Mechanically-driven phase separation in a growing bacterial colony

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 17, 2015, Pages E2166-E2173

  Ghosh, Pushpita ^a   Mondal, Jagannath ^b   Ben Jacob, Eshel ^a,c   Levine, Herbert ^a,d  

^a RICE UNIVERSITY   (United States)

^b Department of Chemistry Columbia University ^*  (United States)

^c TEL AVIV UNIVERSITY   (Israel)

^d Rice University   (United States)

Author keywords

Biofilms; Depletion interaction; Extracellular polymeric substance; Mechanical interaction; Phase separation

Indexed keywords

ARTICLE; BACTERIAL CELL; BACTERIAL GROWTH; BACTERIUM COLONY; CELL AGGREGATION; CELL DIVISION; CELL INTERACTION; COMPARATIVE STUDY; CONTROLLED STUDY; DIFFUSION; EXTRACELLULAR MATRIX; EXTRACELLULAR POLYMERIC SUBSTANCE; GRAM POSITIVE ASPOROGENOUS ROD-SHAPED BACTERIA; NONHUMAN; PHASE SEPARATION; PRIORITY JOURNAL; BACTERIAL PHENOMENA AND FUNCTIONS; BACTERIUM; BIOFILM; BIOLOGICAL MODEL; GROWTH, DEVELOPMENT AND AGING;

BACTERIA (MICROORGANISMS);

BACTERIA; BACTERIAL PHYSIOLOGICAL PHENOMENA; BIOFILMS; MODELS, BIOLOGICAL;

EID: 84928549171     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1504948112     Document Type: Article

References (42)

1. Cross MC, Hohenberg PC (1993) Pattern formation outside of equilibrium. Rev Mod Phys 65(3):851-1123.
2. Vicsek T, Zafeiris A (2012) Collective motion. Phys Rep 517(3-4):71-140.
3. Marchetti MC, et al. (2013) Hydrodynamics of soft active matter. Rev Mod Phys 85(3):1143-1189.
4. Zhang HP, Be'er A, Florin EL, Swinney HL (2010) Collective motion and density fluctuations in bacterial colonies. Proc Natl Acad Sci USA 107(31):13626-13630.
5. Basan M, Elgeti J, Hannezo E, Rappel WJ, Levine H (2013) Alignment of cellular motility forces with tissue flow as a mechanism for efficient wound healing. Proc Natl Acad Sci USA 110(7):2452-2459.
6. Zhou S, Sokolov A, Lavrentovich OD, Aranson IS (2014) Living liquid crystals. Proc Natl Acad Sci USA 111(4):1265-1270.
7. Costerton JW, Lewandowski Z, Caldwell DE, Korber DR, Lappin-Scott HM (1995) Microbial biofilms. Annu Rev Microbiol 49:711-745.
8. O'Toole G, Kaplan HB, Kolter R (2000) Biofilm formation as microbial development. Annu Rev Microbiol 54:49-79.
9. Asally M, et al. (2012) Localized cell death focuses mechanical forces during 3D patterning in a biofilm. Proc Natl Acad Sci USA 109(46):18891-18896.
10. Seminara A, et al. (2012) Osmotic spreading of Bacillus subtilis biofilms driven by an extracellular matrix. Proc Natl Acad Sci USA 109(4):1116-1121.
11. Gloag ES, et al. (2013) Self-organization of bacterial biofilms is facilitated by extracellular DNA. Proc Natl Acad Sci USA 110(28):11541-11546.
12. Ghosh P, Ben-Jacob E, Levine H (2013) Modeling cell-death patterning during biofilm formation. Phys Biol 10(6):066006.
13. Pratt LA, Kolter R (1998) Genetic analysis of Escherichia coli biofilm formation: Roles of flagella, motility, chemotaxis and type I pili. Mol Microbiol 30(2):285-293.
14. Cates ME, Marenduzzo D, Pagonabarraga I, Tailleur J (2010) Arrested phase separation in reproducing bacteria creates a generic route to pattern formation. Proc Natl Acad Sci USA 107(26):11715-11720.
15. Davies DG, et al. (1998) The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science 280(5361):295-298.
16. Liu C, et al. (2011) Sequential establishment of stripe patterns in an expanding cell population. Science 334(6053):238-241.
17. McBride MJ (2001) Bacterial gliding motility: Multiple mechanisms for cell movement over surfaces. Annu Rev Microbiol 55:49-75.
18. Ben-Jacob E, Cohen I, Levine H (2000) Cooperative self-organization of microorganisms. Adv Phys 49(4):395-554.
19. Lushi E, Wioland H, Goldstein RE (2014) Fluid flows created by swimming bacteria drive self-organization in confined suspensions. Proc Natl Acad Sci USA 111(27):9733-9738.
20. Waters CM, Bassler BL (2005) Quorum sensing: Cell-to-cell communication in bacteria. Annu Rev Cell Dev Biol 21:319-346.
21. Cho H, et al. (2007) Self-organization in high-density bacterial colonies: Efficient crowd control. PLoS Biol 5(11):e302.
22. Boyer D, et al. (2011) Buckling instability in ordered bacterial colonies. Phys Biol 8(2):026008.
23. Wensink HH, et al. (2012) Meso-scale turbulence in living fluids. Proc Natl Acad Sci USA 109(36):14308-14313.
24. Volfson D, Cookson S, Hasty J, Tsimring LS (2008) Biomechanical ordering of dense cell populations. Proc Natl Acad Sci USA 105(40):15346-15351.
25. Farrell FDC, Hallatschek O, Marenduzzo D, Waclaw B (2013) Mechanically driven growth of quasi-two-dimensional microbial colonies. Phys Rev Lett 111(16):168101.
26. Grant MAA, Wacław B, Allen RJ, Cicuta P (2014) The role of mechanical forces in the planar-to-bulk transition in growing Escherichia coli microcolonies. J R Soc Interface 11(97):20140400.
27. Harris RH, Mitchell R (1973) The role of polymers in microbial aggregation. Annu Rev Microbiol 27:27-50.
28. Asakura S, Oosawa F (1958) Interaction between particles suspended in solutions of macromolecules. J Polym Sci Polym Phys Ed 33(126):183-192.
29. Yodh AG, et al. (2001) Entropically driven self-assembly and interaction in suspension. Phil Trans R Soc A 359(1782):921-937.
30. Neu B, Meiselman HJ (2002) Depletion-mediated red blood cell aggregation in polymer solutions. Biophys J 83(5):2482-2490.
31. Steffen P, Verdier C, Wagner C (2013) Quantification of depletion-induced adhesion of red blood cells. Phys Rev Lett 110(1):018102.
32. Richter K, Nessling M, Lichter P (2007) Experimental evidence for the influence of molecular crowding on nuclear architecture. J Cell Sci 120(Pt 9):1673-1680.
33. Hancock R (2004) A role for macromolecular crowding effects in the assembly and function of compartments in the nucleus. J Struct Biol 146(3):281-290.
34. Zhou HX, Rivas G, Minton AP (2008) Macromolecular crowding and confinement: Biochemical, biophysical, and potential physiological consequences. Annu Rev Biophys 37:375-397.
35. Tuinier R, Dhont JKG, De Kruif CG (2000) Depletion-induced phase separation of aggregated whey protein colloids by an exocellular polysaccharide. Langmuir 16(4):1497-1507.
36. Schwarz-Linek J, et al. (2010) Polymer-induced phase separation in suspensions of bacteria. Europhys Lett 89(6):68003.
37. Schwarz-Linek J, et al. (2010) Polymer-induced phase separation in escherichia coli suspensions. Soft Matter 6:4540-4549.
38. Dorken G, Ferguson GP, French CE, Poon WCK (2012) Aggregation by depletion attraction in cultures of bacteria producing exopolysaccharide. J R Soc Interface 9(77):3490-3502.
39. Schwarz-Linek J, et al. (2012) Phase separation and rotor self-assembly in active particle suspensions. Proc Natl Acad Sci USA 109(11):4052-4057.
40. Dilanji GE, Teplitski M, Hagen SJ (2014) Entropy-driven motility of sinorhizobium meliloti on a semi-solid surface. Proc R Soc B Biol Sci 281(1784):20132575.
41. Rein ten Wolde P, RuizMontero MJ, Frenkel D (1996) Numerical calculation of the rate of crystal nucleation in a lennardjones system at moderate undercooling. J Chem Phys 104(24):9932-9947.
42. Steinhardt PJ, Nelson DR, Ronchetti M (1983) Bond-orientational order in liquids and glasses. Phys Rev B 28(2):784-805.