Defining Division of Labor in Microbial Communities
Abstract
In order to survive and reproduce, organisms must perform a multitude of tasks. However, trade-offs limit their ability to allocate energy and resources to all of these different processes. One strategy to solve this problem is to specialize in some traits and team up with other organisms that can help by providing additional, complementary functions. By reciprocally exchanging metabolites and/or services in this way, both parties benefit from the interaction. This phenomenon, which has been termed functional specialization or division of labor, is very common in nature and exists on all levels of biological organization. Also, microorganisms have evolved different types of synergistic interactions. However, very often, it remains unclear whether or not a given example represents a true case of division of labor. Here we aim at filling this gap by providing a list of criteria that clearly define division of labor in microbial communities. Furthermore, we propose a set of diagnostic experiments to verify whether a given interaction fulfills these conditions. In contrast to the common use of the term, our analysis reveals that both intraspecific and interspecific interactions meet the criteria defining division of labor. Moreover, our analysis identified non-cooperators of intraspecific public goods interactions as growth specialists that divide labor with conspecific producers, rather than being social parasites. By providing a conceptual toolkit, our work will help to unambiguously identify cases of division of labor and stimulate more detailed investigations of this important and widespread type of inter-microbial interaction.
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Cell-to-cell heterogeneity has important implications, allowing populations of cells to diversify to survive environmental stress, according to the proposed theory of division of labor.
“Thus, cell-to-cell heterogeneity has important implications, allowing populations of cells to diversify to survive environmental stress, according to the proposed theory of division of labor [33,34].”
From Microbiota of Cheese Ecosystems: A Perspective on Cheesemaking (2025) · cites this paper as [33]
Cites
Axelrod, R., & Hamilton, W. D. (1981) · Science · doi:10.1126/science.7466396 · Cited by 20,065 · see citing works
The genetical evolution of social behaviour. I
Hamilton, W. D. (1964) · Journal of Theoretical Biology · doi:10.1016/0022-5193(64)90038-4 · Cited by 15,725 · see citing works
The Evolution of Reciprocal Altruism
Trivers, R. L. (1971) · The Quarterly Review of Biology · doi:10.1086/406755 · Cited by 11,010 · see citing works
Bacterial biofilms: from the Natural environment to infectious diseases
Hall‐Stoodley, L., Costerton, J. W., & Stoodley, P. (2004) · Nature Reviews Microbiology · doi:10.1038/nrmicro821 · Cited by 7,133 · see citing works
Stochastic Gene Expression in a Single Cell
Elowitz, M. B., Levine, A. J., Siggia, E. D., & Swain, P. S. (2002) · Science · doi:10.1126/science.1070919 · Cited by 5,441 · see citing works
The genetical evolution of social behaviour. II
Hamilton, W. D. O. (1964) · Journal of Theoretical Biology · doi:10.1016/0022-5193(64)90039-6 · Cited by 4,158 · see citing works
Antibiotic resistance of bacterial biofilms
Høiby, N., Bjarnsholt, T., Givskov, M., Molin, S., & Ciofu, O. (2010) · International Journal of Antimicrobial Agents · doi:10.1016/j.ijantimicag.2009.12.011 · Cited by 3,238 · see citing works
A principle of natural self-organization: Part A: Emergence of the hypercycle
Eigen, M., & Schuster, P. (1977) · Naturwissenschaften · doi:10.1007/bf00450633 · Cited by 1,752 · see citing works
Regulation of noise in the expression of a single gene
Özbudak, E. M., Thattai, M., Kurtser, I., Grossman, A. D., & van Oudenaarden, A. (2002) · Nature Genetics · doi:10.1038/ng869 · Cited by 1,559 · see citing works
Algae acquire vitamin B12 through a symbiotic relationship with bacteria
Croft, M. T., Lawrence, A. D., Raux-Deery, E., Warren, M. J., & Smith, A. G. (2005) · Nature · doi:10.1038/nature04056 · Cited by 1,536 · see citing works
Nowak, M. A., Tarnita, C. E., & Wilson, E. O. (2010) · Nature · doi:10.1038/nature09205 · Cited by 1,483 · see citing works
Gessner, M. O., Swan, C. M., Dang, C. K., McKie, B. G., Bardgett, R. D., Wall, D. H., & Hättenschwiler, S. (2010) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2010.01.010 · Cited by 1,335 · see citing works
Turning a hobby into a job: How duplicated genes find new functions
Conant, G. C., & Wolfe, K. H. (2008) · Nature Reviews Genetics · doi:10.1038/nrg2482 · Cited by 1,281 · see citing works
The Black Queen Hypothesis: Evolution of Dependencies through Adaptive Gene Loss
Morris, J., Lenski, R. E., & Zinser, E. R. (2012) · mBio · doi:10.1128/mbio.00036-12 · Cited by 1,212 · see citing works
Social evolution theory for microorganisms
West, S. A., Griffin, A. S., Gardner, A., & Diggle, S. P. (2006) · Nature Reviews Microbiology · doi:10.1038/nrmicro1461 · Cited by 1,183 · see citing works
Cooperation and competition in pathogenic bacteria
Griffin, A. S., West, S. A., & Buckling, A. (2004) · Nature · doi:10.1038/nature02744 · Cited by 1,104 · see citing works
Evolutionary Explanations for Cooperation
West, S. A., Griffin, A. S., & Gardner, A. (2007) · Current Biology · doi:10.1016/j.cub.2007.06.004 · Cited by 1,010 · see citing works
Biogeography of a human oral microbiome at the micron scale
Mark Welch, J. L., Rossetti, B. J., Rieken, C. W., Dewhirst, F. E., & Borisy, G. G. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1522149113 · Cited by 968 · see citing works
Metabolic dependencies drive species co-occurrence in diverse microbial communities
Zelezniak, A., Andrejev, S., Ponomarova, O., Mende, D. R., Bork, P., & Patil, K. R. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1421834112 · Cited by 930 · see citing works
A functional perspective on phenotypic heterogeneity in microorganisms
Ackermann, M. (2015) · Nature Reviews Microbiology · doi:10.1038/nrmicro3491 · Cited by 922 · see citing works
Microbial syntrophy: interaction for the common good
Morris, B. E. L., Henneberger, R. M., Huber, H., & Moissl‐Eichinger, C. (2013) · FEMS Microbiology Reviews · doi:10.1111/1574-6976.12019 · Cited by 918 · see citing works
Thinking about Bacterial Populations as Multicellular Organisms
Shapiro, J. A. (1998) · Annual Review of Microbiology · doi:10.1146/annurev.micro.52.1.81 · Cited by 876 · see citing works
Cooperation and conflict in quorum-sensing bacterial populations
Diggle, S. P., Griffin, A. S., Campbell, G. S., & West, S. A. (2007) · Nature · doi:10.1038/nature06279 · Cited by 824 · see citing works
The evolution of cooperation and altruism – a general framework and a classification of models
Lehmann, L., & Keller, L. (2006) · Journal of Evolutionary Biology · doi:10.1111/j.1420-9101.2006.01119.x · Cited by 801 · see citing works
The evolution of mutualisms: exploring the paths between conflict and cooperation
Herre, E. A., Knowlton, N., MUELLER, U., & REHNER, S. (1999) · Trends in Ecology & Evolution · doi:10.1016/s0169-5347(98)01529-8 · Cited by 798 · see citing works
West, S. A., Diggle, S. P., Buckling, A. G. J., Gardner, A., & Griffin, A. S. (2007) · Annual Review of Ecology Evolution and Systematics · doi:10.1146/annurev.ecolsys.38.091206.095740 · Cited by 679 · see citing works
How context dependent are species interactions?
Chamberlain, S., Bronstein, J. L., & Rudgers, J. A. (2014) · Ecology Letters · doi:10.1111/ele.12279 · Cited by 674 · see citing works
Snowdrift game dynamics and facultative cheating in yeast
Gore, J., Youk, H., & van Oudenaarden, A. (2009) · Nature · doi:10.1038/nature07921 · Cited by 653 · see citing works
Shifts in growth strategies reflect tradeoffs in cellular economics
Molenaar, D., van Berlo, R., de Ridder, D., & Teusink, B. (2009) · Molecular Systems Biology · doi:10.1038/msb.2009.82 · Cited by 653 · see citing works
Bacterial charity work leads to population-wide resistance
Lee, H. H., Molla, M. N., Cantor, C. R., & Collins, J. J. (2010) · Nature · doi:10.1038/nature09354 · Cited by 638 · see citing works
The evolution of cooperation within the gut microbiota
Rakoff-Nahoum, S., Foster, K. R., & Comstock, L. E. (2016) · Nature · doi:10.1038/nature17626 · Cited by 616 · see citing works
Evolution of cooperation and conflict in experimental bacterial populations
Rainey, P. B., & Rainey, K. (2003) · Nature · doi:10.1038/nature01906 · Cited by 568 · see citing works
Bacterial Communities: Interactions to Scale
Stubbendieck, R. M., Vargas-Bautista, C., & Straight, P. D. (2016) · Frontiers in Microbiology · doi:10.3389/fmicb.2016.01234 · Cited by 562 · see citing works
Ecology and evolution of metabolic cross-feeding interactions in bacteria
D’Souza, G. G., Shitut, S., Preußger, D., Yousif, G., Waschina, S., & Kost, C. (2018) · Natural Product Reports · doi:10.1039/c8np00009c · Cited by 556 · see citing works
Expanded metabolic versatility of ubiquitous nitrite-oxidizing bacteria from the genus Nitrospira
Koch, H., Lücker, S., Albertsen, M., Kitzinger, K., Herbold, C. W., Spieck, E., Nielsen, P. H., Wagner, M., & Daims, H. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1506533112 · Cited by 551 · see citing works
Interactions in multispecies biofilms: do they actually matter?
Burmølle, M., Ren, D., Bjarnsholt, T., & Sørensen, S. J. (2014) · Trends in Microbiology · doi:10.1016/j.tim.2013.12.004 · Cited by 544 · see citing works
The β-lactamases of Gram-negative bacteria and their rôle in resistance to β-lactam antibiotics
SYKES, R. B., & Matthew, M. (1976) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/2.2.115 · Cited by 536 · see citing works
Glycolytic strategy as a tradeoff between energy yield and protein cost
Flamholz, A., Noor, E., Bar-Even, A., Liebermeister, W., & Milo, R. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1215283110 · Cited by 531 · see citing works
Microbial Cell Individuality and the Underlying Sources of Heterogeneity
Avery, S. V. (2006) · Nature Reviews Microbiology · doi:10.1038/nrmicro1460 · Cited by 521 · see citing works
The population genetics of ecological specialization in evolving Escherichia coli populations
Cooper, V. S., & Lenski, R. E. (2000) · Nature · doi:10.1038/35037572 · Cited by 519 · see citing works
Distinguishing mechanisms for the evolution of co-operation
Bull, J. J., & Rice, W. R. (1991) · Journal of Theoretical Biology · doi:10.1016/s0022-5193(05)80072-4 · Cited by 519 · see citing works
The evolutionary consequences of erroneous protein synthesis
Allan Drummond, D., & Wilke, C. O. (2009) · Nature Reviews Genetics · doi:10.1038/nrg2662 · Cited by 515 · see citing works
Cyanobacterial HeterocystsPreprint
Kumar, K. P., Mella-Herrera, R. A., & Golden, J. W. (2010) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a000315 · Cited by 511 · see citing works
Altruism and social cheating in the social amoeba Dictyostelium discoideum
Strassmann, J. E., Zhu, Y. Q., & Queller, D. C. (2000) · Nature · doi:10.1038/35050087 · Cited by 509 · see citing works
Xu, K. D., Stewart, P. S., Xia, F., Huang, C., & McFeters, G. A. (1998) · Applied and Environmental Microbiology · doi:10.1128/aem.64.10.4035-4039.1998 · Cited by 501 · see citing works
Eating For Two: How Metabolism Establishes Interspecies Interactions in the Gut
Fischbach, M. A., & Sonnenburg, J. L. (2011) · Cell Host & Microbe · doi:10.1016/j.chom.2011.10.002 · Cited by 494 · see citing works
Why is metabolic labour divided in nitrification?
Costa, E., Pérez, J., & Kreft, J. (2006) · Trends in Microbiology · doi:10.1016/j.tim.2006.03.006 · Cited by 487 · see citing works
López‐Mondéjar, R., Zühlke, D., Becher, D., Riedel, K., & Baldrián, P. (2016) · Scientific Reports · doi:10.1038/srep25279 · Cited by 484 · see citing works
Defined spatial structure stabilizes a synthetic multispecies bacterial community
Kim, H. J., Boedicker, J. Q., Choi, J. W., & Ismagilov, R. F. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0807935105 · Cited by 481 · see citing works
Bacterial solutions to multicellularity: a tale of biofilms, filaments and fruiting bodies
Claessen, D., Rozen, D. E., Kuipers, O. P., Søgaard‐Andersen, L., & van Wezel, G. P. (2014) · Nature Reviews Microbiology · doi:10.1038/nrmicro3178 · Cited by 476 · see citing works
Evolutionary tipping points in the capacity to adapt to environmental change
Botero, C. A., Weissing, F. J., WRIGHT, J. M., & Rubenstein, D. R. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1408589111 · Cited by 475 · see citing works
Maurelli, A. T., Fernández, R. E., Bloch, C. A., Rode, C. K., & Fasano, A. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.7.3943 · Cited by 457 · see citing works
Siderophores from Neighboring Organisms Promote the Growth of Uncultured Bacteria
Donofrio, A. E., Crawford, J. M., Stewart, E. J., Witt, K., Gavrish, E., Epstein, S. S., Clardy, J., & Lewis, K. (2010) · Chemistry & Biology · doi:10.1016/j.chembiol.2010.02.010 · Cited by 457 · see citing works
Modifying and reacting to the environmental pH can drive bacterial interactions
Ratzke, C., & Gore, J. (2018) · PLoS Biology · doi:10.1371/journal.pbio.2004248 · Cited by 456 · see citing works
Synthetic cooperation in engineered yeast populations
Shou, W., Ram, S., & Vilar, J. M. G. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0610575104 · Cited by 454 · see citing works
Compartmentalized function through cell differentiation in filamentous cyanobacteria
Flores, E., & Herrero, A. (2009) · Nature Reviews Microbiology · doi:10.1038/nrmicro2242 · Cited by 448 · see citing works
Metabolic Complementarity and Genomics of the Dual Bacterial Symbiosis of Sharpshooters
Wu, D., Daugherty, S. C., Aken, S. E. V., Pai, G., Watkins, K. L., Khouri, H. M., Tallon, L. J., Zaborsky, J., Dunbar, H. E., Tran, P. L., et al. (2006) · PLoS Biology · doi:10.1371/journal.pbio.0040188 · Cited by 443 · see citing works
Meeks, J. C., & Elhai, J. (2002) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.66.1.94-121.2002 · Cited by 429 · see citing works
Self-destructive cooperation mediated by phenotypic noise
Ackermann, M., Stecher, B., Freed, N. E., Songhet, P., Hardt, W., & Doebeli, M. (2008) · Nature · doi:10.1038/nature07067 · Cited by 420 · see citing works
Metabolic niche of a prominent sulfate-reducing human gut bacterium
Rey, F. E., Gonzalez, M. D., Cheng, J., Wu, M., Ahern, P. P., & Gordon, J. I. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1312524110 · Cited by 412 · see citing works
An Ecological Network of Polysaccharide Utilization among Human Intestinal Symbionts
Rakoff-Nahoum, S., Coyne, M. J., & Comstock, L. E. (2013) · Current Biology · doi:10.1016/j.cub.2013.10.077 · Cited by 410 · see citing works
Wheeler, W. M. (1911) · Journal of Morphology · doi:10.1002/jmor.1050220206 · Cited by 388 · see citing works
Genetic and genomic analyses of the division of labour in insect societies
Smith, C. R., Toth, A. L., Suarez, A. V., & Robinson, G. E. (2008) · Nature Reviews Genetics · doi:10.1038/nrg2429 · Cited by 371 · see citing works
Rosenzweig, R. F., Sharp, R. R., Treves, D. S., & Adams, J. (1994) · Genetics · doi:10.1093/genetics/137.4.903 · Cited by 357 · see citing works
Production of NO and N2O by soil nitrifying bacteria
Lipschultz, F., Zafiriou, O. C., Wofsy, S. C., McElroy, M. B., Valois, F. W., & Watson, S. W. (1981) · Nature · doi:10.1038/294641a0 · Cited by 354 · see citing works
A twelve-step program for evolving multicellularity and a division of labor
Kirk, D. L. (2005) · BioEssays · doi:10.1002/bies.20197 · Cited by 345 · see citing works
Field, J. A., Stams, A. J. M., Kato, M. T., & Schraa, G. (1995) · Antonie van Leeuwenhoek · doi:10.1007/bf00872195 · Cited by 341 · see citing works
Cordero, O. X., Ventouras, L.-A., DeLong, E. F., & Polz, M. F. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1213344109 · Cited by 334 · see citing works
Evolution of individuality during the transition from unicellular to multicellular life
Michod, R. E. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0701489104 · Cited by 334 · see citing works
Developmental cheating in the social bacterium Myxococcus xanthus
Velicer, G. J., Kroos, L., & Lenski, R. E. (2000) · Nature · doi:10.1038/35007066 · Cited by 333 · see citing works
Frequency-dependent selection in bacterial populations
Levin, B. R. (1988) · Philosophical transactions of the Royal Society of London. Series B, Biological sciences · doi:10.1098/rstb.1988.0059 · Cited by 328 · see citing works
Fitness and stability of obligate cross-feeding interactions that emerge upon gene loss in bacteria
Pande, S., Merker, H., Bohl, K., Reichelt, M., Schuster, S., de Figueiredo, L. F., Kaleta, C., & Kost, C. (2013) · The ISME Journal · doi:10.1038/ismej.2013.211 · Cited by 321 · see citing works
Enhanced bioremediation of oil spills in the sea
Ron, E. Z., & ROSENBERG, E. B. (2014) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2014.02.004 · Cited by 301 · see citing works
Metabolic division of labor in microbial systems
Tsoi, R., Wu, F., Zhang, C., Bewick, S. A., Karig, D., & You, L. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1716888115 · Cited by 298 · see citing works
Cheating and the evolutionary stability of mutualisms
Ferrière, R., Bronstein, J., Rinaldi, S., Law, R., & Gauduchon, M. (2002) · Proceedings of the Royal Society of London. Series B: Biological Sciences · doi:10.1098/rspb.2001.1900 · Cited by 296 · see citing works
Frequency Dependence and Cooperation: Theory and a Test with Bacteria
Ross‐Gillespie, A., Gardner, A., West, S. A., & Griffin, A. S. (2007) · The American Naturalist · doi:10.1086/519860 · Cited by 292 · see citing works
Resource competition and social conflict in experimental populations of yeast
MacLean, R. C., & Gudelj, I. (2006) · Nature · doi:10.1038/nature04624 · Cited by 285 · see citing works
Bacterial Adaptation through Loss of Function
Hottes, A. K., Freddolino, L., Khare, A., Donnell, Z. N., Liu, J. C., & Tavazoie, S. (2013) · PLoS Genetics · doi:10.1371/journal.pgen.1003617 · Cited by 270 · see citing works
NOVEL COOPERATION EXPERIMENTALLY EVOLVED BETWEEN SPECIES
Harcombe, W. R. (2010) · Evolution · doi:10.1111/j.1558-5646.2010.00959.x · Cited by 267 · see citing works
Stable Coexistence of Five Bacterial Strains as a Cellulose-Degrading Community
Kato, S., Haruta, S., Cui, Z. J., Ishii, M., & Igarashi, Y. (2005) · Applied and Environmental Microbiology · doi:10.1128/aem.71.11.7099-7106.2005 · Cited by 265 · see citing works
Strategies of microbial cheater control
Travisano, M., & Velicer, G. J. (2004) · Trends in Microbiology · doi:10.1016/j.tim.2003.12.009 · Cited by 265 · see citing works
Networks of energetic and metabolic interactions define dynamics in microbial communities
Embree, M., Liu, J. K., Al-Bassam, M. M., & Zengler, K. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1506034112 · Cited by 256 · see citing works
Rapid evolution of stability and productivity at the origin of a microbial mutualism
Hillesland, K. L., & Stahl, D. A. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0908456107 · Cited by 254 · see citing works
Hazan, R., & Engelberg–Kulka, H. (2004) · Molecular Genetics and Genomics · doi:10.1007/s00438-004-1048-y · Cited by 248 · see citing works
Syntrophic biodegradation of hydrocarbon contaminants
Gieg, L. M., Fowler, J., & Berdugo‐Clavijo, C. (2013) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2013.09.002 · Cited by 248 · see citing works
Morishita, T., Deguchi, Y., YAJIMA, M., Sakurai, T., & Yura, T. (1981) · Journal of Bacteriology · doi:10.1128/jb.148.1.64-71.1981 · Cited by 246 · see citing works
Patowary, K., Patowary, R., Kalita, M. C., & Deka, S. (2016) · Frontiers in Microbiology · doi:10.3389/fmicb.2016.01092 · Cited by 245 · see citing works
van Gestel, J., Weissing, F. J., Kuipers, O. P., & Kovács, Á. T. (2014) · The ISME Journal · doi:10.1038/ismej.2014.52 · Cited by 240 · see citing works
Division of Labor during Biofilm Matrix Production
Dragoš, A., Kiesewalter, H. T., Martin, M., Hsu, C.-Y., Hartmann, R., Wechsler, T., Eriksen, C., Brix, S., Drescher, K., Stanley‐Wall, N. R., et al. (2018) · Current Biology · doi:10.1016/j.cub.2018.04.046 · Cited by 236 · see citing works
Selection-Driven Gene Loss in Bacteria
Koskiniemi, S., Sun, S., Berg, O. G., & Andersson, D. I. (2012) · PLoS Genetics · doi:10.1371/journal.pgen.1002787 · Cited by 232 · see citing works
From Cell Differentiation to Cell Collectives: Bacillus subtilis Uses Division of Labor to Migrate
van Gestel, J., Vlamakis, H. C., & Kolter, R. (2015) · PLoS Biology · doi:10.1371/journal.pbio.1002141 · Cited by 221 · see citing works
Trade-off Mechanisms Shaping the Diversity of Bacteria
Ferenci, T. (2015) · Trends in Microbiology · doi:10.1016/j.tim.2015.11.009 · Cited by 220 · see citing works
An Evolutionary Perspective on Self-Organized Division of Labor in Social Insects
Duarte, A., Weissing, F. J., Pen, I. R., & Keller, L. (2011) · Annual Review of Ecology Evolution and Systematics · doi:10.1146/annurev-ecolsys-102710-145017 · Cited by 216 · see citing works
The Relative Importance of Competition and Predation Varies with Productivity in a Model Community
Bohannan, B. J. M., & Lenski, R. E. (2000) · The American Naturalist · doi:10.1086/303393 · Cited by 210 · see citing works
Sieuwerts, S., Douwe Molenaar, B., van Hijum, S. A. F. T., Beerthuyzen, M. M., Stevens, M. J. A., Janssen, P. W. M., Ingham, C. J., de Bok, F. A. M., de Vos, W. M., & Vlieg, J. E. T. V. H. (2010) · Applied and Environmental Microbiology · doi:10.1128/aem.01122-10 · Cited by 209 · see citing works
Environmental and genetic modulation of the phenotypic expression of antibiotic resistance
Hughes, D., & Andersson, D. I. (2017) · FEMS Microbiology Reviews · doi:10.1093/femsre/fux004 · Cited by 207 · see citing works
Cooperation, competition and antibiotic resistance in bacterial colonies
Frost, I., Smith, W. P. J., Mitri, S., Millán, Á. S., Davit, Y., Osborne, J. M., Pitt‐Francis, J., MacLean, R. C., & Foster, K. R. (2018) · The ISME Journal · doi:10.1038/s41396-018-0090-4 · Cited by 200 · see citing works
Modular Assembly of Polysaccharide-Degrading Marine Microbial Communities
Enke, T. N., Datta, M. S., Schwartzman, J. A., Cermak, N., Schmitz, D. A., Barrere, J., Pascual‐García, A., & Cordero, O. X. (2019) · Current Biology · doi:10.1016/j.cub.2019.03.047 · Cited by 197 · see citing works
Division of Labor in Biofilms: the Ecology of Cell Differentiation
van Gestel, J., Vlamakis, H. C., & Kolter, R. (2015) · Microbiology Spectrum · doi:10.1128/microbiolspec.mb-0002-2014 · Cited by 195 · see citing works
Cooperation and virulence in acute Pseudomonas aeruginosainfections
Harrison, F., Browning, L. E., Vos, M., & Buckling, A. G. J. (2006) · BMC Biology · doi:10.1186/1741-7007-4-21 · Cited by 191 · see citing works
Pande, S., Kaftan, F., Lang, S. N., Svatoš, A., Germerodt, S., & Kost, C. (2015) · The ISME Journal · doi:10.1038/ismej.2015.212 · Cited by 188 · see citing works
Mycobacterial mistranslation is necessary and sufficient for rifampicin phenotypic resistance
Javid, B., Sorrentino, F., Toosky, M., Zheng, W., Pinkham, J. T., Jain, N. K., Pan, M., Deighan, P., & Rubin, E. J. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1317580111 · Cited by 188 · see citing works
Peyraud, R., Cottret, L., Marmiesse, L., Gouzy, J., & Genin, S. (2016) · PLoS Pathogens · doi:10.1371/journal.ppat.1005939 · Cited by 181 · see citing works
Division of labour in microorganisms: an evolutionary perspective
West, S. A., & Cooper, G. A. (2016) · Nature Reviews Microbiology · doi:10.1038/nrmicro.2016.111 · Cited by 180 · see citing works
Heterogeneity in surface sensing suggests a division of labor in Pseudomonas aeruginosa populations
Armbruster, C. R., Lee, C. K., Parker-Gilham, J., de Anda, J., Xia, A., Zhao, K., Murakami, K., Tseng, B. S., Hoffman, L. R., Jin, F., et al. (2019) · eLife · doi:10.7554/elife.45084 · Cited by 178 · see citing works
Repeated, Selection-Driven Genome Reduction of Accessory Genes in Experimental Populations
Lee, M.-C., & Marx, C. J. (2012) · PLoS Genetics · doi:10.1371/journal.pgen.1002651 · Cited by 177 · see citing works
From division of labor to the collective behavior of social insects
Gordon, D. M. (2015) · Behavioral Ecology and Sociobiology · doi:10.1007/s00265-015-2045-3 · Cited by 171 · see citing works
Organization of the Prokaryotic Genome
(1999) · ASM Press eBooks · doi:10.1128/9781555818180 · Cited by 170 · see citing works
Bachmann, H., Starrenburg, M. J. C., Molenaar, D., Kleerebezem, M., & van Hylckama Vlieg, J. E. T. (2012) · Genome Research · doi:10.1101/gr.121285.111 · Cited by 170 · see citing works
Evolution of functional specialization and division of labor
Rueffler, C., Hermisson, J., & Wagner, G. P. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1110521109 · Cited by 168 · see citing works
Stadie, J., Gulitz, A., Ehrmann, M. A., & Vogel, R. F. (2013) · Food Microbiology · doi:10.1016/j.fm.2013.03.009 · Cited by 168 · see citing works
Bantinaki, E., Kassen, R., Cg, K., Robinson, Z., Spiers, A. J., & Rainey, P. B. (2007) · Genetics · doi:10.1534/genetics.106.069906 · Cited by 168 · see citing works
The evolution of a pleiotropic fitness tradeoff in Pseudomonas fluorescens
MacLean, R. C., Bell, G., & Rainey, P. B. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0307195101 · Cited by 162 · see citing works
Trade-offs and coexistence in microbial microcosms
Bohannan, B. J. M., Kerr, B., Jessup, C. M., Hughes, J. B., & Sandvik, G. (2002) · Antonie van Leeuwenhoek · doi:10.1023/a:1020585711378 · Cited by 161 · see citing works
Litchman, E., Edwards, K. F., & Klausmeier, C. A. (2015) · Frontiers in Microbiology · doi:10.3389/fmicb.2015.00254 · Cited by 160 · see citing works
Prospects for harnessing biocide resistance for bioremediation and detoxification
Atashgahi, S., Sánchez‐Andrea, I., Heipieper, H. J., van der Meer, J. R., Stams, A. J. M., & Smidt, H. (2018) · Science · doi:10.1126/science.aar3778 · Cited by 157 · see citing works
Heterocyst formation in cyanobacteria
Adams, D. G. (2000) · Current Opinion in Microbiology · doi:10.1016/s1369-5274(00)00150-8 · Cited by 147 · see citing works
Czárán, T., & Hoekstra, R. F. (2009) · PLoS ONE · doi:10.1371/journal.pone.0006655 · Cited by 147 · see citing works
Experimental Evolution of Metabolic Dependency in Bacteria
D’Souza, G. G., & Kost, C. (2016) · PLoS Genetics · doi:10.1371/journal.pgen.1006364 · Cited by 146 · see citing works
Interactions in a mixed bacterial population growing on methane in continuous culture
Wilkinson, T. G., Topiwala, H. H., & Hamer, G. (1974) · Biotechnology and Bioengineering · doi:10.1002/bit.260160105 · Cited by 145 · see citing works
Proteome reallocation in <i>Escherichia coli</i> with increasing specific growth rate
Peebo, K., Valgepea, K., Maser, A., Nahku, R., Adamberg, K., & Vilu, R. (2015) · Molecular BioSystems · doi:10.1039/c4mb00721b · Cited by 145 · see citing works
Paul, C., Mausz, M. A., & Pohnert, G. (2012) · Metabolomics · doi:10.1007/s11306-012-0453-1 · Cited by 142 · see citing works
Leiby, N., & Marx, C. J. (2014) · PLoS Biology · doi:10.1371/journal.pbio.1001789 · Cited by 141 · see citing works
Evolution of bidirectional costly mutualism from byproduct consumption
Harcombe, W. R., Chacón, J. M., Adamowicz, E. M., Chubiz, L. M., & Marx, C. J. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1810949115 · Cited by 137 · see citing works
The self-inhibitory nature of metabolic networks and its alleviation through compartmentalization
Alam, M. T., Olín‐Sandoval, V., Stincone, A., Keller, M. A., Zelezniak, A., Luisi, B. F., & Ralser, M. (2017) · Nature Communications · doi:10.1038/ncomms16018 · Cited by 136 · see citing works
Symbiosis: mechanisms and model systems
(2003) · Choice Reviews Online · doi:10.5860/choice.40-3390 · Cited by 136 · see citing works
Metabolic specialization and the assembly of microbial communities
Johnson, D. R., Goldschmidt, F., Lilja, E., & Ackermann, M. (2012) · The ISME Journal · doi:10.1038/ismej.2012.46 · Cited by 134 · see citing works
Multiple syntrophic interactions in a terephthalate-degrading methanogenic consortium
Lykidis, A., Chen, C.-L., Tringe, S. G., McHardy, A. C., Copeland, A., Kyrpides, N. C., Hugenholtz, P., Macarie, H., Olmos, A., Monroy, O., et al. (2010) · The ISME Journal · doi:10.1038/ismej.2010.125 · Cited by 134 · see citing works
Understanding microbial cooperation
Damore, J. A., & Gore, J. (2011) · Journal of Theoretical Biology · doi:10.1016/j.jtbi.2011.03.008 · Cited by 126 · see citing works
Evolutionary construction by staying together and coming together
Tarnita, C. E., Taubes, C. H., & Nowak, M. A. (2013) · Journal of Theoretical Biology · doi:10.1016/j.jtbi.2012.11.022 · Cited by 119 · see citing works
The group covariance effect and fitness trade-offs during evolutionary transitions in individuality
Michod, R. E. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0601080103 · Cited by 117 · see citing works
Pervasive Selection for Cooperative Cross-Feeding in Bacterial Communities
Germerodt, S., Bohl, K., Lück, A., Pande, S., Schroeter, A., Kaleta, C., Schuster, S., & Kost, C. (2016) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1004986 · Cited by 117 · see citing works
A Mixture of “Cheats” and “Co-Operators” Can Enable Maximal Group Benefit
MacLean, R. C., Fuentes-Hernández, A., Greig, D., Hurst, L. D., & Gudelj, I. (2010) · PLoS Biology · doi:10.1371/journal.pbio.1000486 · Cited by 115 · see citing works
The Evolutionary Origin of an Altruistic Gene
Nedelcu, A. M., & Michod, R. E. (2006) · Molecular Biology and Evolution · doi:10.1093/molbev/msl016 · Cited by 114 · see citing works
Dugatkin, L. A., Perlin, M. H., Lucas, J. S., & Atlas, R. (2004) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2004.2916 · Cited by 111 · see citing works
Metabolic interactions between dynamic bacterial subpopulations
Rosenthal, A. Z., Qi, Y., Hormoz, S., Park, J., Li, H., & Elowitz, M. B. (2018) · eLife · doi:10.7554/elife.33099 · Cited by 105 · see citing works
Optimal regulatory strategies for metabolic pathways in Escherichia coli depending on protein costs
Wessely, F., Bartl, M., Guthke, R., Li, P., Schuster, S., & Kaleta, C. (2011) · Molecular Systems Biology · doi:10.1038/msb.2011.46 · Cited by 103 · see citing works
‘Division of labour’ in response to host oxidative burst drives a fatal Cryptococcus gattii outbreak
Voelz, K., Johnston, S. A., Taylor-Smith, L. M., Hall, R. A., Idnurm, A., & May, R. C. (2014) · Nature Communications · doi:10.1038/ncomms6194 · Cited by 101 · see citing works
The dynamic genetic repertoire of microbial communities
Wilmes, P., Simmons, S. L., Denef, V. J., & Banfield, J. F. (2008) · FEMS Microbiology Reviews · doi:10.1111/j.1574-6976.2008.00144.x · Cited by 99 · see citing works
Zhang, Z., Du, C., de Barsy, F., Liem, M. K., Liakopoulos, A., van Wezel, G. P., Choi, Y. H., Claessen, D., & Rozen, D. E. (2020) · Science Advances · doi:10.1126/sciadv.aay5781 · Cited by 97 · see citing works
Structural correlations in bacterial metabolic networks
Bernhardsson, S., Gerlee, P., & Lizana, L. (2011) · BMC Evolutionary Biology · doi:10.1186/1471-2148-11-20 · Cited by 94 · see citing works
Self-establishing communities enable cooperative metabolite exchange in a eukaryote
Campbell, K., Vowinckel, J., Mülleder, M., Malmsheimer, S., Lawrence, N. J., Calvani, E., Miller‐Fleming, L., Alam, M. T., Christen, S., Keller, M. A., et al. (2015) · eLife · doi:10.7554/elife.09943 · Cited by 93 · see citing works
Evolutionary tradeoffs in cellular composition across diverse bacteria
Kempes, C. P., Wang, L., Amend, J. P., Doyle, J., & Hoehler, T. (2016) · The ISME Journal · doi:10.1038/ismej.2016.21 · Cited by 87 · see citing works
Live to cheat another day: bacterial dormancy facilitates the social exploitation of β-lactamases
Medaney, F., Dimitriu, T., Ellis, R. J., & Raymond, B. (2015) · The ISME Journal · doi:10.1038/ismej.2015.154 · Cited by 87 · see citing works
Competition between species can stabilize public‐goods cooperation within a species
Celiker, H., & Gore, J. (2012) · Molecular Systems Biology · doi:10.1038/msb.2012.54 · Cited by 86 · see citing works
Cheating fosters species co-existence in well-mixed bacterial communities
Leinweber, A., Inglis, R. F., & Kümmerli, R. (2017) · The ISME Journal · doi:10.1038/ismej.2016.195 · Cited by 85 · see citing works
Estrela, S., & Brown, S. P. (2013) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1003398 · Cited by 84 · see citing works
A Generalization of Hamilton’s Rule for the Evolution of Microbial Cooperation
Smith, J. S., Dyken, J. D. V., & Zee, P. C. (2010) · Science · doi:10.1126/science.1189675 · Cited by 82 · see citing works
Rapid radiation in bacteria leads to a division of labour
Kim, W., Levy, S. B., & Foster, K. R. (2016) · Nature Communications · doi:10.1038/ncomms10508 · Cited by 82 · see citing works
Potential role of phenotypic mutations in the evolution of protein expression and stability
Goldsmith, M., & Tawfik, D. S. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0809506106 · Cited by 81 · see citing works
Quorum-sensing control of antibiotic resistance stabilizes cooperation in Chromobacterium violaceum
Evans, K. C., Benomar, S., Camuy‐Vélez, L. A., Nasseri, E. B., Wang, X., Neuenswander, B., & Chandler, J. R. (2018) · The ISME Journal · doi:10.1038/s41396-018-0047-7 · Cited by 81 · see citing works
The evolutionary path to terminal differentiation and division of labor in cyanobacteria
Rossetti, V., Schirrmeister, B. E., Bernasconi, M. V., & Bagheri, H. C. (2009) · Journal of Theoretical Biology · doi:10.1016/j.jtbi.2009.09.009 · Cited by 73 · see citing works
Behavior of peripheral rods and their role in the life cycle of Myxococcus xanthus
O’Connor, K. A., & Zusman, D. R. (1991) · Journal of Bacteriology · doi:10.1128/jb.173.11.3342-3355.1991 · Cited by 70 · see citing works
Erosion of functional independence early in the evolution of a microbial mutualism
Hillesland, K. L., Lim, S., Flowers, J. J., Turkarslan, S., Pinel, N., Zane, G. M., Elliott, N., Qin, Y., Wu, L., Baliga, N. S., et al. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1407986111 · Cited by 70 · see citing works
Kümmerli, R., Santorelli, L. A., Granato, E. T., Dumas, Z., Dobay, A., Griffin, A. S., & West, S. A. (2015) · Journal of Evolutionary Biology · doi:10.1111/jeb.12751 · Cited by 69 · see citing works
Understanding Microbial Divisions of Labor
Zhang, Z., Claessen, D., & Rozen, D. E. (2016) · Frontiers in Microbiology · doi:10.3389/fmicb.2016.02070 · Cited by 69 · see citing works
Almstrand, R., Daims, H., Persson, F., Sörensson, F., & Hermansson, M. (2013) · Applied and Environmental Microbiology · doi:10.1128/aem.01727-13 · Cited by 67 · see citing works
Ultrastructural Characterization of the Prokaryotic Symbiosis in “ Chlorochromatium aggregatum ”
Wanner, G., Vogl, K., & Overmann, J. (2008) · Journal of Bacteriology · doi:10.1128/jb.00027-08 · Cited by 65 · see citing works
Seeking the Ultimate and Proximate Causes of Volvox Multicellularity and Cellular Differentiation
Kirk, D. L. (2003) · Integrative and Comparative Biology · doi:10.1093/icb/43.2.247 · Cited by 63 · see citing works
Varying virulence: epigenetic control of expression noise and disease processes
Miller‐Jensen, K., Dey, S. S., Schaffer, D. V., & Arkin, A. P. (2011) · Trends in biotechnology · doi:10.1016/j.tibtech.2011.05.004 · Cited by 62 · see citing works
Genomic Flux: Genome Evolution by Gene Loss and Acquisition
Lawrence, J. G., & Roth, J. R. (2014) · ASM Press eBooks · doi:10.1128/9781555818180.ch15 · Cited by 60 · see citing works
Evolving the Division of Labour: Generalists, Specialists and Task Allocation
Wahl, L. M. (2002) · Journal of Theoretical Biology · doi:10.1006/jtbi.2002.3133 · Cited by 60 · see citing works
An Environment-Sensitive Synthetic Microbial Ecosystem
Hu, B., Du, J., Zou, R., & Yuan, Y. (2010) · PLoS ONE · doi:10.1371/journal.pone.0010619 · Cited by 59 · see citing works
Rodionova, I. A., Li, X., Plymale, A. E., Motamedchaboki, K., Konopka, A. E., Romine, M. F., Fredrickson, J. K., Osterman, A. L., & Rodionov, D. A. (2014) · Environmental Microbiology Reports · doi:10.1111/1758-2229.12227 · Cited by 59 · see citing works
Transitions in individuality through symbiosis
Estrela, S., Kerr, B., & Morris, J. (2016) · Current Opinion in Microbiology · doi:10.1016/j.mib.2016.04.007 · Cited by 58 · see citing works
Aerobic Granules: Microbial Landscape and Architecture, Stages, and Practical Implications
Gonzalez-Gil, G., & Holliger, C. (2014) · Applied and Environmental Microbiology · doi:10.1128/aem.00250-14 · Cited by 55 · see citing works
Kim, H. J., Du, W., & Ismagilov, R. F. (2010) · Integrative Biology · doi:10.1039/c0ib00019a · Cited by 48 · see citing works
Gene Duplication and the Evolution of Enzymes
Watts, R. L., & WATTS, D. C. (1968) · Nature · doi:10.1038/2171125a0 · Cited by 47 · see citing works
Suzuki, S., Horinouchi, S., & Beppu, T. (1988) · Microbiology · doi:10.1099/00221287-134-8-2353 · Cited by 47 · see citing works
Marchal, M., Goldschmidt, F., Derksen-MĂźller, S., Panke, S., Ackermann, M., & Johnson, D. R. (2017) · BMC Evolutionary Biology · doi:10.1186/s12862-017-0950-y · Cited by 47 · see citing works
Degradation of 4-aminobenzenesulfonate by a two-species bacterial coculture
Dangmann, E., Stolz, A., Kuhm, A. E., Hammer, A., Feigel, B. J., Noisommit‐Rizzi, N., Rizzi, M., Reu�, M., & Knackmuss, H. (1996) · Biodegradation · doi:10.1007/bf00058181 · Cited by 46 · see citing works
Quantifying the effects of the division of labor in metabolic pathways
Harvey, E., Heys, J. J., & Gedeon, T. (2014) · Journal of Theoretical Biology · doi:10.1016/j.jtbi.2014.07.011 · Cited by 39 · see citing works
Bacterial Quorum Sensing Stabilizes Cooperation by Optimizing Growth Strategies
Bruger, E. L., & Waters, C. M. (2016) · Applied and Environmental Microbiology · doi:10.1128/aem.01945-16 · Cited by 38 · see citing works
Cooperation within and among species
Sachs, J. L. (2006) · Journal of Evolutionary Biology · doi:10.1111/j.1420-9101.2006.01152.x · Cited by 27 · see citing works
Individual‐ versus group‐optimality in the production of secreted bacterial compounds
Schiessl, K. T., Ross‐Gillespie, A., Cornforth, D. M., Weigert, M., Bigosch, C., Brown, S. P., Ackermann, M., & Kümmerli, R. (2019) · Evolution · doi:10.1111/evo.13701 · Cited by 27 · see citing works
Phototrophic Consortia: A Tight Cooperation Between Non-Related Eubacteria
Overmann, J. (2006) · Kluwer Academic Publishers eBooks · doi:10.1007/0-306-48173-1_15 · Cited by 23 · see citing works
The Division of Labor: Genotypic versus Phenotypic Specialization
Wahl, L. M. (2002) · The American Naturalist · doi:10.1086/340601 · Cited by 22 · see citing works
Horemans, B., Smolders, E., & Springael, D. (2012) · FEMS Microbiology Ecology · doi:10.1111/1574-6941.12033 · Cited by 19 · see citing works
Rossetti, V., & Bagheri, H. C. (2012) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2012.0755 · Cited by 15 · see citing works
Receptor uptake arrays for vitamin B 12 , siderophores, and glycans shape bacterial communities
Frank, S. A. (2017) · Ecology and Evolution · doi:10.1002/ece3.3544 · Cited by 7 · see citing works
Individual-versus group-optimality in the production of secreted bacterial compoundsPreprint
Schiessl, K. T., Ross‐Gillespie, A., Cornforth, D. M., et al. (2016) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/094086 · Cited by 5 · see citing works
Kramer, J., Carrasco, M. Á. L., & Kümmerli, R. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/477471 · Cited by 2 · see citing works
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Gradients and consequences of heterogeneity in biofilms
Jo, J., Price‐Whelan, A., & Dietrich, L. E. P. (2022) · Nature Reviews Microbiology · doi:10.1038/s41579-022-00692-2 · Cited by 327 · see citing works
Canon, F., Nidelet, T., Guédon, É., Thierry, A., & Gagnaire, V. (2020) · Frontiers in Microbiology · doi:10.3389/fmicb.2020.02088 · Cited by 167 · see citing works
Liang, Y., Ma, A., & Zhuang, G. (2022) · Frontiers in Microbiology · doi:10.3389/fmicb.2022.829717 · Cited by 146 · see citing works
Metabolic dissimilarity determines the establishment of cross-feeding interactions in bacteria
Giri, S., Oña, L., Waschina, S., Shitut, S., Yousif, G., Kaleta, C., & Kost, C. (2021) · Current Biology · doi:10.1016/j.cub.2021.10.019 · Cited by 109 · see citing works
Division of labor for substrate utilization in natural and synthetic microbial communities
Rafieenia, R., Atkinson, E., & Ledesma‐Amaro, R. (2022) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2022.102706 · Cited by 84 · see citing works
Wang, Z., Wang, S., He, Q., Yang, X., Zhao, B., Zhang, H., & Deng, Y. (2025) · ISME Communications · doi:10.1093/ismeco/ycaf133 · Cited by 83 · see citing works
“This emergent property arises from evolutionary processes,including speciation, genetic diversification, and ecological interactions (competition, cooperation, and cheating) [82], with human intervention further modulating these dynamics [83].”
Navigating Environmental Transitions: the Role of Phenotypic Variation in Bacterial Responses
Spratt, M. R., & Lane, K. M. (2022) · mBio · doi:10.1128/mbio.02212-22 · Cited by 65 · see citing works
“In a division of labor strategy, energetically costly functions required of the population are distributed among discrete coexisting subpopulations, minimizing the burden placed on individuals (20, 21).”
BackgroundFrommeyer, B., Fiedler, A. W., Oehler, S. R., Hanson, B. T., Loy, A., Franchini, P., Spiteller, D., & Schleheck, D. (2020) · iScience · doi:10.1016/j.isci.2020.101510 · Cited by 68 · see citing works
Giri, S., Shitut, S., & Kost, C. (2020) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2019.12.012 · Cited by 67 · see citing works
Cooperation increases robustness to ecological disturbance in microbial cross‐feeding networks
Oña, L., & Kost, C. (2022) · Ecology Letters · doi:10.1111/ele.14006 · Cited by 66 · see citing works
Selective Drivers of Simple Multicellularity
Tong, K., Bozdag, G. O., & Ratcliff, W. C. (2021) · Current Opinion in Microbiology · doi:10.1016/j.mib.2022.102141 · Cited by 65 · see citing works
Recurrent Urinary Tract Infections: Unraveling the Complicated Environment of Uncomplicated rUTIs
Josephs‐Spaulding, J., Krogh, T. J., Rettig, H. C., Lyng, M., Chkonia, M., Waschina, S., Graspeuntner, S., Rupp, J., Møller‐Jensen, J., & Kaleta, C. (2021) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2021.562525 · Cited by 59 · see citing works
“The mechanisms for various species interact with one another is likely within a system to support one another through crossfeeding, co-exist in neutralism, or rigorously compete in a multispecies system respectively (Bauer et al., 2017; Ferreiro et al., 2018; Giri et al., 2019).”
BackgroundSpatially structured microbial consortia and their role in food fermentations
Michielsen, S., Vercelli, G. T., Cordero, O. X., & Bachmann, H. (2024) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2024.103102 · Cited by 49 · see citing works
Labour sharing promotes coexistence in atrazine degrading bacterial communities
Billet, L., Devers‐Lamrani, M., Rouard, N., Martin-Laurent, F. A., & Spor, A. (2019) · Scientific Reports · doi:10.1038/s41598-019-54978-2 · Cited by 45 · see citing works
Lindemann, S. R. (2020) · Current Opinion in Chemical Engineering · doi:10.1016/j.coche.2020.08.004 · Cited by 44 · see citing works
Ma, Q., Sun, Q., Tan, M., Li, X., Zhang, Y., Yang, M., Zhuo, M., Zhao, K., Li, Y., Xu, Q., et al. (2021) · Journal of Agricultural and Food Chemistry · doi:10.1021/acs.jafc.1c01513 · Cited by 40 · see citing works
Microbiota of Cheese Ecosystems: A Perspective on Cheesemaking
Neviani, E., Gatti, M., Gardini, F., & Levante, A. (2025) · Foods · doi:10.3390/foods14050830 · Cited by 39 · see citing works
“Thus, cell-to-cell heterogeneity has important implications, allowing populations of cells to diversify to survive environmental stress, according to the proposed theory of division of labor [33,34].”
Wu, S., Li, X., Fan, H., Dong, Y., Wang, Y., Bai, Z., & Zhuang, X. (2022) · Journal of Hazardous Materials · doi:10.1016/j.jhazmat.2022.130221 · Cited by 37 · see citing works
Canon, F., Mariadassou, M., Maillard, M.-B., Falentin, H., Parayre, S., Madec, M., Valence, F., Henry, G., Laroute, V., Daveran‐Mingot, M., et al. (2020) · Frontiers in Microbiology · doi:10.3389/fmicb.2020.584163 · Cited by 35 · see citing works
Prevalent emergence of reciprocity among cross-feeding bacteria
Giri, S., Yousif, G., Shitut, S., Oña, L., & Kost, C. (2022) · ISME Communications · doi:10.1038/s43705-022-00155-y · Cited by 32 · see citing works
de Paz, G. Á., Ledezma-Villanueva, A., Robledo-Mahón, T., Pozo, C., Calvo, C., Aranda, E., & Purswani, J. (2022) · Chemosphere · doi:10.1016/j.chemosphere.2022.137472 · Cited by 28 · see citing works
Mutational meltdown of putative microbial altruists in Streptomyces coelicolor colonies
Zhang, Z., Shitut, S., Claushuis, B., Claessen, D., & Rozen, D. E. (2022) · Nature Communications · doi:10.1038/s41467-022-29924-y · Cited by 27 · see citing works
Lessons From Insect Fungiculture: From Microbial Ecology to Plastics Degradation
Barcoto, M. O., & Rodrigues, A. L. (2022) · Frontiers in Microbiology · doi:10.3389/fmicb.2022.812143 · Cited by 27 · see citing works
Rafieenia, R., Klemm, C., Hapeta, P., Fu, J., García, M. G., & Ledesma‐Amaro, R. (2024) · Trends in biotechnology · doi:10.1016/j.tibtech.2024.10.015 · Cited by 24 · see citing works
Complex Ecotype Dynamics Evolve in Response to Fluctuating Resources
Behringer, M. G., Ho, W.-C., Meraz, J. C., Miller, S. F., Boyer, G. F., Stone, C. J., Andersen, M., & Lynch, M. (2022) · mBio · doi:10.1128/mbio.03467-21 · Cited by 22 · see citing works
Malla, M. A., Ansari, F. A., Bux, F., & Kumari, S. (2024) · Environmental Research · doi:10.1016/j.envres.2024.119439 · Cited by 22 · see citing works
Rodriguez-Conde, F. C., Zhu, S., & Dikicioǧlu, D. (2025) · Critical Reviews in Biotechnology · doi:10.1080/07388551.2025.2455607 · Cited by 20 · see citing works
“In a recent review, Giri et al. outlined the criteria for classifying ecological interactions as division of labor [1].”
InfluentialLiu, L., Tian, C. F., Wang, M., Ying, L., Huang, Y., Jiang, T., Zhao, H., Yu, Q., Wang, E. T., Yang, J., et al. (2025) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2500664122 · Cited by 19 · see citing works
“Extensive research has employed synthetic microbial communities to explore how coop erative partners manage exploitative behaviors in exchanging communally valuable nutri ents, such as amino acids and vitamins ( 13 , 15 – 17 ).”
Non-Genetic Diversity in Chemosensing and Chemotactic Behavior
Moore, J. P., Kamino, K., & Emonet, T. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22136960 · Cited by 17 · see citing works
Role of horizontal gene transfer and cooperation in rhizosphere microbiome assembly
Cotta, S. R., Dias, A. C. F., Mendes, R., & Andreote, F. D. (2024) · Brazilian Journal of Microbiology · doi:10.1007/s42770-024-01583-9 · Cited by 17 · see citing works
“This is achieved through the division of complex metabolic processes into smaller steps, with each step performed by specific microbial groups [85–87].”
Varahan, S., Sinha, V., Walvekar, A. S., Krishna, S., & Laxman, S. (2020) · eLife · doi:10.7554/elife.57609 · Cited by 17 · see citing works
“While division of labor has often been used loosely, more stringent definitions of division of labor require (1) functional complementarity, (2) synergistic advantages, (3) negative frequency-dependent selection, and (4) positive assortment (Giri et al., 2019).”
BackgroundEcological drivers of division of labour in Streptomyces
Traxler, M. F., & Rozen, D. E. (2022) · Current Opinion in Microbiology · doi:10.1016/j.mib.2022.102148 · Cited by 17 · see citing works
Uncovering phenotypic inheritance from single cells with Microcolony-seq
Faigenbaum-Romm, R., Yedidi, N., Gefen, O., Katsowich, N., Aroeti, L., Ronin, I., Bar‐Meir, M., Rosenshine, I., & Balaban, N. Q. (2025) · Cell · doi:10.1016/j.cell.2025.08.001 · Cited by 16 · see citing works
Cooperative Virus-Virus Interactions: An Evolutionary Perspective
Segredo-Otero, E. A., & Sanjuán, R. (2022) · BioDesign Research · doi:10.34133/2022/9819272 · Cited by 15 · see citing works
“The conditions required for such coexistence include functional complementary, synergistic advantages, and a positive assortment of specialists [87].”
BackgroundDu, B., Wang, Y., & Wu, G. (2025) · Bioresource Technology · doi:10.1016/j.biortech.2025.132862 · Cited by 14 · see citing works
Li, X., Wu, S., Fan, H., Dong, Y., Wang, Y., Bai, Z., Jing, C., & Zhuang, X. (2022) · Journal of Hazardous Materials · doi:10.1016/j.jhazmat.2023.131460 · Cited by 13 · see citing works
Bacterial phenotypic heterogeneity through the lens of single-cell RNA sequencing
Walls, A. W., & Rosenthal, A. Z. (2024) · Transcription · doi:10.1080/21541264.2024.2334110 · Cited by 12 · see citing works
“Another benefit provided by transcriptional heterogeneity is the division of labor, in which cells can segregate the production of metabolically incompatible or energetically expensive gene products into a subpopulation of cells [87].”
BackgroundXu, F., Jiang, M., Li, D., Yu, P., Ma, H., & Lü, H. (2024) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2024.172668 · Cited by 12 · see citing works
The evolution of division of labour: preconditions and evolutionary feedback
Michael Taborsky, A. (2025) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2023.0262 · Cited by 12 · see citing works
Evolution of genome fragility enables microbial division of labor
Colizzi, E. S., van Dijk, B., Merks, R. M. H., Rozen, D. E., & Vroomans, R. M. A. (2023) · Molecular Systems Biology · doi:10.15252/msb.202211353 · Cited by 10 · see citing works
“…of labor have been described in the microbial world (Ratcliff et al , 2012; Claessen et al , 2014; Gestel et al , 2015; Drago ˇ s et al , 2018; Giri et al , 2019); it has been proposed that reproductive division of labor existed already before the Origin of Life, among prebiotic replicators…”
BackgroundMridha, S., & Kümmerli, R. (2022) · Journal of Evolutionary Biology · doi:10.1111/jeb.14001 · Cited by 8 · see citing works
“…theory and to experimentally investigate division of labour and the underlying evolutionary forces (Ackermann et al., 2008; van Gestel et al., 2015; Kim et al., 2016; West and Cooper, 2016; Dragoš et al., 2018a; Dragoš et al., 2018b; Giri et al., 2019; Armbruster et al., 2020; Yanni et al., 2020).”
BackgroundD’Souza, G. G. (2020) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2019.12.013 · Cited by 10 · see citing works
Prospecting artificial microbial consortia toward lignin valorization
Hu, J., Gao, B.-C., Liu, Z., Li, X., Yuan, Y., & Li, B. (2025) · Chemical Engineering Journal · doi:10.1016/j.cej.2025.162375 · Cited by 9 · see citing works
Varahan, S., & Laxman, S. (2021) · Genetics · doi:10.1093/genetics/iyab109 · Cited by 8 · see citing works
Enrichable consortia of microbial symbionts degrade macroalgal polysaccharides in Kyphosus fish
Oliver, A., Podell, S. B., Kelly, L. W., Sparagon, W. J., Plominsky, Á. M., Nelson, R. S., Laurens, L. M. L., Augytė, S., Sims, N. A., Nelson, C. E., et al. (2024) · mBio · doi:10.1128/mbio.00496-24 · Cited by 10 · see citing works
“A division of labor strategy cannot be fully confirmed without in vitro tests (94), although the first condition of genomically encoded functional complementarity appears to hold true between Kyphosus symbionts based on bioinformatic criteria.”
BackgroundFazl, U., Wang, J., Yin, J., Jiang, X., Meng, F., Zhang, W., Zhang, L., & Zhao, H. (2024) · Agronomy · doi:10.3390/agronomy14071553 · Cited by 8 · see citing works
Wilssens, H., Wannemaeker, L. D., & Mey, M. D. (2025) · FEMS Microbiology Reviews · doi:10.1093/femsre/fuaf055 · Cited by 8 · see citing works
Limited Pairwise Synergistic and Antagonistic Interactions Impart Stability to Microbial Communities
Mall, A., Kasarlawar, S. T., & Saini, S. (2022) · Frontiers in Ecology and Evolution · doi:10.3389/fevo.2022.648997 · Cited by 6 · see citing works
Liu, H., Li, F. Y., Liu, J., Shi, C., Tang, K., Yang, Q., Liu, Y., Fu, Q., Gao, X., Wang, N., et al. (2023) · Frontiers in Microbiology · doi:10.3389/fmicb.2023.1113157 · Cited by 6 · see citing works
“Although imaginative scholars have been characterized by the division of labor effect (Giri et al., 2019; Oña and Kost, 2022) or stable marriage problem (Goyal et al.”
BackgroundDynamic proteome allocation regulates the profile of interaction of auxotrophic bacterial consortia
Reyes-González, D., Luna-Valenciano, H. D., Utrilla, J., Sieber, M., Peña‐Miller, R., & Fuentes-Hernández, A. (2022) · Royal Society Open Science · doi:10.1098/rsos.212008 · Cited by 5 · see citing works
Ulmer, A., Veit, S., Erdemann, F., Freund, A., Loesch, M., Teleki, A., Zeidan, A. A., & Takors, R. (2023) · Bioengineering · doi:10.3390/bioengineering10010103 · Cited by 5 · see citing works
Lynn, B. K., Leenheer, P. D., & Schuster, M. (2024) · PLoS ONE · doi:10.1371/journal.pone.0300887 · Cited by 5 · see citing works
Peng, Q., & Lin, L. (2025) · Biotechnology for Biofuels and Bioproducts · doi:10.1186/s13068-025-02605-w · Cited by 5 · see citing works
Can a microbial community become an evolutionary individual?
Salazar, A., & Mitri, S. (2025) · Current Opinion in Microbiology · doi:10.1016/j.mib.2025.102596 · Cited by 4 · see citing works
Niño-Padilla, E. I., Espitia, C., Velázquez, C. A., Alday, E., Silva‐Campa, E., Burgara-Estrella, A., Enciso‐Moreno, J. A., Valenzuela, O., Astiazarán‐García, H., & Garibay‐Escobar, A. (2023) · ACS Omega · doi:10.1021/acsomega.3c05703 · Cited by 4 · see citing works
“13,14 This genetic diversity is recognized as being an essential element in the development of tolerance, which can eventually lead to resistance in both in vivo and in vitro settings.”
BackgroundAnthamatten, L., von Bieberstein, P. R., Thabuis, C., Menzi, C., Reichlin, M., Meola, M., Rodriguez, B., Cordero, O. X., Lacroix, C., de Wouters, T., et al. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.07.04.547750 · Cited by 4 · see citing works
Prusak, H., Gutowska, N., Alaux, E., Szczygiełda, M., Wint, N. Y., Sousa, D. Z., Lezyk, M. J., & Oleśkowicz-Popiel, P. (2026) · Green Chemistry · doi:10.1039/d5gc05638a · Cited by 3 · see citing works
Taillefer, B., Schattenberg, F., Doan, T., Müller, S., & Cascalès, E. (2026) · PLoS Biology · doi:10.1371/journal.pbio.3003838 · Cited by 3 · see citing works
“In division of labor, phenotypically distinct subpopulations accomplish specialized tasks independently that enhance group fitness [28].”
Dynamic mechanism of phase variation in bacteria based on multistable gene regulatory networks
Galimzyanov, A. V., & Tchuraev, R. N. (2022) · Journal of Theoretical Biology · doi:10.1016/j.jtbi.2022.111212 · Cited by 3 · see citing works
Taillefer, B., Schattenberg, F., Doan, T., Müller, S., & Cascalès, E. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.02.11.637775 · Cited by 3 · see citing works
Avcı, F. G., & Wendisch, V. F. (2026) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2026.1820441 · Cited by 2 · see citing works
“In natural environments, microorganisms form complex communities that cooperate through cellular division of labor, enabling functional specialization, efficient resource utilization, and enhanced competitive fitness (Giri et al., 2019).”
Wilmsen, S., & Kost, C. (2025) · Biological Theory · doi:10.1007/s13752-024-00486-0 · Cited by 2 · see citing works
“(Shapiro 1988 ; Sendova-Franks and Franks 1994; Traniello and Rosengaus 1997; Dall et al. 2012 ; Ispo - latov et al. 2012 ; Rueffler et al. 2012; Giri et al. 2019; Poulin et al. 2019) Table 1 Hallmarks of organismality. of organization.”
Jerdan, R., Iungin, O. S., Moshynets, O. V., Potters, G., & Spiers, A. J. (2020) · IntechOpen eBooks · doi:10.5772/intechopen.90955 · Cited by 2 · see citing works
Bellaver, E. H., Redin, E. E., da Costa, I. M., Moroni, L. S., & Kempka, A. P. (2025) · ACS Food Science & Technology · doi:10.1021/acsfoodscitech.5c00396 · Cited by 1 · see citing works
Sui, M., Miao, K., Tang, L. H., Zhao, J., Jin, C., Zhao, Y., & Guo, L. (2025) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2025.180311 · Cited by 1 · see citing works
Wang, Y., Wang, Y., Xue, W., Li, J., Zhang, F., Lv, X., Zhang, F., Li, Y., Wang, C., & Hu, W. (2025) · mBio · doi:10.1128/mbio.02568-25 · Cited by 1 · see citing works
Bruce, J., Barona‐Gómez, F., & Hoskisson, P. A. (2026) · Essays in Biochemistry · doi:10.1042/ebc20250017 · Cited by 1 · see citing works
Baumann, C. T., Hydorn, M. A., Cooke, S. F., Dworkin, J. E., & Rosenthal, A. Z. (2026) · Science Advances · doi:10.1126/sciadv.adz1707 · Cited by 1 · see citing works
Synergistic degradation of fucoidans in the ocean
Sichert, A., Pollak, S., Priest, T., Goyal, A., Miravet‐Verde, S., Sunagawa, S., Cordero, O. X., & Sauer, U. (2026) · Nature · doi:10.1038/s41586-026-10980-z · Cited by 1 · see citing works
“On the subset of co-cultures with altered degradation outcomes, we classified interaction types using absolute species abundances determined by strain-specific quantitative PCR (qPCR) 48 (Fig.”
Anaerobic Digestion and Its Understanding by Introducing the Design-Build-Test-Learn Cycle
Wu, G. (2024) · Green energy and technology · doi:10.1007/978-3-031-69378-6_1 · Cited by 1 · see citing works
Mutational meltdown of microbial altruists in Streptomyces coelicolor coloniesPreprint
Zhang, Z., Claushuis, B., Claessen, D., & Rozen, D. E. (2020) · Research Square · doi:10.21203/rs.3.rs-101912/v1 · Cited by 1 · see citing works
Enrichable consortia of microbial symbionts degrade macroalgal polysaccharides in Kyphosus fishPreprint
Oliver, A., Podell, S. B., Kelly, L. W., Sparagon, W. J., Plominsky, Á. M., Nelson, R. S., Laurens, L. M. L., Augytė, S., Sims, N. A., Nelson, C. E., et al. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.11.28.568905 · Cited by 1 · see citing works
Kwak, G.-Y., Goo, E., Jeong, H., & Hwang, I. (2020) · PLoS ONE · doi:10.1371/journal.pone.0238151
Baumann, C. T., Hydorn, M. A., Cooke, S. F., Dworkin, J. E., & Rosenthal, A. Z. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.04.22.649982
Ahmad, M. F., & Laxman, S. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.07.09.664033
Multicellular cooperation and the hallmarks of cancer: A new foundation
Maley, C. C., Boddy, A. M., Nedelcu, A. M., & Aktipis, A. (2025) · Evolution Medicine and Public Health · doi:10.1093/emph/eoaf026
Exploring the Patterns of Bacterial Interactions with the Other
Joy, R. (2025) · Biosemiotics · doi:10.1007/s12304-025-09629-7
“It includes characteristics typical of eusocial animals, such as division of labor (Giri et al., 2019).”
A review: shining a light on cheater microbes with positive molecular detection techniques
Dakheel, K. H., Abid, S. A., Al-Kadmy, I. M. S., & Aziz, S. N. (2025) · Reviews in Medical Microbiology · doi:10.1097/mrm.0000000000000434
Backes, C., Ranava, D., Infossi, P., Delecourt, L., Roger, M., & Giudici‐Orticoni, M. (2026) · Frontiers in Microbiology · doi:10.3389/fmicb.2026.1682391
Microalgae cocultures: concepts and applications
Bahari, N., Almalki, W. J., Almahmoudi, Z., Islam, M., Veeramani, S., & Vaidyanathan, S. (2026) · Elsevier eBooks · doi:10.1016/b978-0-443-34082-6.00004-0
Micromolar concentrations of metabolites enable coexistence of bacterial species in chemostatsPreprint
Ulrich, E., & Mitri, S. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.04.23.720424
Enagbonma, B. J., Molefe, R. R., Adebayo, A. A., Oyedoh, O. P., Oribhabor, G. O., Shittu, O. E., & Babalola, O. O. (2026) · Biotechnology and Bioengineering · doi:10.1002/bit.70291
“When all members gain from cross‐feeding exchange, it is known as functional specialization (Giri et al. 2019).”
Ahmad, M. F., Muthu, G., & Laxman, S. (2026) · mSystems · doi:10.1128/msystems.00333-26
“Amino acids are commonly exchanged between microbial cells (5, 20–23); yet, they are not homogeneous but are chemically, metabolically, and functionally distinct and present at different amounts (24, 25).”
Engineering rhizobacterial communities for soil and plant health
Garcia‐Perez, E., Perrin, L., Malone, J. G., Thompson, C. M. A., & Guiziou, S. (2026) · Microbiology · doi:10.1099/mic.0.001748
“Two main strategies for tweaking social interactions are commonly employed – negative and positive – that can also be combined to create bidirectional relationships [48, 62, 63].”
Impact of Petroleum Contamination on Microbial Mats
Goñi‐Urriza, M., & Duran, R. (2026) · Springer eBooks · doi:10.1007/978-3-319-60063-5_14-2
Monroy-Martínez, W., González‐Hernández, J. C., & Chávez-Parga, M. D. C. (2026) · World Journal of Microbiology and Biotechnology · doi:10.1007/s11274-026-05268-3
“For the interaction within these consortia to be formally classified as DoL, it must meet various criteria proposed by Giri et al. (2019): (1) functional complementarity, (2) synergistic advantage, (3) negative frequency-dependent selection, and (4) positive settlement.”
- Authors
- Giri, S., Waschina, S., Kaleta, C., & Kost, C.
- Affiliations
- Osnabrück University (DE)
- Christian-Albrechts-Universität zu Kiel (DE)
- Corresponding author
- Kost, Christian
- Venue
- Journal of Molecular Biology
- Publisher
- Elsevier BV
- Published
- 2019-11
- Volume
- 431
- Issue
- 23
- Pages
- 4712-4731
- ISSN
- 0022-2836 (ISSN-L)
- OpenAlex
- W2954410834
- Cited by
- 89
- References
- 186
- Citations by year
- 2026: 15 · 2025: 21 · 2024: 11 · 2023: 7 · 2022: 18 · 2021: 6 · 2020: 10 · 2019: 1
- FWCI
- 0.77
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Molecular Biology (publishedVersion)
- PubMed (publishedVersion)
- MPG.PuRe (Max Planck Society) (submittedVersion)
- Funders
- Deutsche Forschungsgemeinschaft (SPP1617, ExC 306, SFB 944-P19)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Bacterial biofilms and quorum sensing
- Physical Sciences › Environmental Science › Ecology › Microbial Community Ecology and Physiology
- Social Sciences › Sociology and Political Science › Evolutionary Game Theory and Cooperation
- Keywords
- division of labor, microbial communities, functional specialization, intraspecific interactions, species interactions, public goods, social parasites, metabolic cooperation, diagnostic criteria, microbial symbiosis
- MeSH terms
- Biological Evolution, Gene Expression Regulation, Microbiological Phenomena, Phenotype, Microbiota
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