Frontiers of Chemical Science and Engineering >
Synthetically engineered microbes reveal interesting principles of cooperation
Received date: 31 May 2016
Accepted date: 21 Sep 2016
Published date: 17 Mar 2017
Copyright
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.
Key words: synthetic biology; engineered bacteria; cooperation; cheater; quorum sensing
Michael D. Dressler , Corey J. Clark , Chelsea A. Thachettu , Yasmine Zakaria , Omar Tonsi Eldakar , Robert P. Smith . Synthetically engineered microbes reveal interesting principles of cooperation[J]. Frontiers of Chemical Science and Engineering, 2017 , 11(1) : 3 -14 . DOI: 10.1007/s11705-016-1605-z
1 |
Nowak M A. Five rules for the evolution of cooperation. Science, 2006, 314(5805): 1560–1563
|
2 |
Axelrod R, Hamilton W D. The evolution of cooperation. Science, 1981, 211(4489): 1390–1396
|
3 |
Fehr E, Fischbacher U. Social norms and human cooperation. Trends in Cognitive Sciences, 2004, 8(4): 185–190
|
4 |
Shan W, Hamilton W. Country—specific advantage and international cooperation. Strategic Management Journal, 1991, 12(6): 419–432
|
5 |
Hardin G. The tragedy of the commons. Science, 1968, 162(3859): 1243–1248
|
6 |
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
|
7 |
Hamilton W. The evolution of altruistic behavior. American Naturalist, 1963, 97(896): 354–356
|
8 |
Eldakar O T, Wilson D S. Eight criticisms not to make about group selection. Evolution, 2011, 65(6): 1523–1526
|
9 |
Wilson D S, Wilson E O. Rethinking the theoretical foundation of sociobiology. Quarterly Review of Biology, 2007, 82(4): 327–348
|
10 |
Rapoport A, Chammah A M. Prisoner’s dilemma: A study in conflict and cooperation. Michigan: University of Michigan press, 1965: 31–44
|
11 |
Doebeli M, Hauert C. Models of cooperation based on the Prisoner’s Dilemma and the Snowdrift game. Ecology Letters, 2005, 8(7): 748–766
|
12 |
Allee W C. Cooperation among animals. American Journal of Sociology, 1951, 1: 93–95
|
13 |
Seger J. Cooperation and conflict in social insects. Behavioural Ecology: An Evolutionary Approach, 1991, 338–373
|
14 |
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
|
15 |
Gintis H, Bowles S, Boyd R, Fehr E. Explaining altruistic behavior in humans. Evolution and Human Behavior, 2003, 24(3): 153–172
|
16 |
Sober E, Wilson D S. Unto others: The evolution and psychology of unselfish behavior. Massachusetts: Harvard University Press, 1999, 6–14
|
17 |
Tanouchi Y, Smith R, You L. Engineering microbial systems to explore ecological and evolutionary dynamics. Current Opinion in Biotechnology, 2012, 23(5): 791–797
|
18 |
Benner S A, Sismour A M. Synthetic biology. Nature Reviews. Genetics, 2005, 6(7): 533–543
|
19 |
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
|
20 |
Khalil A S, Collins J J. Synthetic biology: Applications come of age. Nature Reviews. Genetics, 2010, 11(5): 367–379
|
21 |
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
|
22 |
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
|
23 |
Pianka E R. On r- and K-selection. American Naturalist, 1970, 104(940): 592–597
|
24 |
Miller M B, Bassler B L. Quorum sensing in bacteria. Annual Review of Microbiology, 2001, 55(1): 165–199
|
25 |
Berendsen R L, Pieterse C M, Bakker P A. The rhizosphere microbiome and plant health. Trends in Plant Science, 2012, 17(8): 478–486
|
26 |
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
|
27 |
De Kievit T R, Gillis R, Marx S, Brown C, Iglewski B H. Quorum-sensing genes in Pseudomonas aeruginosa biofilms: Their role and expression patterns. Applied and Environmental Microbiology, 2001, 67(4): 1865–1873
|
28 |
De Kievit T R, Iglewski B H. Bacterial quorum sensing in pathogenic relationships. Infection and Immunity, 2000, 68(9): 4839–4849
|
29 |
Stewart P S, Costerton J W. Antibiotic resistance of bacteria in biofilms. Lancet, 2001, 358(9276): 135–138
|
30 |
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
|
31 |
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
|
32 |
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
|
33 |
Allee W, Emerson A, Park O, Park T, Schmidt K. Principles of Animal Ecology. Philadelphia, Pennsylvania, USA, 1949, 416–425
|
34 |
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
|
35 |
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
|
36 |
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
|
37 |
Tobin P C, Berec L, Liebhold A M. Exploiting Allee effects for managing biological invasions. Ecology Letters, 2011, 14(6): 615–624
|
38 |
Hackney E E, McGraw J B. Experimental demonstration of an Allee effect in American ginseng. Conservation Biology, 2001, 15(1): 129–136
|
39 |
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
|
40 |
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
|
41 |
Myers R, Barrowman N, Hutchings J, Rosenberg A. Population dynamics of exploited fish stocks at low population levels. Science, 1995, 269(5227): 1106–1108
|
42 |
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
|
43 |
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
|
44 |
Liebhold A M, Tobin P C. Population ecology of insect invasions and their management. Annual Review of Entomology, 2008, 53(1): 387–408
|
45 |
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
|
46 |
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
|
47 |
Dai L, Korolev K S, Gore J. Slower recovery in space before collapse of connected populations. Nature, 2013, 496(7445): 355–358
|
48 |
Ratzke C, Gore J. Self-organized patchiness facilitates survival in a cooperatively growing Bacillus subtilis population. Nature Microbiology, 2016: 16022
|
49 |
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
|
50 |
Boulant J A. Hypothalamic mechanisms in thermoregulation. Federation Proceedings, 1981, 40(14): 2843-50
|
51 |
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
|
52 |
Liermann H, Hilborn. Depensation: Evidence, models and implications. Fish and Fisheries, 2001, 2(1): 33–58
|
53 |
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
|
54 |
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
|
55 |
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
|
56 |
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
|
57 |
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
|
58 |
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
|
59 |
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
|
60 |
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
|
61 |
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
|
62 |
Ameisen J C. The origin of programmed cell death. Science, 1996, 272(5266): 1278–1279
|
63 |
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
|
64 |
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
|
65 |
Breznak J A. Symbiotic relationships between termites and their intestinal microbiota. Symposia of the Society for Experimental Biology, 1975, 29: 559–580
|
66 |
Glaser R. The intracellular bacteria of the cockroach in relation to symbiosis. Journal of Parasitology, 1946, 32(5): 483–489
|
67 |
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
|
68 |
Wintermute E H, Silver P A. Dynamics in the mixed microbial concourse. Genes & Development, 2010, 24(23): 2603–2614
|
69 |
Wintermute E H, Silver P A. Emergent cooperation in microbial metabolism. Molecular Systems Biology, 2010, 6(1): 820–833
|
70 |
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
|
71 |
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
|
72 |
Brenner K, You L, Arnold F H. Engineering microbial consortia: A new frontier in synthetic biology. Trends in Biotechnology, 2008, 26(9): 483–489
|
73 |
Hu B, Du J, Zou R Y, Yuan Y J. An environment-sensitive synthetic microbial ecosystem. PLoS One, 2010, 5(5): e10619
|
74 |
Kerner A, Park J, Williams A, Lin X N. A programmable Escherichia coli consortium via tunable symbiosis. PLoS One, 2012, 7(3): e34032
|
75 |
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
|
76 |
Berryman A A. The orgins and evolution of predator-prey theory. Ecology, 1992, 73(5): 1530–1535
|
77 |
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
|
78 |
Wangersky P J. Lotka-Volterra population models. Annual Review of Ecology and Systematics, 1978, 9(1): 189–218
|
79 |
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
|
80 |
Yuan S, Xu C, Zhang T. Spatial dynamics in a predator-prey model with herd behavior. Chaos (Woodbury, N.Y.), 2013, 23(3): 033102
|
81 |
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
|
82 |
Yamamura N, Higashi M, Behera N, Yuichiro Wakano J. Evolution of mutualism through spatial effects. Journal of Theoretical Biology, 2004, 226(4): 421–428
|
83 |
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
|
84 |
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
|
85 |
Wilson W, Morris W, Bronstein J. Coexistence of mutualists and exploiters on spatial landscapes. Ecological Monographs, 2003, 73(3): 397–413
|
86 |
Brenner K, Arnold F H. Self-organization, layered structure, and aggregation enhance persistence of a synthetic biofilm consortium. PLoS One, 2011, 6(2): e16791
|
87 |
Chuang J S, Rivoire O, Leibler S. Cooperation and Hamilton’s rule in a simple synthetic microbial system. Molecular Systems Biology, 2010, 6: 398
|
88 |
Chuang J S, Rivoire O, Leibler S. Simpson’s paradox in a synthetic microbial system. Science, 2009, 323(5911): 272–275
|
89 |
Gore J, Youk H, van Oudenaarden A. Snowdrift game dynamics and facultative cheating in yeast. Nature, 2009, 459(7244): 253–256
|
90 |
Griffin A S, West S A, Buckling A. Cooperation and competition in pathogenic bacteria. Nature, 2004, 430(7003): 1024–1027
|
91 |
West S A, Pen I, Griffin A S. Cooperation and competition between relatives. Science, 2002, 296(5565): 72–75
|
92 |
Celiker H, Gore J. Competition between species can stabilize public—goods cooperation within a species. Molecular Systems Biology, 2012, 8(1): 621
|
93 |
Bergstrom T, Blume L, Varian H. On the private provision of public goods. Journal of Public Economics, 1986, 29(1): 25–49
|
94 |
Driscoll W W, Pepper J W. Theory for the evolution of diffusible external goods. Evolution, 2010, 64(9): 2682–2687
|
95 |
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
|
96 |
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
|
97 |
Chen A, Sanchez A, Dai L, Gore J. Dynamics of a producer-freeloader ecosystem on the brink of collapse. Nature Communications, 2014, 5: 3713
|
98 |
Venturi V, Bertani I, Kerényi Á, Netotea S, Pongor S. Co-swarming and local collapse: Quorum sensing conveys resilience to bacterial communities by localizing cheater mutants in Pseudomonas aeruginosa. PLoS One, 2010, 5(4): e9998
|
99 |
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
|
100 |
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
|
101 |
Ross-Gillespie A, Weigert M, Brown S P, Kümmerli R. Gallium-mediated siderophore quenching as an evolutionarily robust antibacterial treatment. Evolution, Medicine, and Public Health, 2014, 2014(1): 18–29
|
102 |
Hood M I, Skaar E P. Nutritional immunity: Transition metals at the pathogen-host interface. Nature Reviews. Microbiology, 2012, 10(8): 525–537
|
103 |
Skaar E P. The battle for iron between bacterial pathogens and their vertebrate hosts. PLoS Pathogens, 2010, 6(8): e1000949
|
104 |
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
|
105 |
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
|
106 |
Pepper J W. Defeating pathogen drug resistance: Guidance from evolutionary theory. Evolution, 2008, 62(12): 3185–3191
|
107 |
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
|
108 |
Folkman J. Angiogenesis. Annual Review of Medicine, 2006, 57: 1–18
|
109 |
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
|
110 |
Saeidi N, Wong C K, Lo T M, Nguyen H X, Ling H, Leong S S J, Poh C L, Chang M W. Engineering microbes to sense and eradicate Pseudomonas aeruginosa, a human pathogen. Molecular Systems Biology, 2011, 7(1): 521
|
/
〈 | 〉 |