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A field guide to bacterial swarming motility

Nature Reviews Microbiology volume 8, pages 634–644 (2010)Cite this article

Subjects

Key Points

  • Swarming motility is operationally defined as multicellular, flagella-mediated surface migration of bacteria. Swarming requires intercellular interactions, surfactant secretion and an increase in flagellar numbers.

  • Swarming motility has often been genetically bred out of laboratory strains and is best observed in natural isolates. In the laboratory, one must take care to standardize swarming conditions. Although the specific conditions that promote swarming are species dependent, swarming generally occurs on nutrient-rich media solidified by agar concentrations of greater than 0.3%.

  • A period of non-motility, or a swarm lag, will manifest when cells are transferred from liquid to a solid medium. The lag is thought to indicate a physiological change in cells to become swarming proficient.

  • Some bacteria become elongated during swarming. It is not clear whether cell elongation is required for or simply co-regulated with swarming in these species. The mechanistic connection between swarming motility and cell elongation is unknown, and many swarming bacteria do not become elongated.

  • Swarming often requires the chemotaxis sensory transduction system for functions that are unrelated to chemotaxis, or directed movement, per se.

  • The mechanism of surface sensing (the bacterial 'sense of touch') is unknown, but swarming motility provides a strong model system for its study. Models have been proposed to explain the bacterial response to surface contact, including sensing resistance to flagellar rotation when impeded by surface contact and sensing perturbations in the Gram-negative outer membrane.

  • The ecology of swarming is unknown, but swarming is often associated with pathogenesis. Swarming bacteria also enjoy enhanced resistance to antibiotics and eukaryotic engulfment as well as gaining enhanced nutrition and a competitive advantage from secreted surfactants.

Abstract

How bacteria regulate, assemble and rotate flagella to swim in liquid media is reasonably well understood. Much less is known about how some bacteria use flagella to move over the tops of solid surfaces in a form of movement called swarming. The focus of bacteriology is changing from planktonic to surface environments, and so interest in swarming motility is on the rise. Here, I review the requirements that define swarming motility in diverse bacterial model systems, including an increase in the number of flagella per cell, the secretion of a surfactant to reduce surface tension and allow spreading, and movement in multicellular groups rather than as individuals.

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Figure 1: Bacteria move by a range of mechanisms.
Figure 2: Phylogenetic distribution of swarming motility.
Figure 3: Rafting.
Figure 4: Surfactants.
Figure 5: Swarming lag.
Figure 6: Cell filaments and cell chains.
Figure 7: Colony pattern formation.

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References

  1. Verstraeten, N. et al. Living on a surface: swarming and biofilm formation. Trends Microbiol. 16, 496–506 (2008).

    Article  CAS  PubMed  Google Scholar 

  2. Henrichsen, J. Bacterial surface translocation: a survey and a classification. Bacteriol. Rev. 36, 478–503 (1972). This landmark study characterizes the motile behaviour of over 500 bacterial isolates and defines the main types of bacterial movement: swimming, swarming, twitching, gliding and sliding.

    CAS  PubMed  PubMed Central  Google Scholar 

  3. Jarrell, K. F. & McBride, M. J. The surprisingly diverse ways that prokaryotes move. Nature Rev. Microbiol. 6, 466–476 (2008).

    Article  CAS  Google Scholar 

  4. Mattick, J. S. Type IV pili and twitching motility. Annu. Rev. Biochem. 56, 289–314 (2002).

    CAS  Google Scholar 

  5. Mignot, T. The elusive engine in Myxococcus xanthus gliding motility. Cell. Mol. Life Sci. 64, 2733–2745 (2007).

    Article  CAS  PubMed  Google Scholar 

  6. Matsuyama, T. et al. A novel extracellular cyclic lipopeptide which promotes flagellum-dependent and -independent spreading growth of Serratia marcescens. J. Bacteriol. 174, 1769–1776 (1992).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Kinsinger, R. F., Kearns, D. B., Hale, M. & Fall, R. Genetic requirements for potassium ion-dependent colony spreading in Bacillus subtilis. J. Bacteriol. 187, 8462–8469 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Murray, T. S. & Kazmierczak, B. I. Pseudomonas aeruginosa exhibits sliding motiliy in the absence of type IV pili and flagella. J. Bacteriol. 190, 2700–2708 (2008).

    Article  CAS  PubMed  Google Scholar 

  9. Matsuyama, T., Bhasin, A. & Harshey, R. M. Mutational analysis of flagellum-independent surface spreading of Serratia marcescens 274 on a low-agar medium. J. Bacteriol. 177, 987–991 (1995).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Be'er, A. et al. Paenibacillus dendritiformis bacterial colony growth depends on surfactant but not on bacterial motion. J. Bacteriol. 191, 5758–5764 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Kearns, D. B. & Losick, R. Swarming motility in undomesticated Bacillus subtilis. Mol. Microbiol. 49, 581–590 (2003). A comprehensive phenotypic and genetic analysis of swarming motility.

    Article  CAS  PubMed  Google Scholar 

  12. Patrick, J. E. & Kearns, D. B. Laboratory strains of Bacillus subtilis do not exhibit swarming motility. J. Bacteriol. 191, 7129–7133 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Ghelardi, E. et al. Swarming behavior of and hemolysin BL secretion by Bacillus cereus. Appl. Env. Microbiol. 73, 4089–4093 (2007).

    Article  CAS  Google Scholar 

  14. Kim, W. & Surette, M. G. Prevalence of surface swarming behavior in Salmonella. J. Bacteriol. 187, 6580–6583 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Velicer, G. J., Kroos, L. & Lenski, R. E. Loss of social behaviors by Myxococcus xanthus during evolution in an unstructured habitat. Proc. Natl Acad. Sci. USA 95, 12376–12380 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Julkowska, D., Obuchowski, M., Holland, B. I. & Séror, S. J. Comparative analysis of the development of swarming communities of Bacillus subtilis 168 and a natural wild type: critical effects of surfactin and the composition of the medium. J. Bacteriol. 187, 65–76 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Young, G. M., Smith, M. J., Minnich, S. A. & Miller, V. L. The Yersinia enterocolitica motility master regulatory operon, flhDC, is required for flagellin production, swimming motility, and swarming motility. J. Bacteriol. 181, 2823–2833 (1999). Another comprehensive phenotypic and genetic analysis of swarming motility.

    CAS  PubMed  PubMed Central  Google Scholar 

  18. Harshey, R. M. & Matsuyama, T. Dimorphic transition in Escherichia coli and Salmonella typhimurium: surface-induced differentiation into hyperflagellate swarmer cells. Proc. Natl Acad. Sci. USA 91, 8631–8635 (1994).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Jones, H. E. & Park, R. W. A. The influence of medium composition on the growth and swarming of Proteus. J. Gen. Microbiol. 47, 369–378 (1967).

    Article  CAS  PubMed  Google Scholar 

  20. Eberl, L., Molin, S. & Givskov, M. Surface motility of Serratia liquefaciens MG1. J. Bacteriol. 181, 1703–1712 (1999). An excellent data-filled review specific to S. liquefaciens swarming that serves as a template that is generally applicable to many systems.

    CAS  PubMed  PubMed Central  Google Scholar 

  21. Tremblay, J. & Déziel, E. Improving the reproducibility of Pseudomonas aeruginosa swarming motility assays. J. Basic Microbiol. 48, 509–515 (2008).

    Article  CAS  PubMed  Google Scholar 

  22. Mayfield, C. I. & Inniss, W. E. A rapid, simple method for staining bacterial flagella. Can. J. Microbiol. 23, 1311–1313 (1977).

    Article  CAS  PubMed  Google Scholar 

  23. Turner, L., Ryu, W. S. & Berg, H. C. Real-time imaging of fluorescent flagellar filaments. J. Bacteriol. 182, 2793–2801 (2000). The authors devise a simple, rapid and robust means of fluorescently labelling the flagella of Gram-negative bacteria. This work is a great leap forward for the imaging of flagellar dynamics.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Copeland, M. F., Flickinger, S. T., Tuson, H. H. & Weibel, D. B. Studying the dynamics of flagella in multicellular communities of Escherichia coli by using biarsenical dyes. Appl. Environ. Microbiol. 76, 1241–1250 (2010). An important first effort towards monitoring flagellar dynamics in a swarm.

    Article  CAS  PubMed  Google Scholar 

  25. Hoeniger, J. F. M. Development of flagella by Proteus mirabilis. J. Gen. Microbiol. 40, 29–42 (1965).

    Article  Google Scholar 

  26. Jones, B. V., Young, R., Mahenthiralingam, E. & Stickler, D. J. Ultrastructure of Proteus mirabilis swarmer cell rafts and role of swarming in catheter-associated urinary tract infection. Infect. Immun. 72, 3941–3950 (2004). An article containing beautiful electron micrographs of P. mirabilis swarms on the surface of a catheter.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Chevance, F. F. V. & Hughes, K. T. Coordinating assembly of a bacterial macromolecular machine. Nature Rev. Microbiol. 6, 455–465 (2008).

    Article  CAS  Google Scholar 

  28. Shinoda, S. & Okamoto, K. Formation and function of Vibrio parahaemolyticus lateral flagella. J. Bacteriol. 129, 1266–1271 (1977). The first observation that synthesis of lateral flagella is induced in V. parahaemolyticus by contact with a surface.

    CAS  PubMed  PubMed Central  Google Scholar 

  29. Alberti, L. & Harshey, R. M. Differentiation of Serratia marcescens 274 into swimmer and swarmer cells. J. Bacteriol. 172, 4322–4328 (1990).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Merino, S., Shaw, J. G. & Tomás, J. M. Bacterial lateral flagella: an inducible flagella system. FEMS Microbiol. Lett. 263, 127–135 (2006).

    Article  CAS  PubMed  Google Scholar 

  31. Ulitzur, S. & Kessel, M. Giant flagellar bundles of Vibrio alginolyticus (NCMB 1803). Arch. Mikrobiol. 94, 331–339 (1973).

    Article  CAS  PubMed  Google Scholar 

  32. Schneider, W. R. & Doetsch, R. N. Effect of viscosity on bacterial motility. J. Bacteriol. 117, 696–701 (1974).

    CAS  PubMed  PubMed Central  Google Scholar 

  33. Berg, H. C. & Turner, L. Movement of microorganisms in viscous environments. Nature 278, 349–351 (1979).

    Article  CAS  PubMed  Google Scholar 

  34. Atsumi, T. et al. Effect of viscosity on swimming by the lateral and polar flagella of Vibrio alginolyticus. J. Bacteriol. 178, 5024–5026 (1996).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Zhang, R., Turner, L. & Berg, H. C. The upper surfaces of an Escherichia coli swarm is stationary. Proc. Natl Acad. Sci. USA 107, 288–290 (2010). A simple and fascinating approach to measuring the thickness of the fluid surrounding a swarm, including the unexpected finding that the top surface of the swarm fluid is relatively static.

    Article  CAS  PubMed  Google Scholar 

  36. Darnton, N. C., Turner, L., Rojevsky, S. & Berg, H. C. Dyanmics of bacterial swarming. Biophys. J. 98, 2082–2090 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Turner, L., Zhang, R., Darnton, N. C. & Berg, H. C. Visualization of flagella during bacterial swarming. J. Bacteriol. 192, 3259–3267 (2010). An important first effort towards monitoring flagellar dynamics in a swarm.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Ragatz, L., Jiang, Z. Y., Bauer, C. & Gest, H. Macroscopic phototactic behavior of the purple photosynthetic bacterium Rhodospirillum centenum. Arch. Microbiol. 163, 1–6 (1995).

    Article  CAS  PubMed  Google Scholar 

  39. Gavín, R. et al. Lateral flagella of Aeromonas species are essential for epithelial cell adherence and biofilm formation. Mol. Microbiol. 43, 383–397 (2002).

    Article  PubMed  Google Scholar 

  40. Kirov, S. M. et al. Lateral flagella and swarming motility in Aeromonas species. J. Bacteriol. 184, 547–555 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. McCarter, L. L. & Wright, M. E. Identification of genes encoding components of the swarmer cell flagellar motor and propeller and a sigma factor controlling differentiation of Vibrio parahaemolyticus. J. Bacteriol. 175, 3361–3371 (1993).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Kim, Y. K. & McCarter, L. L. Analysis of the polar flagellar gene system of V. parahaemolyticus. J. Bacteriol. 182, 3693–3704 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Doyle, T. B., Hawkins, A. C. & McCarter, L. L. The complex flagellar torque generator of Pseudomonas aeruginosa. J. Bacteriol. 186, 6341–6350 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Toutain, C. M., Zegans, M. E., & O'Toole, G. A. Evidence for two flagellar stators and their role in the motility of Pseudomonas aeruginosa. J. Bacteriol. 187, 771–777 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Senesi, S. et al. Swarming motility in Bacillus cereus and characterization of a fliY mutant impaired in swarm cell differentiation. Microbiology 148, 1785–1794 (2002).

    Article  CAS  PubMed  Google Scholar 

  46. Lai, H. C., Gygi, D., Fraser, G. M. & Hughes, C. A swarming defective mutant of Proteus mirabilis lacking a putative cation-transporting membrane P-type ATPase. Microbiology 144, 1957–1961 (1998).

    Article  CAS  PubMed  Google Scholar 

  47. Furness, R. B., Fraser, G. M., Hay, N. A. & Hughes, C. Negative feedback from a Proteus class II flagellum export defect to the flhDC master operon controlled cell division and flagellum assembly. J. Bacteriol. 179, 5585–5588 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Köhler, T., Curty, L. K., Barja, F., Van Delden, C. & Pechère, J.C. Swarming of Pseudomonas aeruginosa is dependent on cell-to-cell signaling and requires flagella and pili. J. Bacteriol. 182, 5990–5996 (2000).

    Article  PubMed  PubMed Central  Google Scholar 

  49. Rashid, M. H. & Kornberg, A. Inorganic polyphosphate is needed for swimming, swarming, and twitching motilities of Pseudomonas aeruginosa. Proc. Natl Acad. Sci. USA 97, 4885–4890 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Hay, N. A., Tipper, D. J., Gygi, D. & Hughes, C. A nonswarming mutant of Proteus mirabilis lacks the Lrp global transcriptional regulator. J. Bacteriol. 179, 4741–4746 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Dufour, A., Furness, R. B. & Hughes, C. Novel genes that upregulate the Proteus mirabilis master operon controlling flagellar biogenesis and swarming. Mol. Microbiol. 29, 741–751 (1998).

    Article  CAS  PubMed  Google Scholar 

  52. Kearns, D. B., Chu, F., Rudner, R. & Losick, R. Genes governing swarming in Bacillus subtilis and evidence for a phase variation mechanism controlling surface motility. Mol. Microbiol. 52, 357–369 (2004).

    Article  CAS  PubMed  Google Scholar 

  53. Calvio, C. et al. Swarming differentiation and swimming motility in Bacillus subtilis are controlled by swrA, a newly identified dicistronic operon. J. Bacteriol. 187, 5356–5366 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Kearns, D. B. & Losick, R. Cell population heterogeneity during growth of Bacillus subtilis. Genes Dev. 19, 3083–3094 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Wang, Q., Suzuki, A., Mariconda, S., Powollik, S. & Harshey, R. M. Sensing wetness: a new role for the bacterial flagellum. EMBO J. 24, 2034–2042 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Morgenstein, R. M., Clemmer, K. M. & Rather, P. N. Loss of the waaL O-antigen ligase prevents surface activation of the flagellar gene cascase in Proteus mirabilis. J. Bacteriol. 192, 3213–3221 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Soo, P. C. et al. Regulation of swarming motility and flhDC Sm expression by RssAB signaling in Serratia marcescens. J. Bacteriol. 190, 2496–2504 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Belas, R., Schneider, R. & Melch, M. Characterization of Proteus mirabilis precocious swarming mutants: identification of rsbA, encoding a regulator of swarming behavior. J. Bacteriol. 180, 6126–6139 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  59. Stevenson, L. G. & Rather, P. N. A novel gene involved in regulating the flagellar gene cascade in Proteus mirabilis. J. Bacteriol. 188, 7830–7839 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Claret, L. & Hughes, C. Rapid turnover of FlhD and FlhC, the flagellar regulon transcriptional activator proteins, during Proteus swarming. J. Bacteriol. 182, 833–836 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Morrison, R. B. & Scott, A. Swarming of Proteus — a solution to an old problem. Nature 211, 255–257 (1966). The first detailed description of the rafting phenomenon. The authors raise many questions concerning swarming motility that remain unresolved to this day.

    Article  CAS  PubMed  Google Scholar 

  62. O'Rear, J., Alberti, L. & Harshey, R. M. Mutations that impair swarming motility in Serratia marcescens 274 include but are not limited to those affecting chemotaxis or flagellar function. J. Bacteriol. 174, 6125–6137 (1992).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Girgis, H. S., Liu, Y., Ryu, W. S. & Tavazoie, S. A comprehensive genetic characterization of bacterial motility. PLOS Genet. 3, 154–166 (2007). An exceptionally well-executed re-investigation of the genetic requirements for swimming and swarming motility in E. coli . New swarming genes are identified, characterized and interpreted by epistasis analysis.

    Article  CAS  Google Scholar 

  64. Julkowska, D., Obuchowski, M., Holland, B. I. & Séror, S. J. Branched swarming patterns on a synthetic medium by wild-type Bacillus subtilis strain 3610: detection of different cellular morphologies and constellations of cells as the complex architecture develops. Microbiology 150, 1839–1849 (2004).

    Article  CAS  PubMed  Google Scholar 

  65. Toguchi, A., Siano, M., Burkart, M. & Harshey, R. M. Genetics of swarming motility in Salmonella enterica serovar Typhimurium: critical role for lipopolysaccharide. J. Bacteriol. 182, 6308–6321 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Jain, D. K., Collins-Thompson, D. L., Lee, H. & Trevors, J. T. A drop-collapsing test for screening surfactant producing microorganisms. J. Microbiol. Methods 13, 271–279 (1991).

    Article  Google Scholar 

  67. Chen, B. G., Turner, L. & Berg, H. C. The wetting agent required for swarming in Salmonella enterica serovar Typhimurium is not a surfactant. J. Bacteriol. 189, 8750–8753 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Lindum, P. W. et al. N-acyl-L-homoserine lactone autoinducers control production of an extracellular lipopeptide biosurfactant required for swarming motility in Serratia liquefaciens MG1. J. Bacteriol. 180, 6384–6388 (1988). A superb analysis of the genetics, regulation and physiology of surfactants and swarming motility.

    Google Scholar 

  69. Peypoux, F., Bonmatin, J. M. & Wallach, J. Recent trends in the biochemistry of surfactin. Appl. Microbiol. Biotechnol. 51, 553–563 (1999).

    Article  CAS  PubMed  Google Scholar 

  70. Arima, K., Kakinuma, A. & Tamura, G. Surfactin, a crystalline peptidelipid surfactant produced by Bacillus subtilis: isolation, characterization, and its inhibition of fibrin clot formation. Biochem. Biophys. Res. Commun. 31, 488–494 (1968).

    Article  CAS  PubMed  Google Scholar 

  71. Cosmina, P. et al. Sequence and analysis of the genetic locus responsible for surfactin synthesis in Bacillus subtilis. Mol. Microbiol. 8, 821–831 (1993).

    Article  CAS  PubMed  Google Scholar 

  72. Caiazza, N. C., Shanks, R. M. & O'Toole, G. A. Rhamnolipids modulate swarming patterns of Pseudomonas aeruginosa. J. Bacteriol. 187, 7351–7361 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Ochsner, U. A., Fiechter, A. & Reiser, J. Isolation, characterization, and expression in Escherichia coli of the Pseudomonas aeruginosa rhlAB genes encoding a rhamnosyltransferase involved in rhamnolipid biosurfactant synthesis. J. Biol. Chem. 31, 19787–19795 (1994).

    Google Scholar 

  74. Déziel, E., Lépine, F., Milot, S. & Villemur, R. rhlA is required for the production of a novel biosurfactant promoting swarming motility in Pseudomonas aeruginosa: 3-(3-hydroxyalkanoyloxy) alkanoic acids (HAAs), the precursors of rhamnolipids. Microbiology 149, 2005–2013 (2003).

    Article  PubMed  CAS  Google Scholar 

  75. Tremblay, J., Richardson, A.-P., Lepine, F. & Déziel, E. Self-produced extracellular stimuli modulate the Pseudomonas aeruginosa swarming motility behavior. Environ. Microbiol. 9, 2622–2630 (2007).

    Article  CAS  PubMed  Google Scholar 

  76. Ochsner, U. A. & Reiser, J. Autoinducer-mediated regulation of rhamnolipid biosurfactant synthesis in Pseudomonas aeruginosa. Proc. Natl Acad. Sci. USA 92, 6424–6428 (1995).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Eberl, L. et al. Involvement of N-acyl-L-homoserine lactone autoinducers in controlling the multicellular behavior of Serratia liquefaciens. Mol. Microbiol. 20, 127–136 (1996).

    Article  CAS  PubMed  Google Scholar 

  78. Magnuson, R., Solomon, J. & Grossman, A. D. Biochemical and genetic characterization of a competence pheromone from B. subtilis. Cell 77, 207–216 (1994).

    Article  CAS  PubMed  Google Scholar 

  79. Francez-Charlot, A. et al. RcsCDB His-Asp phosphorelay system negatively regulates the flhDC operon in Escherichia coli. Mol. Microbiol. 49, 823–832 (2003).

    Article  CAS  PubMed  Google Scholar 

  80. Belas, R., Simon, M. & Silverman, M. Regulation of lateral flagella gene transcription in Vibrio parahaemolyticus. J. Bacteriol. 167, 210–218 (1986). The authors couple luciferase expression to expression of a lateral flagellar gene and determine that viscosity is an inducer of the swarming state.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Hoeniger, J. F. M. Cellular changes accompanying the swarming of Proteus mirabilis. I. Observation of living cultures. Can. J. Microbiol. 10, 1–9 (1964).

    Article  CAS  PubMed  Google Scholar 

  82. Rauprich, O. et al. Periodic phenomena in Proteus mirabilis swarm colony development. J. Bacteriol. 178, 6525–6538 (1996). A detailed analysis of the macroscopic bull's eye pattern formation during swarming motility in P. mirabilis.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Williams, F. D., Anderson, D. M., Hoffman, P. S., Schwarzhoff, R. H. & Leonard, S. Evidence against the involvement of chemotaxis in swarming Proteus mirabilis. J. Bacteriol. 127, 237–248 (1976).

    CAS  PubMed  PubMed Central  Google Scholar 

  84. Chen, R., Guttenplan, S. B., Blair, K. M. & Kearns, D. B. Role of the σD-dependent autolysins in Bacillus subtilis population heterogeneity. J. Bacteriol. 191, 5775–5784 (2009).

    Article  CAS  PubMed  Google Scholar 

  85. Zheng, Y., Wong, M. L., Alberts, B. & Mitchison, T. Nucleation of microtubule assembly by a γ-tubulin-containing ring complex. Nature 378, 578–583 (1995).

    Article  CAS  PubMed  Google Scholar 

  86. Mitchison, T. & Kirschner, M. Dynamic instability of microtubule growth. Nature 312, 237–242 (1984).

    Article  CAS  PubMed  Google Scholar 

  87. Hoeniger, J. F. M. Cellular changes accompanying the swarming of Proteus mirabilis. II. Observations of stained organisms. Can. J. Microbiol. 12, 113–123 (1965). This paper documents the filamentous, aseptate, multinucleoid cell type that is associated with P. mirabilis swarming.

    Article  Google Scholar 

  88. Tolker-Nielsen, T. et al. Assessment of flhDC mRNA levels in Serratia liquefaciens swarm cells. J. Bacteriol. 182, 2680–2686 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Belas, R. & Colwell, R. R. Scanning electron microscope observation of the swarming phenomenon of Vibrio parahaemolyticus. J. Bacteriol. 150, 956–959 (1982).

    CAS  PubMed  PubMed Central  Google Scholar 

  90. Ingham, C. J. & Ben Jacob, E. Swarming and complex pattern formation in Paenibacillus vortex studied by imaging and tracking cells. BMC Microbiol. 8, 36 (2008).

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  91. Mariconda, S., Wang, Q. & Harshey, R. M. A mechanical role for the chemotaxis system in swarming motility. Mol. Microbiol. 60, 1590–1602 (2006).

    Article  CAS  PubMed  Google Scholar 

  92. Shimada, H. et al. Dependence of local cell density on concentric ring colony formation by bacterial species Bacillus subtilis. J. Physical Soc. Japan 73, 1082–1089 (2004).

    Article  CAS  Google Scholar 

  93. Hiramatsu, F. et al. Patterns of expansion produced by a structured cell population of Serratia marscescens in response to different media. Microbes Environ. 20, 120–125 (2005).

    Article  Google Scholar 

  94. Matsuyama, T. et al. Dynamic aspects of the structured cell population in swarming colony of Proteus mirabilis. J. Bacteriol. 182, 385–393 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Bisset, K. A. & Douglas, C. W. I. A continuous study of morphological phase in the swarm of Proteus. J. Med. Microbiol. 9, 229–231 (1975).

    Article  Google Scholar 

  96. Douglas, C. W. I. & Bisset, K. A. Development of concentric zones in the Proteus swarm colony. J. Med. Microbiol. 9, 497–500 (1976).

    Article  CAS  PubMed  Google Scholar 

  97. Rudner, R., Martsinkevich, O, Leung, W. & Jarvis, E. D. Classification and genetic characterization of pattern forming Bacilli. Mol. Microbiol. 27, 687–703 (1998).

    Article  CAS  PubMed  Google Scholar 

  98. Patrick, J. E. & Kearns, D. B. MinJ (YvjD) is a topological determinant of cell division in Bacillus subtilis. Mol. Microbiol. 70, 1166–1179 (2008).

    Article  CAS  PubMed  Google Scholar 

  99. Wadhams, G. H. & Armitage, J. P. Making sense of it all: bacterial chemotaxis. Nature Rev. Mol. Cell Biol. 5, 1024–1037 (2004).

    Article  CAS  Google Scholar 

  100. Adler, J. Chemotaxis in bacteria. Science 153, 708–716 (1966).

    Article  CAS  PubMed  Google Scholar 

  101. Hughes, H. A reconsideration of the swarming of Proteus vulgaris. J. Gen. Microbiol. 17, 49–58 (1957).

    Article  CAS  PubMed  Google Scholar 

  102. Kojima, M., Kubo, R., Yakushi, T., Homma, M. & Kawagishi, I. The bidirectional polar and unidirectional lateral flagellar motors of Vibrio alginolyticus are controlled by a single CheY species. Mol. Microbiol. 64, 57–67 (2007).

    Article  CAS  PubMed  Google Scholar 

  103. Allison, C., Lai, H. C., Gygi, D. & Hughes, C. Cell differentiation of Proteus mirabilis is initiated by glutamine, a specific chemoattractant for swarming cells. Mol. Microbiol. 8, 53–60 (1993).

    Article  CAS  PubMed  Google Scholar 

  104. Sar, N., McCarter, L., Simon, M. & Silverman, M. Chemotactic control of the two flagellar systems of Vibrio parahaemolyticus. J. Bacteriol. 172, 334–341 (1990).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. Ragatz, L., Jiang, Z. Y., Bauer, C. & Gest, H. Phototactic purple bacteria. Nature 370, 104 (1994).

    Article  Google Scholar 

  106. Burkhart, M., Toguchi, A. & Harshey, R. M. The chemotaxis system, but not chemotaxis, is essential for swarming motility in Escherichia coli. Proc. Natl Acad. Sci. USA 95, 2568–2573 (1998). This important work provides genetic and physiological data that separate chemotaxis from swarming motility.

    Article  Google Scholar 

  107. Jiang, Z. Y., Gest, H. & Bauer, C. E. Chemosensory and photosensory perception in purple photosynthetic bacteria utilize common signal transduction components. J. Bacteriol. 179, 5720–5727 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  108. Berleman, J. E. & Bauer, C. E. A che-like signal transduction cascade involved in controlling flagella biosynthesis in Rhodospirillum centenum. Mol. Microbiol. 55, 1390–1402 (2005).

    Article  CAS  PubMed  Google Scholar 

  109. McCarter, L., Hilmen, M. & Silverman, M. Flagellar dynamometer controls swarmer cell differentiation of V. parahaemolyticus. Cell 54, 345–351 (1988). The flagellum is implicated as a sensor for surface contact by the demonstration that impeding flagellar rotation (using flagellum-specific antibodies or cells carrying mutations that affect the flagellar filament) induces expression of the lateral-flagella genes.

    Article  CAS  PubMed  Google Scholar 

  110. Kawagishi, I., Imagawa, M., Imae, Y., McCarter, L. & Homma, M. The sodium-driven polar flagellar motor of marine Vibrio as the mechanosensor that regulates lateral flagellar expression. Mol. Microbiol. 20, 693–699 (1996).

    Article  CAS  PubMed  Google Scholar 

  111. Jaques, S., Kim, Y. K. & McCarter, L. L. Mutations conferring resistance to phenamil and amiloride, inhibitors of sodium-driven motility of Vibrio parahaemolyticus. Proc. Natl Acad. Sci. USA 96, 5740–5745 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Belas, R. & Suvanasuthi, R. The ability of Proteus mirabilis to sense surfaces and regulated virulence gene expression involves FliL, a flagellar basal body protein. J. Bacteriol. 187, 6789–6803 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Attmannspacher, U., Scharf, B. E. & Harshey, R. M. FliL is essential for swarming: motor rotation in absence of FliL fractures the flagellar rod in swarmer cells of Salmonella enterica. Mol. Microbiol. 68, 328–341 (2008).

    Article  CAS  PubMed  Google Scholar 

  114. Darnton, N. C. & Berg, H. C. Bacterial flagella are firmly anchored. J. Bacteriol. 190, 8223–8224 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. Jones, H. E. & Park, R. W. A. The short forms and long forms of Proteus. J. Gen. Microbiol. 47, 359–367 (1967).

    Article  CAS  PubMed  Google Scholar 

  116. Falkinham, J. O. 3rd & Hoffman, P. S. Unique developmental characteristics of the swarm and short cells of Proteus vulgaris and Proteus mirabilis. J. Bacteriol. 158, 1037–1040 (1984).

    CAS  PubMed  PubMed Central  Google Scholar 

  117. Wang, Q., Frye, J. G., McClelland, M. & Harshey, R. M. Gene expression patterns during swarming in Salmonella typhimurium: genes specific to surface growth and putative new motility and pathogenicity genes. Mol. Microbiol. 52, 169–187 (2004).

    Article  CAS  PubMed  Google Scholar 

  118. Overhage, J., Bains, M., Brazas, M. D. & Hancock, R. E. W. Swarming of Pseudomonas aeruginosa is a complex adaptation leading to increased production of virulence factors and antibiotic resistance. J. Bacteriol. 190, 2671–2679 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. Kim, W. & Surette, M. G. Metabolic differentiation in actively swarming Salmonella. Mol. Microbiol. 54, 702–714 (2004).

    Article  CAS  PubMed  Google Scholar 

  120. Andersen, J. B. et al. Surface motility in Pseudomonas sp. DSS73 is required for efficient biological containment of the root-pathogenic microfungi Rhizoctonia solani and Pythium ultimum. Microbiology 149, 37–46 (2003).

    Article  CAS  PubMed  Google Scholar 

  121. Wasserman, H. H., Keggi, J. J. & McKeon, J. E. Serratamolide, a metabolic product of Serratia. J. Am. Chem. Soc. 83, 4107–4108 (1961).

    Article  CAS  Google Scholar 

  122. Carrillo, C., Teruel, J. A., Aranda, F. J. & Ortiz, A. Molecular mechanism of membrane permeabilization by the peptide antibiotic surfactin. Biochim. Biophys. Acta 1611, 91–97 (2003).

    Article  CAS  PubMed  Google Scholar 

  123. Arino, S., Marchal, R. & Vandecasteele, J. P. Involvement of a rhamnolipid-producing strain of Pseudomonas aeruginosa in the degradation of polycyclic aromatic hydrocarbons by a bacterial community. J. Appl. Microbiol. 84, 769–776 (1998).

    Article  CAS  PubMed  Google Scholar 

  124. Zhang, Y. & Miller, R. A. Enhanced octadecane dispersion and biodegradation by a Pseudomonas rhamnolipid surfactant (biosurfactant). Appl. Environ. Microbiol. 58, 3276–3282 (1992).

    CAS  PubMed  PubMed Central  Google Scholar 

  125. Zhang, Y. & Miller, R. A. Effect of a Pseudomonas rhamnolipid biosurfactant on cell hydrophobicity and biodegradation of octadecane. Appl. Environ. Microbiol. 60, 2101–2106 (1994).

    CAS  PubMed  PubMed Central  Google Scholar 

  126. Allison, C., Lai, H. C. & Hughes, C. Co-ordinate expression of virulence genes during swarm-cell differentiation and population migration of Proteus mirabilis. Mol. Microbiol. 6, 1583–1591 (1992).

    Article  CAS  PubMed  Google Scholar 

  127. Callegan, M. C., Novosad, B. D., Ramtrez, R., Ghelardi, E. & Senesi, S. Role of swarming migration in the pathogenesis of Bacillus endophthalmitis. Invest. Opthalmol. Vis. Sci. 47, 4461–4467 (2006).

    Article  Google Scholar 

  128. Ammendola, A., et al. Serratia liquefaciens swarm cells exhibit enhanced resistance to predation by Tetrahymena sp. FEMS Microbiol. Lett. 164, 69–75 (1998).

    Article  CAS  PubMed  Google Scholar 

  129. Givskov, M., Eberl, L., Christiansen, G., Benedik, M. J. & Molin, S. Induction of phospholipase- and flagellar synthesis in Serratia liquefaciens is controlled by expression of the flagellar master operon flhD. Mol. Microbiol. 15, 445–454 (1995).

    Article  CAS  PubMed  Google Scholar 

  130. Lai, S., Tremblay, J. & Déziel, E. Swarming motility: a multicellular behavior conferring antimicrobial resistance. Environ. Microbiol. 11, 126–136 (2009).

    Article  CAS  PubMed  Google Scholar 

  131. Kim, W., Killam, T., Sood, V. & Surette, M. G. Swarm-cell differentiation in Salmonella enterica serovar Typhimurium results in elevated resistance to multiple antibiotics. J. Bacteriol. 185, 3111–3117 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  132. Butler, M. T., Wang, Q. & Harshey, R. M. Cell density and mobility protect swarming bacteria against antibiotics. Proc. Natl Acad. Sci. USA 107, 3776–3781 (2010). This study shows that the apparent enhanced antibiotic resistance that is enjoyed by swarming cells is due to their inherent high cell density and rapid movement.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  133. Tsuge, K., Ohata, Y. & Shoda, M. Gene yerP, involved in surfactin self-resistance in Bacillus subtilis. Antimicrob. Agents Chemother. 45, 3566–3573 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  134. Gooderham, W. J., Bains, M., McPhee, J. B., Wiegard, I. & Hancock, R. E. W. Induction by cationic antimicrobial peptides and involvement in intrinsic polymyxin and antimicrobial peptide resistance, biofilm formation, and swarming motility of PsrA in Pseudomonas aeruginosa. J. Bacteriol. 190, 5624–5634 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  135. Skerker, J. M. & Laub, M. T. Cell-cycle progression and the generation of asymmetry in Caulobacter crescentus. Nature Rev. Microbiol. 2, 325–337 (2004).

    Article  CAS  Google Scholar 

  136. Berleman, J. E & Kirby, J. R. Deciphering the hunting strategy of a bacterial wolfpack. FEMS Microbiol. Rev. 33, 942–957 (2009).

    Article  CAS  PubMed  Google Scholar 

  137. Stickler, D. J. & Feneley, R. C. The encrustation and blockage of long-term indwelling bladder catheters: a way forward in prevention and control. Spinal Cord 6 Apr 2010 (doi: 10.1038/sc.2010.32).

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

I am grateful to R. Belas, H. Berg, E. Déziel, R. Harshey, D. Kysela, L. McCarter, G. O'Toole, P. Rather, R. Rudner, J. Shrout and D. Weibel for thoughtful discussions about swarming motility and critical reading of the manuscript. I also thank P.R., G.O'T. and R.R. for donation of the bacterial strains used in figure 7b–d. Work in my laboratory is supported by the US National Institutes of Health (grant GM093030).

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    Daniel B. Kearns

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DATABASES

Entrez Genome Project

Bacillus subtilis

Paenibacillus vortex

Proteus mirabilis

Pseudomonas aeruginosa

Rhodosprillum centenum

Salmonella enterica

Serratia marcescens

Vibrio parahaemolyticus

Yersinia entercolitica

FURTHER INFORMATION

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Glossary

Planktonic

Of bacteria: growing as dispersed cells in a liquid environment.

Flagellum

A complex molecular machine, assembled from over 40 different proteins, that is the motor for swimming and swarming motility. Rotation of a membrane-anchored basal body rotates a long, extracellular, corkscrew-shaped filament that acts like a propeller to generate force.

Type IV pilus

A proteinaceous pilus that extends from one pole of the cell, attaches to a surface and retracts, thus acting as the motor for twitching motility. Retraction causes the cell body to move towards the anchor point of the pilus.

Focal-adhesion complex

A putative cell surface-associated complex that anchors a bacterium to a substrate and might act as a motor for gliding motility. When coupled to an internal motor, the cell body moves relative to the focal-adhesion complex.

Surfactant

A secreted molecule that associates with a surface and acts like a lubricant to reduce surface tension.

Hyperflagellate

Of a bacterium: with an increased number of flagella on the cell surface.

Quorum sensing

A strategy by which bacteria regulate gene expression in a manner that is dependent on high population density.

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Kearns, D. A field guide to bacterial swarming motility. Nat Rev Microbiol 8, 634–644 (2010). https://doi.org/10.1038/nrmicro2405

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