Abstract
Collective motion can be observed in biological systems over a wide range of length scales, from large animals to bacteria. Collective motion is thought to confer an advantage for defense and adaptation. A central question in the study of biological collective motion is how the traits of individuals give rise to the emergent behavior at population level. This question is relevant to the dynamics of general self-propelled particle systems, biological self-organization, and active fluids. Bacteria provide a tractable system to address this question, because bacteria are simple and their behavior is relatively easy to control. In this mini review we will focus on a special form of bacterial collective motion, i.e., bacterial swarming in two dimensions. We will introduce some organization principles known in bacterial swarming and discuss potential means of controlling its dynamics. The simplicity and controllability of 2D bacterial behavior during swarming would allow experimental examination of theory predictions on general collective motion.
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Vicsek, T. and Zafeiris, A. (2012) Collective motion. Phys. Rep., 517, 71–140
Ioannou, C. C., Guttal, V. and Couzin, I. D. (2012) Predatory fish select for coordinated collective motion in virtual prey. Science, 337, 1212–1215
Cavagna, A., Cimarelli, A., Giardina, I., Parisi, G., Santagati, R., Stefanini, F. and Viale, M. (2010) Scale-free correlations in starling flocks. Proc. Natl. Acad. Sci. USA, 107, 11865–11870
Attanasi, A., Cavagna, A., Del Castello, L., Giardina, I., Jelic, A., Melillo, S., Parisi, L., Pohl, O., Shen, E. and Viale, M. (2015) Emergence of collective changes in travel direction of starling flocks from individual birds’ fluctuations. J. R. Soc. Interface, 12, 20150319
Bazazi, S., Buhl, J., Hale, J. J., Anstey, M. L., Sword, G. A., Simpson, S. J. and Couzin, I. D. (2008) Collective motion and cannibalism in locust migratory bands. Curr. Biol., 18, 735–739
Friedl, P. and Gilmour, D. (2009) Collective cell migration in morphogenesis, regeneration and cancer. Nat. Rev. Mol. Cell Biol., 10, 445–457
Hallegraeff, G. M. (1993) A review of harmful algal blooms and their apparent global increase. Phycologia, 32, 79–99.
Tyson, J. J. and Murray, J. D. (1989) Cyclic AMP waves during aggregation of Dictyostelium amoebae. Development, 106, 421–426
Kaiser, D. (2007) Bacterial swarming: a re-examination of cellmovement patterns. Curr. Biol., 17, R561–R570
Verstraeten, N., Braeken, K., Debkumari, B., Fauvart, M., Fransaer, J., Vermant, J. and Michiels, J. (2008) Living on a surface: swarming and biofilm formation. Trends Microbiol., 16, 496–506
Vásárhelyi, G., Virágh, C., Somorjai, G., Tarcai, N., Szörényi, T., et al. (2014) Outdoor flocking and formation flight with autonomous aerial robots. arXiv:14023588
Gross, R., Bonani, M., Mondada, F. and Dorigo, M. (2006) Autonomous self-assembly in swarm-bots. Robotics. IEEE Transactions on, 22, 1115–1130
Rubenstein, M., Cornejo, A. and Nagpal, R. (2014) Programmable selfassembly in a thousand-robot swarm. Science, 345, 795–799
Martens, D., Baesens, B. and Fawcett, T. (2011) Editorial survey: swarm intelligence for data mining. Mach. Learn., 82, 1–42
Ramaswamy, S. (2010) The mechanics and statistics of active matter. Annu. Rev. Condens. Matter Phys., 1, 323–345
Koch, D. L. and Subramanian, G. (2011) Collective hydrodynamics of swimming microorganisms: living fluids. Annu. Rev. Fluid Mech., 43, 637–659
Wu, Y., Jiang, Y., Kaiser, A. D. and Alber, M. (2011) Self-organization in bacterial swarming: lessons from myxobacteria. Phys. Biol., 8, 055003
Marchetti, M. C., Joanny, J. F., Ramaswamy, S., Liverpool, T. B., Prost, J., Rao, M. and Simha, R. A. (2013) Hydrodynamics of soft active matter. Rev. Mod. Phys., 85, 1143–1189
Berg, H. C. (2004) E. coli in Motion. New York: Springer-Verlag
Saragosti, J., Calvez, V., Bournaveas, N., Perthame, B., Buguin, A. and Silberzan, P. (2011) Directional persistence of chemotactic bacteria in a traveling concentration wave. Proc. Natl. Acad. Sci. USA, 108, 16235–16240
Mazzag, B. C., Zhulin, I. B. and Mogilner, A. (2003) Model of bacterial band formation in aerotaxis. Biophys. J., 85, 3558–3574
Wu, X.-L. and Libchaber, A. (2000) Particle diffusion in a quasi-twodimensional bacterial bath. Phys. Rev. Lett., 84, 3017–3020
Sokolov, A., Aranson, I. S., Kessler, J. O. and Goldstein, R. E. (2007) Concentration dependence of the collective dynamics of swimming bacteria. Phys. Rev. Lett., 98, 158102
Sokolov, A. and Aranson, I. S. (2012) Physical properties of collective motion in suspensions of bacteria. Phys. Rev. Lett., 109, 248109
Dombrowski, C., Cisneros, L., Chatkaew, S., Goldstein, R. E. and Kessler, J. O. (2004) Self-concentration and large-scale coherence in bacterial dynamics. Phys. Rev. Lett., 93, 098103
Cisneros, L. H., Kessler, J. O., Ganguly, S. and Goldstein, R. E. (2011) Dynamics of swimming bacteria: transition to directional order at high concentration. Phys. Rev. E Stat. Nonlin. Soft Matter Phys., 83, 061907
Lushi, E., Wioland, H. and Goldstein, R. E. (2014) Fluid flows created by swimming bacteria drive self-organization in confined suspensions. Proc. Natl. Acad. Sci. USA, 111, 9733–9738
Wensink, H. H., Dunkel, J., Heidenreich, S., Drescher, K., Goldstein, R. E., Löwen, H. and Yeomans, J. M. (2012) Meso-scale turbulence in living fluids. Proc. Natl. Acad. Sci. USA, 109, 14308–14313
Petroff, A. P., Wu, X.- L. and Libchaber, A. (2015) Fast-moving bacteria self-organize into active two-dimensional crystals of rotating cells. Phys. Rev. Lett., 114, 158102
Xiao, C., Xiang, Y., Mingcheng, Y. and Zhang, H. P. (2015) Dynamic clustering in suspension of motile bacteria. EPL, 111, 54002
López, D., Vlamakis, H. and Kolter, R. (2010) Biofilms. Cold Spring Harb. Perspect. Biol., 2, a000398
Kerr, B., Riley, M. A., Feldman, M. W. and Bohannan, B. J. M. (2002) Local dispersal promotes biodiversity in a real-life game of rock-paperscissors. Nature, 418, 171–174
Struthers, J. K. and Westran, R. P. (2003) Clinical Bacteriology. 192. Florida: CRC Press
Hauser, G. (1885) Über Fäulnisbakterien und deren Beziehung zur Septicämie. Leipzig: F.G. W. Vogel
Harshey, R. M. (2003) Bacterial motility on a surface: many ways to a common goal. Annu. Rev. Microbiol., 57, 249–273
Kearns, D. B. (2010) A field guide to bacterial swarming motility. Nat. Rev. Microbiol., 8, 634–644
Berg, H. C. (2003) The rotary motor of bacterial flagella. Annu. Rev. Biochem., 72, 19–54
Lauga, E. and Powers, T. R. (2009) The hydrodynamics of swimming microorganisms. Rep. Prog. Phys., 72, 096601
Allison, C., Lai, H.-C., Gygi, D. and Hughes, C. (1993) Cell differentiation of Proteus mirabilis is initiated by glutamine, a specific chemoattractant for swarming cells. Mol. Microbiol., 8, 53–60
Harshey, R. M. and Matsuyama, T. (1994) Dimorphic transition in Escherichia coli and Salmonella typhimurium: surface-induced differentiation into hyperflagellate swarmer cells. Proc. Natl. Acad. Sci. USA, 91, 8631–8635
Partridge, J. D. and Harshey, R. M. (2013) More than motility: Salmonella flagella contribute to overriding friction and facilitating colony hydration during swarming. J. Bacteriol., 195, 919–929
Hamze, K., Autret, S., Hinc, K., Laalami, S., Julkowska, D., Briandet, R., Renault, M., Absalon, C., Holland, I. B., Putzer, H., et al. (2011) Single-cell analysis in situ in a Bacillus subtilis swarming community identifies distinct spatially separated subpopulations differentially expressing hag (flagellin), including specialized swarmers. Microbiology, 157, 2456–2469
Tremblay, J. and Déziel, E. (2010) Gene expression in Pseudomonas aeruginosa swarming motility. BMC Genomics, 11, 587
Henrichsen, J. (1972) Bacterial surface translocation: a survey and a classification. Bacteriol Rev, 36, 478–503
Allison, C. and Hughes, C. (1991) Bacterial swarming: an example of prokaryotic differentiation and multicellular behaviour. Sci. Prog., 75, 403–422
McCarter, L. L. (2004) Dual flagellar systems enable motility under different circumstances. J. Mol. Microbiol. Biotechnol., 7, 18–29
Copeland, M. F. and Weibel, D. B. (2009) Bacterial swarming: a model system for studying dynamic self-assembly. Soft Matter, 5, 1174–1187
Zhang, H. P., Be'er, A., Smith, R. S., Florin, E.-L. and Swinney, H. L. (2009) Swarming dynamics in bacterial colonies. EPL, 87, 48011.
Darnton, N. C., Turner, L., Rojevsky, S. and Berg, H. C. (2010) Dynamics of bacterial swarming. Biophys. J., 98, 2082–2090
Zhang, H. P., Be’er, A., Florin, E.-L. and Swinney, H. L. (2010) Collective motion and density fluctuations in bacterial colonies. Proc. Natl. Acad. Sci. USA, 107, 13626–13630
Wu, Y., Hosu, B. G. and Berg, H. C. (2011) Microbubbles reveal chiral fluid flows in bacterial swarms. Proc. Natl. Acad. Sci. USA, 108, 4147–4151
Turner, L., Zhang, R., Darnton, N. C. and Berg, H. C. (2010) Visualization of flagella during bacterial swarming. J. Bacteriol., 192, 3259–3267
Berg, H. C. and Brown, D. A. (1972) Chemotaxis in Escherichia coli analysed by three-dimensional tracking. Nature, 239, 500–504
Cisneros, L., Dombrowski, C., Goldstein, R. E., Kessler, J. O. (2006) Reversal of bacterial locomotion at an obstacle. Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 73:03090173: 030901
Be’er, A., Strain, S. K., Hernández, R. A., Ben-Jacob, E. and Florin, E.-L. (2013) Periodic reversals in Paenibacillus dendritiformis swarming. J. Bacteriol., 195, 2709–2717
Mariconda, S., Wang, Q. and Harshey, R. M. (2006) A mechanical role for the chemotaxis system in swarming motility. Mol. Microbiol., 60, 1590–1602
Chen, X., Dong, X., Be’er, A., Swinney, H. L. and Zhang, H. P. (2012) Scale-invariant correlations in dynamic bacterial clusters. Phys. Rev. Lett., 108, 148101
Ariel, G., Rabani, A., Benisty, S., Partridge, J. D., Harshey, R. M. and Be’er, A. (2015) Swarming bacteria migrate by Lévy Walk. Nat. Commun., 6, 8396
Peruani, F., Deutsch, A. and Bär, M. (2006) Nonequilibrium clustering of self-propelled rods. Phys. Rev. E Stat. Nonlin. Soft Matter Phys., 74, 030904
Swiecicki, J.-M., Sliusarenko, O. and Weibel, D. B. (2013) From swimming to swarming: Escherichia coli cell motility in twodimensions. Integr. Biol. (Camb), 5, 1490–1494
Drescher, K., Dunkel, J., Cisneros, L. H., Ganguly, S. and Goldstein, R. E. (2011) Fluid dynamics and noise in bacterial cell-cell and cellsurface scattering. Proc. Natl. Acad. Sci. USA, 108, 10940–10945
Zhang, R., Turner, L. and Berg, H. C. (2010) The upper surface of an Escherichia coli swarm is stationary. Proc. Natl. Acad. Sci. USA, 107, 288–290
Wu, Y. and Berg, H. C. (2012) Water reservoir maintained by cell growth fuels the spreading of a bacterial swarm. Proc. Natl. Acad. Sci. USA, 109, 4128–4133
Ping, L., Wu, Y., Hosu, B. G., Tang, J. X. and Berg, H. C. (2014) Osmotic pressure in a bacterial swarm. Biophys. J., 107, 871–878
Semmler, A. B. T., Whitchurch, C. B. and Mattick, J. S. (1999) A reexamination of twitching motility in Pseudomonas aeruginosa. Microbiology, 145, 2863–2873
Nudleman, E. and Kaiser, D. (2004) Pulling together with type IV pili. J. Mol. Microbiol. Biotechnol., 7, 52–62
Anyan, M. E., Amiri, A., Harvey, C. W., Tierra, G., Morales-Soto, N., Driscoll, C. M., Alber, M. S. and Shrout, J. D. (2014) Type IV pili interactions promote intercellular association and moderate swarming of Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. USA, 111, 18013–18018
Hoiczyk, E. and Baumeister, W. (1998) The junctional pore complex, a prokaryotic secretion organelle, is the molecular motor underlying gliding motility in cyanobacteria. Curr. Biol., 8, 1161–1168
McBride, M. J. (2004) Cytophaga-flavobacterium gliding motility. J. Mol. Microbiol. Biotechnol., 7, 63–71
Kaiser, D. (2003) Coupling cell movement to multicellular development in myxobacteria. Nat. Rev. Microbiol., 1, 45–54
Nan, B., McBride, M. J., Chen, J., Zusman, D. R. and Oster, G. (2014) Bacteria that glide with helical tracks. Curr. Biol., 24, R169–R173
Nelson, S. S., Bollampalli, S. and McBride, M. J. (2008) SprB is a cell surface component of the Flavobacterium johnsoniae gliding motility machinery. J. Bacteriol., 190, 2851–2857
Nakane, D., Sato, K., Wada, H., McBride, M. J. and Nakayama, K. (2013) Helical flow of surface protein required for bacterial gliding motility. Proc. Natl. Acad. Sci. USA, 110, 11145–11150
Shrivastava, A., Lele, P. P. and Berg, H. C. (2015) A rotary motor drives Flavobacterium gliding. Curr. Biol., 25, 338–341
Kaiser, D. and Warrick, H. (2014) Transmission of a signal that synchronizes cell movements in swarms of Myxococcus xanthus. Proc. Natl. Acad. Sci. USA, 111, 13105–13110
Jelsbak, L. and Kaiser, D. (2005) Regulating pilin expression reveals a threshold for S motility in Myxococcus xanthus. J. Bacteriol., 187, 2105–2112
Wu, Y., Kaiser, A. D., Jiang, Y. and Alber, M. S. (2009) Periodic reversal of direction allows Myxobacteria to swarm. Proc. Natl. Acad. Sci. USA, 106, 1222–1227
Kudrolli, A. (2010) Concentration dependent diffusion of self-propelled rods. Phys. Rev. Lett., 104, 088001
Igoshin, O. A., Goldbeter, A., Kaiser, D. and Oster, G. (2004) A biochemical oscillator explains several aspects of Myxococcus xanthus behavior during development. Proc. Natl. Acad. Sci. USA, 101, 15760–15765
Berleman, J. E., Scott, J., Chumley, T. and Kirby, J. R. (2008) Predataxis behavior in Myxococcus xanthus. Proc. Natl. Acad. Sci. USA, 105, 17127–17132
Alber, M. S., Kiskowski, M. A. and Jiang, Y. (2004) Two-stage aggregate formation via streams in myxobacteria. Phys. Rev. Lett., 93, 068102
Thutupalli, S., Sun, M., Bunyak, F., Palaniappan, K. and Shaevitz, J.W. (2015) Directional reversals enable Myxococcus xanthus cells to produce collective one-dimensional streams during fruiting-body formation. J. R. Soc. Interface, 12, 20150049
Sozinova, O., Jiang, Y., Kaiser, D. and Alber, M. (2005) A threedimensional model of myxobacterial aggregation by contact-mediated interactions. Proc. Natl. Acad. Sci. USA, 102, 11308–11312
Wu, Y., Jiang, Y., Kaiser, D. and Alber, M. (2007) Social interactions in myxobacterial swarming. PLoS Comput. Biol., 3, e253
Janulevicius, A., van Loosdrecht, M. C. M., Simone, A. and Picioreanu, C. (2010) Cell flexibility affects the alignment of model myxobacteria. Biophys. J., 99, 3129–3138
Peruani, F., Starruß, J., Jakovljevic, V., Søgaard-Andersen, L., Deutsch, A. and Bär, M. (2012) Collective motion and nonequilibrium cluster formation in colonies of gliding bacteria. Phys. Rev. Lett., 108, 098102
Janulevicius, A., van Loosdrecht, M. and Picioreanu, C. (2015) Shortrange guiding can result in the formation of circular aggregates in myxobacteria populations. PLoS Comput. Biol., 11, e1004213
Balagam, R. and Igoshin, O. A. (2015) Mechanism for collective cell alignment in Myxococcus xanthus bacteria. PLoS Comput. Biol., 11, e1004474
Chaté, H., Ginelli, F. and Montagne, R. (2006) Simple model for active nematics: quasi-long-range order and giant fluctuations. Phys. Rev. Lett., 96, 180602
McCandlish, S. R., Baskaran, A. and Hagan, M. F. (2012) Spontaneous segregation of self-propelled particles with different motilities. Soft Matter, 8, 2527–2534.
Hinz, D. F., Panchenko, A., Kim, T.-Y. and Fried, E. (2014) Motility versus fluctuations in mixtures of self-motile and passive agents. Soft Matter, 10, 9082–9089
Nagai, K. H., Sumino, Y., Montagne, R., Aranson, I. S. and Chaté, H. (2015) Collective motion of self-propelled particles with memory. Phys. Rev. Lett., 114, 168001
Liu, C., Fu, X., Liu, L., Ren, X., Chau, C. K. L., Li, S., Xiang, L., Zeng, H., Chen, G., Tang, L. H., et al. (2011) Sequential establishment of stripe patterns in an expanding cell population. Science, 334, 238–241
Deisseroth, K. (2011) Optogenetics. Nat. Methods, 8, 26–29
Lu, S., Bi,W., Liu, F., Wu, X., Xing, B. and Yeow, E. K. (2013) Loss of collective motion in swarming bacteria undergoing stress. Phys. Rev. Lett., 111, 208101
Liu, J., Prindle, A., Humphries, J., Gabalda-Sagarra, M., Asally, M., Lee, D. Y., Ly, S., Garcia-Ojalvo, J. and Süel, G. M. (2015) Metabolic co-dependence gives rise to collective oscillations within biofilms. Nature, 523, 550–554
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Wu, Y. Collective motion of bacteria in two dimensions. Quant Biol 3, 199–205 (2015). https://doi.org/10.1007/s40484-015-0057-7
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DOI: https://doi.org/10.1007/s40484-015-0057-7