Abstract
Cooperation is ubiquitous in biological systems. However, if natural selection favors traits that confer an advantage to one individual over another, then helping others would be paradoxical. Nevertheless, cooperation persists and is critical in maintaining homeostasis in systems ranging from populations of bacteria to groupings of mammals. Developing an understanding of the dynamics and mechanisms by which cooperation operates is critical in understanding ecological and evolutionary relationships. Over the past decade, synthetic biology has emerged as a powerful tool to study social dynamics. By engineering rationally controlled and modulatable behavior into microbes, we have increased our overall understanding of how cooperation enhances, or conversely constrains, populations. Furthermore, it has increased our understanding of how cooperation is maintained within populations, which may provide a useful framework to influence populations by altering cooperation. As many bacterial pathogens require cooperation to infect the host and survive, the principles developed using synthetic biology offer promise of developing novel tools and strategies to treat infections, which may reduce the use of antimicrobial agents. Overall, the use of engineered cooperative microbes has allowed the field to verify existing, and develop novel, theories that may govern cooperative behaviors at all levels of biology.
Similar content being viewed by others
References
Nowak M A. Five rules for the evolution of cooperation. Science, 2006, 314(5805): 1560–1563
Axelrod R, Hamilton W D. The evolution of cooperation. Science, 1981, 211(4489): 1390–1396
Fehr E, Fischbacher U. Social norms and human cooperation. Trends in Cognitive Sciences, 2004, 8(4): 185–190
Shan W, Hamilton W. Country—specific advantage and international cooperation. Strategic Management Journal, 1991, 12(6): 419–432
Hardin G. The tragedy of the commons. Science, 1968, 162(3859): 1243–1248
Feeny D, Berkes F, McCay B J, Acheson J M. The tragedy of the commons: twenty-two years later. Human Ecology, 1990, 18(1): 1–19
Hamilton W. The evolution of altruistic behavior. American Naturalist, 1963, 97(896): 354–356
Eldakar O T, Wilson D S. Eight criticisms not to make about group selection. Evolution, 2011, 65(6): 1523–1526
Wilson D S, Wilson E O. Rethinking the theoretical foundation of sociobiology. Quarterly Review of Biology, 2007, 82(4): 327–348
Rapoport A, Chammah A M. Prisoner’s dilemma: A study in conflict and cooperation. Michigan: University of Michigan press, 1965: 31–44
Doebeli M, Hauert C. Models of cooperation based on the Prisoner’s Dilemma and the Snowdrift game. Ecology Letters, 2005, 8(7): 748–766
Allee W C. Cooperation among animals. American Journal of Sociology, 1951, 1: 93–95
Seger J. Cooperation and conflict in social insects. Behavioural Ecology: An Evolutionary Approach, 1991, 338–373
West S A, El Mouden C, Gardner A. Sixteen common misconceptions about the evolution of cooperation in humans. Evolution and Human Behavior, 2011, 32(4): 231–262
Gintis H, Bowles S, Boyd R, Fehr E. Explaining altruistic behavior in humans. Evolution and Human Behavior, 2003, 24(3): 153–172
Sober E, Wilson D S. Unto others: The evolution and psychology of unselfish behavior. Massachusetts: Harvard University Press, 1999, 6–14
Tanouchi Y, Smith R, You L. Engineering microbial systems to explore ecological and evolutionary dynamics. Current Opinion in Biotechnology, 2012, 23(5): 791–797
Benner S A, Sismour A M. Synthetic biology. Nature Reviews. Genetics, 2005, 6(7): 533–543
Jusiak B, Daniel R, Farzadfard F, Nissim L, Purcell O, Rubens J, Lu T K. Synthetic gene circuits. Reviews in Cell Biology and Molecular Medicine, 2014, 1–56
Khalil A S, Collins J J. Synthetic biology: Applications come of age. Nature Reviews. Genetics, 2010, 11(5): 367–379
Bracho O R, Manchery C, Haskell E C, Blanar C A, Smith R P. Circumvention of learning increases intoxication efficacy of nematicidal engineered bacteria. ACS Synthetic Biology, 2016, 5(3): 241–249
Escalante A E, Rebolleda-Gómez M, Benítez M, Travisano M. Ecological perspectives on synthetic biology: Insights from microbial population biology. Frontiers in Microbiology, 2015, 6: 1–10
Pianka E R. On r-and K-selection. American Naturalist, 1970, 104(940): 592–597
Miller M B, Bassler B L. Quorum sensing in bacteria. Annual Review of Microbiology, 2001, 55(1): 165–199
Berendsen R L, Pieterse C M, Bakker P A. The rhizosphere microbiome and plant health. Trends in Plant Science, 2012, 17(8): 478–486
Antunes L C M, Ferreira R B R, Buckner M M C, Finlay B B. Quorum sensing in bacterial virulence. Microbiology, 2010, 156(8): 2271–2282
De Kievit T R, Gillis R, Marx S, Brown C, Iglewski B H. Quorumsensing genes in Pseudomonas aeruginosa biofilms: Their role and expression patterns. Applied and Environmental Microbiology, 2001, 67(4): 1865–1873
De Kievit T R, Iglewski B H. Bacterial quorum sensing in pathogenic relationships. Infection and Immunity, 2000, 68(9): 4839–4849
Stewart P S, Costerton J W. Antibiotic resistance of bacteria in biofilms. Lancet, 2001, 358(9276): 135–138
Darch S E, West S A, Winzer K, Diggle S P. Density-dependent fitness benefits in quorum-sensing bacterial populations. Proceedings of the National Academy of Sciences, 2012: 8259–8263
Pai A, Tanouchi Y, You L. Optimality and robustness in quorum sensing (QS)-mediated regulation of a costly public good enzyme. Proceedings of the National Academy of Sciences of the United States of America, 2012, 109(48): 19810–19815
An J H, Goo E, Kim H, Seo Y S, Hwang I. An J H, Goo E, Kim H, Seo Y-S, Hwang I. Bacterial quorum sensing and metabolic slowing in a cooperative population. Proceedings of the National Academy of Sciences of the United States of America, 2014, 111(41): 14912–14917
Allee W, Emerson A, Park O, Park T, Schmidt K. Principles of Animal Ecology. Philadelphia, Pennsylvania, USA, 1949, 416–425
Driscoll W W, Espinosa N J, Eldakar O T, Hackett J D. Allelopathy as an emergent, exploitable public good in the bloom-forming microalga Prymnesium parvum. Evolution, 2013, 67(6): 1582–1590
Liebhold A M, Tobin P C. Exploiting the Achilles heels of pest invasions: Allee effects, stratified dispersal and management of forest insect establishment and spread. New Zealand Journal of Forestry Science, 2010, 40: S25–S33
Robinet C, Lance D R, Thorpe K W, Onufrieva K S, Tobin P C, Liebhold A M. Dispersion in time and space affect mating success and Allee effects in invading gypsy moth populations. Journal of Animal Ecology, 2008, 77(5): 966–973
Tobin P C, Berec L, Liebhold A M. Exploiting Allee effects for managing biological invasions. Ecology Letters, 2011, 14(6): 615–624
Hackney E E, McGraw J B. Experimental demonstration of an Allee effect in American ginseng. Conservation Biology, 2001, 15(1): 129–136
Smith R, Tan C, Srimani J, Pai A, Riccione K, Song H, You L. Programmed Allee effect results in a tradeoff between population spread and survival. Proceedings of the National Academy of Sciences of the United States of America, 2014, 111(5): 1969–1974
Myers R A, Hutchings J A, Barrowman N J. Why do fish stocks collapse? The example of cod in Atlantic Canada. Ecological Applications, 1997, 7(1): 91–106
Myers R, Barrowman N, Hutchings J, Rosenberg A. Population dynamics of exploited fish stocks at low population levels. Science, 1995, 269(5227): 1106–1108
Dai L, Vorselen D, Korolev K S, Gore J. Generic indicators for loss of resilience before a tipping point leading to population collapse. Science, 2012, 336(6085): 1175–1177
Dai L, Korolev K S, Gore J. Relation between stability and resilience determines the performance of early warning signals under different environmental drivers. Proceedings of the National Academy of Sciences of the United States of America, 2015, 112(32): 10056–10061
Liebhold A M, Tobin P C. Population ecology of insect invasions and their management. Annual Review of Entomology, 2008, 53(1): 387–408
Visick K L, Foster J, Doino J, McFall-Ngai M, Ruby E G. Vibrio fischeri lux genes play an important role in colonization and development of the host light organ. Journal of Bacteriology, 2000, 182(16): 4578–4586
Bahassi E M, O’Dea M H, Allali N, Messens J, Gellert M, Couturier M. Interactions of CcdB with DNA gyrase. Journal of Biological Chemistry, 1999, 274(16): 10936–10944
Dai L, Korolev K S, Gore J. Slower recovery in space before collapse of connected populations. Nature, 2013, 496(7445): 355–358
Ratzke C, Gore J. Self-organized patchiness facilitates survival in a cooperatively growing Bacillus subtilis population. Nature Microbiology, 2016: 16022
Wong C M, Zhou Y, Ng R W, Kung H F, Jin D Y. Cooperation of yeast peroxiredoxins Tsa1p and Tsa2p in the cellular defense against oxidative and nitrosative stress. Journal of Biological Chemistry, 2002, 277(7): 5385–5394
Boulant J A. Hypothalamic mechanisms in thermoregulation. Federation Proceedings, 1981, 40(14): 2843-50
Stephens P A, Frey-Roos F, Arnold W, Sutherland W J. Model complexity and population predictions. The alpine marmot as a case study. Journal of Animal Ecology, 2002, 71(2): 343–361
Liermann H, Hilborn. Depensation: Evidence, models and implications. Fish and Fisheries, 2001, 2(1): 33–58
Aizenman E, Engelberg-Kulka H, Glaser G. An Escherichia coli chromosomal “addiction module” regulated by guanosine 3',5'-bispyrophosphate: A model for programmed bacterial cell death. Proceedings of the National Academy of Sciences of the United States of America, 1996, 93(12): 6059–6063
Misselwitz B, Barrett N, Kreibich S, Vonaesch P, Andritschke D, Rout S, Weidner K, Sormaz M, Songhet P, Horvath P, Chabria M, Vogel V, Spori D M, Jenny P, Hardt W D. Near surface swimming of Salmonella typhimurium explains target-site selection and cooperative invasion. PLoS Pathogens, 2012, 8(7): e1002810
Tan C, Smith R P, Srimani J, Riccione K, Prasada S, Kuehn M, You L. The inoculum effect and band-pass bacterial response to periodic antibiotic treatment. Molecular Systems Biology, 2012, 8(1): 679–688
Lee H H, Molla M N, Cantor C R, Collins J J. Bacterial charity work leads to population-wide resistance. Nature, 2010, 467(7311): 82–85
Vega N M, Allison K R, Samuels A N, Klempner M S, Collins J J. Salmonella typhimurium intercepts Escherichia coli signaling to enhance antibiotic tolerance. Proceedings of the National Academy of Sciences of the United States of America, 2013, 110(35): 14420–14425
Meredith H R, Srimani J K, Lee A J, Lopatkin A J, You L. Collective antibiotic tolerance: Mechanisms, dynamics and intervention. Nature Chemical Biology, 2015, 11(3): 182–188
Nedelcu A M, Driscoll W W, Durand P M, Herron M D, Rashidi A. On the paradigm of altruistic suicide in the unicellular world. Evolution, 2011, 65(1): 3–20
Ackermann M, Stecher B, Freed N E, Songhet P, Hardt W D, Doebeli M. Self-destructive cooperation mediated by phenotypic noise. Nature, 2008, 454(7207): 987–990
Rice K C, Bayles K W. Death’s toolbox: Examining the molecular components of bacterial programmed cell death. Molecular Microbiology, 2003, 50(3): 729–738
Ameisen J C. The origin of programmed cell death. Science, 1996, 272(5266): 1278–1279
Brown S P, West S A, Diggle S P, Griffin A S. Social evolution in micro-organisms and a Trojan horse approach to medical intervention strategies. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 2009, 364(1533): 3157–3168
Moran N A, Degnan P H, Santos S R, Dunbar H E, Ochman H. The players in a mutualistic symbiosis: Insects, bacteria, viruses, and virulence genes. Proceedings of the National Academy of Sciences of the United States of America, 2005, 102(47): 16919–16926
Breznak J A. Symbiotic relationships between termites and their intestinal microbiota. Symposia of the Society for Experimental Biology, 1975, 29: 559–580
Glaser R. The intracellular bacteria of the cockroach in relation to symbiosis. Journal of Parasitology, 1946, 32(5): 483–489
Uhlig H H, Powrie F. Dendritic cells and the intestinal bacterial flora: a role for localized mucosal immune responses. Journal of Clinical Investigation, 2003, 112(5): 648–651
Wintermute E H, Silver P A. Dynamics in the mixed microbial concourse. Genes & Development, 2010, 24(23): 2603–2614
Wintermute E H, Silver P A. Emergent cooperation in microbial metabolism. Molecular Systems Biology, 2010, 6(1): 820–833
Shou W, Ram S, Vilar J M G. Synthetic cooperation in engineered yeast populations. Proceedings of the National Academy of Sciences of the United States of America, 2007, 104(6): 1877–1882
Brenner K, Karig D K, Weiss R, Arnold F H. Engineered bidirectional communication mediates a consensus in a microbial biofilm consortium. Proceedings of the National Academy of Sciences of the United States of America, 2007, 104(44): 17300–17304
Brenner K, You L, Arnold F H. Engineering microbial consortia: A new frontier in synthetic biology. Trends in Biotechnology, 2008, 26(9): 483–489
Hu B, Du J, Zou R Y, Yuan Y J. An environment-sensitive synthetic microbial ecosystem. PLoS One, 2010, 5(5): e10619
Kerner A, Park J, Williams A, Lin X N. A programmable Escherichia coli consortium via tunable symbiosis. PLoS One, 2012, 7(3): e34032
Mee M T, Collins J J, Church G M, Wang H H. Syntrophic exchange in synthetic microbial communities. Proceedings of the National Academy of Sciences of the United States of America, 2014, 111(20): 2149–2156
Berryman A A. The orgins and evolution of predator-prey theory. Ecology, 1992, 73(5): 1530–1535
Balagadde F K, Song H, Ozaki J, Collins C H, Barnet M, Arnold F H, Quake S R, You L. A synthetic Escherichia coli predator-prey ecosystem. Molecular Systems Biology, 2008, 4: 187
Wangersky P J. Lotka-Volterra population models. Annual Review of Ecology and Systematics, 1978, 9(1): 189–218
Sun G Q, Jin Z, Liu Q X, Li L. Dynamical complexity of a spatial predator-prey model with migration. Ecological Modelling, 2008, 219(1-2): 248–255
Yuan S, Xu C, Zhang T. Spatial dynamics in a predator-prey model with herd behavior. Chaos (Woodbury, N.Y.), 2013, 23(3): 033102
Song H, Payne S, Gray M, You L. Spatiotemporal modulation of biodiversity in a synthetic chemical-mediated ecosystem. Nature Chemical Biology, 2009, 5(12): 929–935
Yamamura N, Higashi M, Behera N, YuichiroWakano J. Evolution of mutualism through spatial effects. Journal of Theoretical Biology, 2004, 226(4): 421–428
Poisot T, Bever J D, Thrall P H, Hochberg M E. Dispersal and spatial heterogeneity allow coexistence between enemies and protective mutualists. Ecology and Evolution, 2014, 4(19): 3841–3850
Park J, Kerner A, Burns M A, Lin X N. Microdroplet-enabled highly parallel co-cultivation of microbial communities. PLoS One, 2011, 6(2): e17019
Wilson W, Morris W, Bronstein J. Coexistence of mutualists and exploiters on spatial landscapes. Ecological Monographs, 2003, 73(3): 397–413
Brenner K, Arnold F H. Self-organization, layered structure, and aggregation enhance persistence of a synthetic biofilm consortium. PLoS One, 2011, 6(2): e16791
Chuang J S, Rivoire O, Leibler S. Cooperation and Hamilton’s rule in a simple synthetic microbial system. Molecular Systems Biology, 2010, 6: 398
Chuang J S, Rivoire O, Leibler S. Simpson’s paradox in a synthetic microbial system. Science, 2009, 323(5911): 272–275
Gore J, Youk H, van Oudenaarden A. Snowdrift game dynamics and facultative cheating in yeast. Nature, 2009, 459(7244): 253–256
Griffin A S, West S A, Buckling A. Cooperation and competition in pathogenic bacteria. Nature, 2004, 430(7003): 1024–1027
West S A, Pen I, Griffin A S. Cooperation and competition between relatives. Science, 2002, 296(5565): 72–75
Celiker H, Gore J. Competition between species can stabilize public—goods cooperation within a species. Molecular Systems Biology, 2012, 8(1): 621
Bergstrom T, Blume L, Varian H. On the private provision of public goods. Journal of Public Economics, 1986, 29(1): 25–49
Driscoll W W, Pepper J W. Theory for the evolution of diffusible external goods. Evolution, 2010, 64(9): 2682–2687
Zhang F, Kwan A, Xu A, Süel G M. A synthetic quorum sensing system reveals a potential private benefit for public good production in a biofilm. PLoS One, 2015, 10(7): e0132948
Waite A J, Shou W. Adaptation to a new environment allows cooperators to purge cheaters stochastically. Proceedings of the National Academy of Sciences of the United States of America, 2012, 109(47): 19079–19086
Chen A, Sanchez A, Dai L, Gore J. Dynamics of a producerfreeloader ecosystem on the brink of collapse. Nature Communications, 2014, 5: 3713
Venturi V, Bertani I, Kerényi Á, Netotea S, Pongor S. Coswarming and local collapse: Quorum sensing conveys resilience to bacterial communities by localizing cheater mutants in Pseudomonas aeruginosa. PLoS One, 2010, 5(4): e9998
Bihary D, Tóth M, Kerényi Á, Venturi V, Pongor S. Modeling bacterial quorum sensing in open and closed environments: potential discrepancies between agar plate and culture flask experiments. Journal of Molecular Modeling, 2014, 20(7): 1–6
Pepper J W. The evolution of bacterial social life: From the ivory tower to the front lines of public health. Evolution, Medicine, and Public Health, 2014, 2014(1): 65–68
Ross-Gillespie A, Weigert M, Brown S P, Kümmerli R. Galliummediated siderophore quenching as an evolutionarily robust antibacterial treatment. Evolution, Medicine, and Public Health, 2014, 2014(1): 18–29
Hood M I, Skaar E P. Nutritional immunity: Transition metals at the pathogen-host interface. Nature Reviews. Microbiology, 2012, 10(8): 525–537
Skaar E P. The battle for iron between bacterial pathogens and their vertebrate hosts. PLoS Pathogens, 2010, 6(8): e1000949
Köhler T, Buckling A, van Delden C. Cooperation and virulence of clinical Pseudomonas aeruginosa populations. Proceedings of the National Academy of Sciences of the United States of America, 2009, 106(15): 6339–6344
Merlo L M F, Pepper J W, Reid B J, Maley C C. Cancer as an evolutionary and ecological process. Nature Reviews. Cancer, 2006, 6(12): 924–935
Pepper J W. Defeating pathogen drug resistance: Guidance from evolutionary theory. Evolution, 2008, 62(12): 3185–3191
Boehm T, Folkman J, Browder T, O’Reilly M S. Antiangiogenic therapy of experimental cancer does not induce acquired drug resistance. Nature, 1997, 390(6658): 404–407
Folkman J. Angiogenesis. Annual Review of Medicine, 2006, 57: 1–18
Duan F, March J C. Engineered bacterial communication prevents Vibrio cholerae virulence in an infant mouse model. Proceedings of the National Academy of Sciences of the United States of America, 2010, 107(25): 11260–11264
Saeidi N, Wong C K, Lo T M, Nguyen H X, Ling H, Leong S S J, Poh C L, Chang MW. Engineering microbes to sense and eradicate Pseudomonas aeruginosa, a human pathogen. Molecular Systems Biology, 2011, 7(1): 521
Acknowledgements
Our research is supported by a President’s Faculty Research and Development Grant #335318 and #335304 through Nova Southeastern University. The author’s declare that they do not have any conflicts of interest.
Author information
Authors and Affiliations
Corresponding author
Additional information
Dr. Robert P. Smith completed his undergraduate and graduate studies at Carleton University in Ottawa, Ontario, Canada. During his PhD, he worked with Dr. Myron Smith and studied nonself recognition in the filamentous fungus Neurospora crassa. He then transitioned to a post-doctoral position at Duke University where he was a Duke Scholar in Infectious Disease. Under the guidance of Dr. Lingchong You, he used systems and synthetic biology approaches to study antibiotic resistance and cooperation. Currently, Robert is an Assistant Professor in the Department of Biological Sciences at Nova Southeastern University in Fort Lauderdale, Florida. Work performed in his lab focuses primarily on using a synthetic biology approach to understand the principles driving intra- and interspecific cooperation.
Rights and permissions
About this article
Cite this article
Dressler, M.D., Clark, C.J., Thachettu, C.A. et al. Synthetically engineered microbes reveal interesting principles of cooperation. Front. Chem. Sci. Eng. 11, 3–14 (2017). https://doi.org/10.1007/s11705-016-1605-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11705-016-1605-z