016/S0958-1669(00)00097-5	journal	June 2000
Biochemical characterization of the cutinases from Thermobifida fusca Chen, Sheng; Su, Lingqia; Billig, Susan Journal of Molecular Catalysis B: Enzymatic, Vol. 63, Issue 3-4 https://doi.org/10.1016/j.molcatb.2010.01.001	journal	May 2010
Mobile genetic elements are involved in bacterial sociality Dimitriu, Tatiana; Misevic, Dusan; Lindner, Ariel B. Mobile Genetic Elements, Vol. 5, Issue 1 https://doi.org/10.1080/2159256X.2015.1006110	journal	January 2015
Quantification of syntrophic acetate-oxidizing microbial communities in biogas processes: Quantity of SAO organisms in high ammonia biogas processes Westerholm, Maria; Dolfing, Jan; Sherry, Angela Environmental Microbiology Reports, Vol. 3, Issue 4 https://doi.org/10.1111/j.1758-2229.2011.00249.x	journal	March 2011
Exploring mutualistic interactions between microalgae and bacteria in the omics age Cooper, Matthew B.; Smith, Alison G. Current Opinion in Plant Biology, Vol. 26 https://doi.org/10.1016/j.pbi.2015.07.003	journal	August 2015
Adaptive Diversification in Genes That Regulate Resource Use in Escherichia coli Spencer, Christine C.; Bertrand, Melanie; Travisano, Michael PLoS Genetics, Vol. 3, Issue 1 https://doi.org/10.1371/journal.pgen.0030015	journal	January 2007
Resistance, resilience, and redundancy in microbial communities Allison, S. D.; Martiny, J. B. H. Proceedings of the National Academy of Sciences, Vol. 105, Issue Supplement 1 https://doi.org/10.1073/pnas.0801925105	journal	August 2008
Density Dependence and Cooperation: Theory and a test with Bacteria Ross-Gillespie, Adin; Gardner, Andy; Buckling, Angus Evolution, Vol. 63, Issue 9 https://doi.org/10.1111/j.1558-5646.2009.00723.x	journal	September 2009
Thermodynamics-based design of microbial cell factories for anaerobic product formation Cueto-Rojas, Hugo F.; van Maris, A. J. A.; Wahl, S. Aljoscha Trends in Biotechnology, Vol. 33, Issue 9 https://doi.org/10.1016/j.tibtech.2015.06.010	journal	September 2015
The sociobiology of biofilms Nadell, Carey D.; Xavier, Joao B.; Foster, Kevin R. FEMS Microbiology Reviews, Vol. 33, Issue 1 https://doi.org/10.1111/j.1574-6976.2008.00150.x	journal	January 2009
A bacterium that degrades and assimilates poly(ethylene terephthalate) Yoshida, Shosuke; Hiraga, Kazumi; Takehana, Toshihiko Science, Vol. 351, Issue 6278 https://doi.org/10.1126/science.aad6359	journal	March 2016
Cellobiose Dehydrogenase – A Flavocytochrome from Wood-Degrading, Phytopathogenic and Saprotropic Fungi Zamocky, Marcel; Ludwig, R.; Peterbauer, C. Current Protein & Peptide Science, Vol. 7, Issue 3 https://doi.org/10.2174/138920306777452367	journal	June 2006
Sex Bias in Graduate Admissions: Data from Berkeley Bickel, P. J.; Hammel, E. A.; O'Connell, J. W. Science, Vol. 187, Issue 4175 https://doi.org/10.1126/science.187.4175.398	journal	February 1975
Metabolic modelling in a dynamic evolutionary framework predicts adaptive diversification of bacteria in a long-term evolution experiment Großkopf, Tobias; Consuegra, Jessika; Gaffé, Joël BMC Evolutionary Biology, Vol. 16, Issue 1 https://doi.org/10.1186/s12862-016-0733-x	journal	August 2016
Microbial catabolic activities are naturally selected by metabolic energy harvest rate González-Cabaleiro, Rebeca; Ofiţeru, Irina D.; Lema, Juan M. The ISME Journal, Vol. 9, Issue 12 https://doi.org/10.1038/ismej.2015.69	journal	July 2015
Methanogenic biodegradation of two-ringed polycyclic aromatic hydrocarbons Berdugo-Clavijo, Carolina; Dong, Xiaoli; Soh, Jung FEMS Microbiology Ecology, Vol. 81, Issue 1 https://doi.org/10.1111/j.1574-6941.2012.01328.x	journal	March 2012
How Do Microbial Extracellular Enzymes Locate and Degrade Natural and Synthetic Polymers in Soil Burns, Richard G. Molecular Environmental Soil Science at the Interfaces in the Earth’s Critical Zone https://doi.org/10.1007/978-3-642-05297-2_85	book	January 2010
The Plate Debate: Cultivable communities have no utility in contemporary environmental microbial ecology: The plate debate Ritz, Karl FEMS Microbiology Ecology, Vol. 60, Issue 3 https://doi.org/10.1111/j.1574-6941.2007.00331.x	journal	June 2007
Synthetic Ecology of Microbes: Mathematical Models and Applications Zomorrodi, Ali R.; Segrè, Daniel Journal of Molecular Biology, Vol. 428, Issue 5 https://doi.org/10.1016/j.jmb.2015.10.019	journal	February 2016
Phenotypic plasticity of a cooperative behaviour in bacteria KÜMmerli, R.; Jiricny, N.; Clarke, L. S. Journal of Evolutionary Biology, Vol. 22, Issue 3 https://doi.org/10.1111/j.1420-9101.2008.01666.x	journal	March 2009
Migration and horizontal gene transfer divide microbial genomes into multiple niches Niehus, Rene; Mitri, Sara; Fletcher, Alexander G. Nature Communications, Vol. 6, Issue 1 https://doi.org/10.1038/ncomms9924	journal	November 2015
Overflow metabolism in Escherichia coli results from efficient proteome allocation Basan, Markus; Hui, Sheng; Okano, Hiroyuki Nature, Vol. 528, Issue 7580 https://doi.org/10.1038/nature15765	journal	December 2015
The genome sequence of Desulfatibacillum alkenivorans AK-01: a blueprint for anaerobic alkane oxidation: Genome sequence of Desulfatibacillum alkenivorans AK-01 Callaghan, A. V.; Morris, B. E. L.; Pereira, I. A. C. Environmental Microbiology, Vol. 14, Issue 1 https://doi.org/10.1111/j.1462-2920.2011.02516.x	journal	June 2011
Eco-evolutionary dynamics of complex social strategies in microbial communities Harrington, Kyle I.; Sanchez, Alvaro Communicative & Integrative Biology, Vol. 7, Issue 1 https://doi.org/10.4161/cib.28230	journal	January 2014
Degradation of phenol via carboxylation to benzoate by a defined, obligate syntrophic consortium of anaerobic bacteria Knoll, Gertrud; Winter, Josef Applied Microbiology and Biotechnology, Vol. 30, Issue 3 https://doi.org/10.1007/BF00256225	journal	March 1989
Physiological heterogeneities in microbial populations and implications for physical stress tolerance Carlquist, Magnus; Fernandes, Rita; Helmark, Søren Microbial Cell Factories, Vol. 11, Issue 1 https://doi.org/10.1186/1475-2859-11-94	journal	January 2012
The thermodynamics and kinetics of microbial metabolism Jin, Q.; Bethke, C. M. American Journal of Science, Vol. 307, Issue 4 https://doi.org/10.2475/04.2007.01	journal	April 2007
Sociobiology of the Myxobacteria Velicer, Gregory J.; Vos, Michiel Annual Review of Microbiology, Vol. 63, Issue 1 https://doi.org/10.1146/annurev.micro.091208.073158	journal	October 2009
Five Rules for the Evolution of Cooperation Nowak, M. A. Science, Vol. 314, Issue 5805 https://doi.org/10.1126/science.1133755	journal	December 2006
The interplay between relatedness and horizontal gene transfer drives the evolution of plasmid-carried public goods Mc Ginty, Sorcha É.; Lehmann, Laurent; Brown, Sam P. Proceedings of the Royal Society B: Biological Sciences, Vol. 280, Issue 1761 https://doi.org/10.1098/rspb.2013.0400	journal	June 2013
Overflow Metabolism in Escherichia coli during Steady-State Growth: Transcriptional Regulation and Effect of the Redox Ratio Vemuri, G. N.; Altman, E.; Sangurdekar, D. P. Applied and Environmental Microbiology, Vol. 72, Issue 5 https://doi.org/10.1128/AEM.72.5.3653-3661.2006	journal	May 2006
Simple constrained-optimization view of acetate overflow inE. coli Majewski, R. A.; Domach, M. M. Biotechnology and Bioengineering, Vol. 35, Issue 7 https://doi.org/10.1002/bit.260350711	journal	March 1990
Privatization of cooperative benefits stabilizes mutualistic cross-feeding interactions in spatially structured environments Pande, Samay; Kaftan, Filip; Lang, Stefan The ISME Journal, Vol. 10, Issue 6 https://doi.org/10.1038/ismej.2015.212	journal	December 2015
Challenges in microbial ecology: building predictive understanding of community function and dynamics Widder, Stefanie; Allen, Rosalind J.; Pfeiffer, Thomas The ISME Journal, Vol. 10, Issue 11 https://doi.org/10.1038/ismej.2016.45	journal	March 2016
Ecological study of a bioaugmentation failure Environmental Microbiology, Vol. 2, Issue 2 https://doi.org/10.1046/j.1462-2920.2000.00091.x	journal	April 2000
Microbial diversity arising from thermodynamic constraints Großkopf, Tobias; Soyer, Orkun S. The ISME Journal, Vol. 10, Issue 11 https://doi.org/10.1038/ismej.2016.49	journal	April 2016
Plasticity facilitates sustainable growth in the commons Cavaliere, Matteo; Poyatos, Juan F. Journal of The Royal Society Interface, Vol. 10, Issue 81 https://doi.org/10.1098/rsif.2012.1006	journal	April 2013
A practical kinetic model that considers endproduct inhibition in anaerobic digestion processes by including the equilibrium constant Hoh, C. Y.; Cord-Ruwisch, R. Biotechnology and Bioengineering, Vol. 51, Issue 5 https://doi.org/10.1002/(SICI)1097-0290(19960905)51:5<597::AID-BIT12>3.0.CO;2-F	journal	September 1996
Starch and Microbial α-Amylases: From Concepts to Biotechnological Applications El-Fallal, Amira; Dobara, Mohammed Abou; El-Sayed, Ahmed Carbohydrates - Comprehensive Studies on Glycobiology and Glycotechnology https://doi.org/10.5772/51571	book	November 2012
A model for the evolutionary dynamics of cross-feeding polymorphisms in microorganisms Doebeli, M. Population Ecology, Vol. 44, Issue 2 https://doi.org/10.1007/s101440200008	journal	August 2002
Physiological responses to mixing in large scale bioreactors Enfors, S. -O.; Jahic, M.; Rozkov, A. Journal of Biotechnology, Vol. 85, Issue 2 https://doi.org/10.1016/S0168-1656(00)00365-5	journal	February 2001
Phenotype Fingerprinting Suggests the Involvement of Single-Genotype Consortia in Degradation of Aromatic Compounds by Rhodopseudomonas palustris Karpinets, Tatiana V.; Pelletier, Dale A.; Pan, Chongle PLoS ONE, Vol. 4, Issue 2 https://doi.org/10.1371/journal.pone.0004615	journal	February 2009
Feedback between Population and Evolutionary Dynamics Determines the Fate of Social Microbial Populations Sanchez, Alvaro; Gore, Jeff PLoS Biology, Vol. 11, Issue 4 https://doi.org/10.1371/journal.pbio.1001547	journal	April 2013
Cheaters, diffusion and nutrients constrain decomposition by microbial enzymes in spatially structured environments: Constraints on enzymatic decomposition Allison, Steven D. Ecology Letters, Vol. 8, Issue 6 https://doi.org/10.1111/j.1461-0248.2005.00756.x	journal	April 2005
Rapid radiation in bacteria leads to a division of labour Kim, Wook; Levy, Stuart B.; Foster, Kevin R. Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms10508	journal	February 2016
The Newest Synthesis: Understanding the Interplay of Evolutionary and Ecological Dynamics Schoener, T. W. Science, Vol. 331, Issue 6016 https://doi.org/10.1126/science.1193954	journal	January 2011

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