Cutting through the complexity of cell collectives

Proceedings of the Royal Society B: Biological Sciences

Volumn 280, Issue 1755, 2013, Pages

  Nadell, Carey D ^a   Bucci, Vanni ^b   Drescher, Knut ^a   Levin, Simon A ^a   Bassler, Bonnie L ^a,c   Xavier, João B ^b  

^a PRINCETON UNIVERSITY   (United States)

^b MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

Biofilm; Cancer; Collective behaviour; Cooperation; Emergence; Evolution

Indexed keywords

BACTERIUM; BIOFILM; CANCER; ENZYME ACTIVITY; EVOLUTIONARY THEORY; SECRETION; VIRULENCE;

BACTERIA (MICROORGANISMS);

EID: 84879066613     PISSN: 09628452     EISSN: 14712954     Source Type: Journal    
DOI: 10.1098/rspb.2012.2770     Document Type: Review

References (95)

1. Flierl G, Grünbaum D, Levins S, Olson D. 1999 From individuals to aggregations: the interplay between behavior and physics. J. Theor. Biol. 196, 397-454. (doi:10.1006/jtbi.1998.0842)
2. Sumpter DJ. 2006 The principles of collective animal behaviour. Phil. Trans. R. Soc. B 361, 5-22. (doi:10. 1098/rstb.2005.1733)
3. Couzin I. 2007 Collective minds. Nature 445, 715. (doi:10.1038/445715a)
4. Vicsek T, Zafeiris A. 2012 Collective motion. Phys. Rep. 517, 71-140. (doi:10.1016/j.physrep.2012. 03.004)
5. Bonner JT. 1955 Cells and societies. Princeton, NJ: Princeton University Press.
6. Deisboeck TS, Couzin ID. 2009 Collective behavior in cancer cell populations. Bioessays 31, 190-197. (doi:10.1002/bies.200800084)
7. Nadell CD, Xavier JB, Foster KR. 2009 The sociobiology of biofilms. FEMS Microbiol. Rev. 33, 206-224. (doi:10.1111/j.1574-6976. 2008.00150.x)
8. Sachs JL, Skophammer RG, Regus JU. 2011 Evolutionary transitions in bacterial symbiosis. Proc. Natl Acad. Sci. USA 108, 10 800-10 807. (doi:10. 1073/pnas.1100304108)
9. Fanning S, Mitchell AP. 2012 Fungal biofilms. PLoS Pathog. 8, e1002585. (doi:10.1371/journal. ppat.1002585)
10. Levin SA. 2003 Complex adaptive systems: exploring the known, the unknown, and the unknowable. Bull. Am. Math. Soc. 40, 3-19. (doi:10.1090/S0273-0979-02-00965-5)
11. Thiery JP, Chopin D. 1999 Epithelial cell plasticity in development and tumor progression. Cancer Metastasis. Rev. 18, 31-42. (doi:10.1023/ A:1006256219004)
12. Eichenberger P et al. 2004 The program of gene transcription for a single differentiating cell type during sporulation in Bacillus subtilis. PLoS Biol. 2, e328. (doi:10.1371/journal.pbio.0020328)
13. Waters CM, Bassler BL. 2005 Quorum sensing: cell-to-cell communication in bacteria. Annu. Rev. Cell Dev. Biol. 21, 319-346. (doi:10.1146/annurev. cellbio.21.012704.131001)
14. Battesti A, Majdalani N, Gottesman S. 2011 The RpoS-mediated general stress response in Escherichia coli. Ann. Rev. Microbiol. 65, 189-213. (doi:10.1146/annurev-micro-090110-102946)
15. Kreft JU. 2004 Conflicts of interest in biofilms. Biofilms 1, 265-276. (doi:10.1017/S1479050 504001486)
16. West SA, Griffin AS, Gardner A, Diggle SP. 2006 Social evolution theory for microorganisms. Nat. Rev. Microbiol. 4, 597-607. (doi:10.1038/ nrmicro1461)
17. Merlo LMF, Pepper JW, Reid BJ, Maley CC. 2006 Cancer as an evolutionary and ecological process. Nat. Rev. Cancer 6, 924-935. (doi:10.1038/nrc2013)
18. Xavier JB. 2011 Social interaction in synthetic and natural microbial communities. Mol. Syst. Biol. 7, 483. (doi:10.1038/msb.2011.16)
19. Le Gac M, Plucain J, Hindre T, Lenski RE, Schneider D. 2012 Ecological and evolutionary dynamics of coexisting lineages during a long-term experiment with Escherichia coli. Proc. Natl Acad. Sci. USA 109, 9487-9492. (doi:10.1073/pnas.1207091109)
20. Toner J, Tu YH. 1998 Flocks, herds, and schools: a quantitative theory of flocking. Phys. Rev. E 58, 4828-4858. (doi:10.1103/PhysRevE.58.4828)
21. Ramaswamy S. 2010 The mechanics and statistics of active matter. Annu. Rev. Condens. Matter Phys. 1, 323-345. (doi:10.1146/annurev-conmatphys-070 909-104101)
22. Wensink HH, Dunkel Jr, Heidenreich S, Drescher K, Goldstein RE, Löwen H, Yeomans JM. 2012 Meso-scale turbulence in living fluids. Proc. Natl Acad. Sci. USA 109, 14 308-14 313. (doi:10.1073/pnas. 1202032109)
23. Moon SJ, Nabet B, Leonard NE, Levin SA, Kevrekidis IG. 2007 Heterogeneous animal group models and their group-level alignment dynamics: an equation-free approach. J. Theor. Biol. 246, 100-112. (doi:10.1016/j.jtbi.2006.12.018)
24. Nabet B, Leonard NE, Couzin ID, Levin SA. 2009 Dynamics of decision making in animal group motion. J. Nonlinear Sci. 19, 399-435. (doi:10.1007/s00332-008-9038-6)
25. Raghib M, Levin SA, Kevrekidis IG. 2010 Multiscale analysis of collective motion and decision-making in swarms: an advection-diffusion equation with memory approach. J. Theor. Biol. 264, 893-913. (doi:10.1016/j.jtbi.2010.02.030)
26. Sachs JL, Mueller UG, Wilcox TP, Bull JJ. 2004 The evolution of cooperation. Q. Rev. Biol. 79, 135-160. (doi:10.1086/383541)
27. West SA, Griffin AS, Gardner A. 2007 Evolutionary explanations for cooperation. Curr. Biol. 17, R661-R672. (doi:10.1016/j.cub.2007.06.004)
28. Gardner A, Foster KR. 2008 The evolution and ecology of cooperation: history and concepts. In Ecology of social evolution (eds J Korb, J Heinze), pp. 1-36. Berlin, Germany: Springer.
29. Wenseleers T, Gardner A, Foster KR. 2010 Social evolution theory: a review of methods and approaches. In Social behaviour: genes, ecology and evolution (eds T Szekely, AJ Moore, J Komdeur), pp. 132-158. Cambridge, UK: Cambridge University Press.
30. Griffin AS, West SA. 2002 Kin selection: fact and fiction. Trends Ecol. Evol. 17, 15-21. (doi:10.1016/S0169-5347(01)02355-2)
31. Griffin AS, West SA, Buckling A. 2004 Cooperation and competition in pathogenic bacteria. Nature 430, 1024-1027. (doi:10.1038/nature02744)
32. Smith J, Van Dyken JD, Zee PC. 2010 A generalization of Hamilton's rule for the evolution of microbial cooperation. Science 328, 1700-1703. (doi:10.1126/science.1189675)
33. Damore JA, Gore J. 2012 Understanding microbial cooperation. J. Theor. Biol. 299, 31-41. (doi:10.1016/j.jtbi.2011.03.008)
34. Xavier JB, Picioreanu C, van Loosdrecht MCM. 2005 A framework for multidimensional modelling of activity and structure of multispecies biofilms. Environ. Microbiol. 7, 1085-1103. (doi:10.1111/j. 1462-2920.2005.00787.x)
35. Lardon LA, Merkey BV, Martins S, Dötsch A, Picioreanu C, Kreft J-U, Smets BF. 2011 iDynoMiCS: next-generation individual-based modelling of biofilms. Environ. Microbiol. 13, 2416-2434. (doi:10.1111/j.1462-2920.2011.02414.x)
36. Buckingham E. 1914 On physically similar systems; illustrations of the use of dimensional equations. Phys. Rev. 4, 345-376. (doi:10.1103/ PhysRev.4.345)
37. Stahl WR. 1962 Similarity and dimensional methods in biology. Science 137, 205-212. (doi:10.1126/science.137.3525.205)
38. Bird R, Stewart W, Lightfoot E. 1960 Transport phenomena. New York, NY: Wiley.
39. Guasto JS, Rusconi R, Stocker R. 2012 Fluid mechanics of planktonic microorganisms. Annu. Rev. Fluid Mech. 44, 373-400. (doi:10.1146/annurev-fluid-120710-101156)
40. Stewart PS. 2012 Mini-review: convection around biofilms. Biofouling 28, 187-198. (doi:10.1080/08927014.2012.662641)
41. Purcell EM. 1977 Life at low Reynolds number. Am. J. Phys. 45, 3-11. (doi:10.1119/1.10903)
42. Nadell CD, Foster KR, Xavier JB. 2010 Emergence of spatial structure in cell groups and the evolution of cooperation. PLoS Comput. Biol. 6, e1000716. (doi:10.1371/journal.pcbi.1000716)
43. Picioreanu C, van Loosdrecht MCM, Heijnen JJ. 1998 Mathematical modeling of biofilm structure with a hybrid differential-discrete cellular automaton approach. Biotechnol. Bioeng. 58, 101-116. (doi:10. 1002/(SICI)1097-0290(19980405)58:1,101::AID-BIT11.3.0.CO;2-M)
44. Hallatschek O, Nelson DR. 2008 Gene surfing in expanding populations. Theor. Popul. Biol. 73, 158-170. (doi:10.1016/j.tpb.2007.08.008)
45. Hallatschek O. 2011 The noisy edge of traveling waves. Proc. Natl Acad. Sci. USA 108, 1783-1787. (doi:10.1073/pnas.1013529108)
46. Nadell CD, Bassler BL. 2011 A fitness trade-off between local competition and dispersal in Vibrio cholerae biofilms. Proc. Natl Acad. Sci. USA 108, 14181-14185. (doi:10.1073/pnas. 101111147108)
47. Hallatschek O, Hersen P, Ramanathan S, Nelson DR. 2007 Genetic drift at expanding frontiers promotes gene segregation. Proc. Natl Acad. Sci. USA 104, 19926-19 930. (doi:10.1073/pnas.0710150104)
48. Korolev KS, Xavier JoB, Nelson DR, Foster KR. 2011 A Quantitative test of population genetics using spatiogenetic patterns in bacterial colonies. Am. Nat. 178, 538-552. (doi:10.1086/661897)
49. Buttery NJ, Jack CN, Adu-Oppong B, Snyder KT, Thompson CRL, Queller DC, Strassmann JE. 2012 Structured growth and genetic drift raise relatedness in the social amoeba Dictyostelium discoideum. Biol. Lett. 8, 794-797. (doi:10.1098/ rsbl.2012.0421)
50. Korolev KS, Müller MJI, Karahan N, Murray AW, Hallatschek O, Nelson DR. 2012 Selective sweeps in growing microbial colonies. Phys. Biol. 9, 026008. (doi:10.1088/1478-3975/9/2/026008)
51. Lehe R, Hallatschek O, Peliti L. 2012 The rate of beneficial mutations surfing on the wave of a range expansion. PLoS Comp. Biol. 8, e1002447. (doi:10. 1371/journal.pcbi.1002447)
52. Gerrish PJ, Lenski RE. 1998 The fate of competing beneficial mutations in an asexual population. Genetica 102-3, 127-144. (doi:10.1023/a:10170 67816551)
53. Desai MM, Fisher DS. 2007 Beneficial mutation-selection balance and the effect of linkage on positive selection. Genetics 176, 1759-1798. (doi:10.1534/genetics.106.067678)
54. Desai MM, Fisher DS, Murray AW. 2007 The speed of evolution and maintenance of variation in asexual populations. Curr. Biol. 17, 385-394. (doi:10.1016/ j.cub.2007.01.072)
55. Martens EA, Hallatschek O. 2011 Interfering waves of adaptation promote spatial mixing. Genetics 189, 1045-1060. (doi:10.1534/genetics.111.130112)
56. Fisher RA. 1937 The wave of advance of advantageous genes. Ann. Eugen. 7, 355-369. (doi:10.1111/j.1469-1809.1937.tb02153.x)
57. Kolmogorov AN, Petrovskii IG, Piskunov NS. 1937 A study of the equation of diffusion with increase in the quantity of matter, and its application to a biological problem. Bull. Moscow Univ. Math. Ser. A 1, 713-719.
58. Martens EA, Kostadinov R, Maley CC, Hallatschek O. 2011 Spatial structure increases the waiting time for cancer. New J. Phys. 13, 115014. (doi:10.1088/ 1367-2630/13/11/115014)
59. Axelrod R, Axelrod DE, Pienta KJ. 2006 Evolution of cooperation among tumor cells. Proc. Natl Acad. Sci. USA 103, 13474-13479. (doi:10.1073/pnas. 0606053103)
60. Ng W-L, Bassler BL. 2009 Bacterial quorum-sensing network architectures. Ann. Rev. Genet. 43, 197-222. (doi:10.1146/annurev-genet-102108-134304)
61. Pai A, You L. 2009 Optimal tuning of bacterial sensing potential. Mol. Syst. Biol. 5, 286. (doi:10. 1038/msb.2009.43)
62. Nadell CD, Xavier JB, Levin SA, Foster KR. 2008 The evolution of quorum sensing in bacterial biofilms. PLoS Biol. 6, e14. (doi:10.1371/journal. pbio.0060014)
63. Redfield RJ. 2002 Is quorum sensing a side effect of diffusion sensing? Trends Microbiol. 10, 365-370. (doi:10.1016/S0966-842X(02)02400-9)
64. Hense BA, Kuttler C, Muller J, Rothballer M, Hartmann A, Kreft J-U. 2007 Does efficiency sensing unify diffusion and quorum sensing? Nat. Rev. Microbiol. 5, 230-239. (doi:10.1038/nrmicro1600)
65. Sandoz KM, Mitzimberg SM, Schuster M. 2007 Social cheating in Pseudomonas aeruginosa quorum sensing. Proc. Natl Acad. Sci. USA 104, 15876-15881. (doi:10.1073/pnas.0705653104)
66. Diggle S, Griffin A, Campbell G, West S. 2007 Cooperation and conflict in quorum-sensing bacterial populations. Nature 450, 411-414. (doi:10.1038/nature06279)
67. Stevens AM, Schuster M, Rumbaugh KP. 2012 Working together for the common good: cell-cell communication in bacteria. J. Bacteriol. 194, 2131-2141. (doi:10.1128/jb.00143-12)
68. Wilder CN, Diggle SP, Schuster M. 2011 Cooperation and cheating in Pseudomonas aeruginosa: the roles of the las, rhl and pqs quorum-sensing systems. Isme J. 5, 1332-1343. (doi:10.1038/ismej.2011.13)
69. Popat R, Crusz SA, Messina M, Williams P, West SA, Diggle SP. 2012 Quorum-sensing and cheating in bacterial biofilms. Proc. R. Soc. B 279, 4765-4771. (doi:10.1098/rspb.2012.1976)
70. Rumbaugh KP, Diggle SP, Watters CM, Ross-Gillespie A, Griffin AS, West SA. 2009 Quorum sensing and the social evolution of bacterial virulence. Curr. Biol. 19, 341-345. (doi:10.1016/j.cub.2009.01.050)
71. Gore J, Youk H, van Oudenaarden A. 2009 Snowdrift game dynamics and facultative cheating in yeast. Nature 459, 253-256. (doi:10.1038/nature07921)
72. MaClean RC, Fuentes-Hernandez A, Greig D, Hurst LD, Gudelj I. 2010 A mixture of 'cheats' and 'co-operators' can enable maximal group benefit. PLoS Biol. 8, e1000486. (doi:10.1371/journal.pbio. 1000486)
73. Driscoll WW, Pepper JW. 2010 Theory for the evolution of diffusible external goods. Evolution 64, 2682-2687. (doi:10.1111/j.1558-5646.2010. 01002.x)
74. Bucci V, Nadell CD, Xavier JB. 2011 The evolution of bacteriocin production in bacterial biofilms. Am. Nat. 178, E162-E173. (doi:10.1086/662668)
75. Allison SD. 2005 Cheaters, diffusion and nutrients constrain decomposition by microbial enzymes in spatially structured environments. Ecol. Lett. 8, 626-635. (doi:10.1111/j.1461-0248.2005.00756.x)
76. Songsiriritthigul C, Pantoom S, Aguda AH, Robinson RC, Suginta W. 2008 Crystal structures of Vibrio harveyi chitinase A complexed with chitooligosaccharides: implications for the catalytic mechanism. J. Struct. Biol. 162, 491-499. (doi:10. 1016/j.jsb.2008.03.008)
77. de la Torre JG, Huertas ML, Carrasco B. 2000 Calculation of hydrodynamic properties of globular proteins from their atomic-level structure. Biophys. J. 78, 719-730. (doi:10.1016/S0006-3495(00) 76630-6)
78. Groves P, Rasmussen MO, Molero MD, Samain E, Canada FJ, Driguez H, Jimenez-Barbero J. 2004 Diffusion ordered spectroscopy as a complement to size exclusion chromatography in oligosaccharide analysis. Glycobiology 14, 451-456. (doi:10.1093/ glycob/cwh037)
79. Schuster S, Kreft J-U, Brenner N, Wessely F, Theißen G, Ruppin E, Schroeter A. 2010 Cooperation and cheating in microbial exoenzyme production: theoretical analysis for biotechnological applications. Biotechnol. J. 5, 751-758. (doi:10.1002/biot. 200900303)
80. Hamilton WD. 1964 The genetical evolution of social behaviour I & II. J. Theor. Biol. 7, 1-52. (doi:10.1016/0022-5193(64)90038-4)
81. Price GR. 1970 Selection and covariance. Nature 227, 520-521. (doi:10.1038/227520a0)
82. Hamilton WD. 1970 Selfish and spiteful behavior in an evolutionary model. Nature 228, 1218-1220. (doi:10.1038/2281218a0)
83. Hamilton WD. 1972 Altruism and related phenomena, mainly in social insects. Ann. Rev. Ecol. Syst. 3, 192-232. (doi:10.1146/annurev.es.03. 110172.001205)
84. Queller DC. 1994 Genetic relatedness in viscous 11populations. Evol. Ecol. 8, 70-73. (doi:10.1007/ BF01237667)
85. Frank SA. 1998 The foundations of social evolution. Princeton, NJ: Princeton University Press.
86. Gardner A. 2008 The Price equation. Curr. Biol. 18, R198-R202. (doi:10.1016/j.cub.2008.01.005)
87. Pepper JW. 2000 Relatedness in trait group models of social evolution. J. Theor. Biol. 206, 355-368. (doi:10.1006/jtbi.2000.2132)
88. Xavier JB, De Kreuk MK, Picioreanu C, Van Loosdrecht MCM. 2007 Multi-scale individual-based model of microbial and bioconversion dynamics in aerobic granular sludge. Environ. Sci. Technol. 41, 6410-6417. (doi:10.1021/es070264m)
89. Brockhurst MA, Habets MGJL, Libberton B, Buckling A, Gardner A. 2010 Ecological drivers of the evolution of public-goods cooperation in bacteria. Ecology 91, 334-340. (doi:10.1890/09-0293.1)
90. Xavier JB, Foster KR. 2007 Cooperation and conflict in microbial biofilms. Proc. Natl Acad. Sci. USA 104, 876-881. (doi:10.1073/pnas.0607651104)
91. Brown SP, Johnstone R. 2001 Cooperation in the dark: signalling and collective action in quorum-sensing bacteria. Proc. R. Soc. Lond. B 268, 961-965. (doi:10.1098/rspb.2001.1609)
92. Kuemmerli R, Brown SP. 2010 Molecular and regulatory properties of a public good shape the evolution of cooperation. Proc. Natl Acad. Sci. USA 107, 18 921-18 926. (doi:10.1073/pnas. 1011154107)
93. Xavier JB, Kim W, Foster KR. 2011 A molecular mechanism that stabilizes cooperative secretions in Pseudomonas aeruginosa. Mol. Microbiol. 79, 166-179. (doi:10.1111/j.1365-2958.2010.07436.x)
94. Brown SP, Taddei F. 2007 The durability of public goods changes the dynamics and nature of social dilemmas. PLoS ONE 2, e593. (doi:10.1371/journal. pone.0000593)
95. Foster KR. 2004 Diminishing returns in social evolution: the not-so-tragic commons. J. Evol. Biol. 17, 1058-1072. (doi:10.1111/j.1420-9101.2004. 00747.x)