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A field guide to bacterial swarming motility

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.

References

  1. 1

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

    CAS  Article  Google Scholar 

  2. 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. 3

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

    CAS  Article  Google Scholar 

  4. 4

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

    CAS  Google Scholar 

  5. 5

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

    CAS  PubMed  Article  Google Scholar 

  6. 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).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  7. 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).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  8. 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).

    CAS  PubMed  Article  Google Scholar 

  9. 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).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  10. 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).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  11. 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.

    CAS  PubMed  Article  Google Scholar 

  12. 12

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

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  13. 13

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

    CAS  Article  Google Scholar 

  14. 14

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

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  15. 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).

    CAS  PubMed  Article  Google Scholar 

  16. 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).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  17. 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. 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).

    CAS  PubMed  Article  Google Scholar 

  19. 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).

    CAS  PubMed  Article  Google Scholar 

  20. 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. 21

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

    CAS  PubMed  Article  Google Scholar 

  22. 22

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

    CAS  PubMed  Article  Google Scholar 

  23. 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.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  24. 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.

    CAS  PubMed  Article  Google Scholar 

  25. 25

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

    Article  Google Scholar 

  26. 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.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  27. 27

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

    CAS  Article  Google Scholar 

  28. 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. 29

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

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  30. 30

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

    CAS  PubMed  Article  Google Scholar 

  31. 31

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

    CAS  PubMed  Article  Google Scholar 

  32. 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. 33

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

    CAS  PubMed  Article  Google Scholar 

  34. 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).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  35. 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.

    CAS  PubMed  Article  Google Scholar 

  36. 36

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

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  37. 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.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  38. 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).

    CAS  PubMed  Article  Google Scholar 

  39. 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).

    PubMed  Article  Google Scholar 

  40. 40

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

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  41. 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).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  42. 42

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

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  43. 43

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

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  44. 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).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  45. 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).

    CAS  PubMed  Article  Google Scholar 

  46. 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).

    CAS  PubMed  Article  Google Scholar 

  47. 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).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  48. 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).

    PubMed  Article  PubMed Central  Google Scholar 

  49. 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).

    CAS  PubMed  Article  Google Scholar 

  50. 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).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  51. 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).

    CAS  PubMed  Article  Google Scholar 

  52. 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).

    CAS  PubMed  Article  Google Scholar 

  53. 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).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  54. 54

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

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  55. 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).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  56. 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).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  57. 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).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  58. 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. 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).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  60. 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).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  61. 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.

    CAS  PubMed  Article  Google Scholar 

  62. 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).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  63. 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. 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).

    CAS  PubMed  Article  Google Scholar 

  65. 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).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  66. 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. 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).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  68. 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. 69

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

    CAS  PubMed  Article  Google Scholar 

  70. 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).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  71. 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).

    CAS  PubMed  Article  Google Scholar 

  72. 72

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

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  73. 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. 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).

    PubMed  Article  CAS  Google Scholar 

  75. 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).

    CAS  PubMed  Article  Google Scholar 

  76. 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).

    CAS  Article  Google Scholar 

  77. 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).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  78. 78

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

    CAS  PubMed  Article  Google Scholar 

  79. 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).

    CAS  PubMed  Article  Google Scholar 

  80. 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.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  81. 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).

    CAS  PubMed  Article  Google Scholar 

  82. 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.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  83. 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. 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).

    CAS  PubMed  Article  Google Scholar 

  85. 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).

    CAS  PubMed  Article  Google Scholar 

  86. 86

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

    CAS  Article  Google Scholar 

  87. 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. 88

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

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  89. 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. 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).

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  91. 91

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

    CAS  PubMed  Article  Google Scholar 

  92. 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).

    CAS  Article  Google Scholar 

  93. 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. 94

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

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  95. 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. 96

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

    CAS  PubMed  Article  Google Scholar 

  97. 97

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

    CAS  PubMed  Article  Google Scholar 

  98. 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).

    CAS  Article  Google Scholar 

  99. 99

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

    CAS  Article  Google Scholar 

  100. 100

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

    CAS  PubMed  Article  Google Scholar 

  101. 101

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

    CAS  PubMed  Article  Google Scholar 

  102. 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).

    CAS  PubMed  Article  Google Scholar 

  103. 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).

    CAS  PubMed  Article  Google Scholar 

  104. 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).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  105. 105

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

    Article  Google Scholar 

  106. 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. 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. 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).

    CAS  Article  Google Scholar 

  109. 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.

    CAS  PubMed  Article  Google Scholar 

  110. 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).

    CAS  PubMed  Article  Google Scholar 

  111. 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).

    CAS  PubMed  Article  Google Scholar 

  112. 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).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  113. 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).

    CAS  PubMed  Article  Google Scholar 

  114. 114

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

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  115. 115

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

    CAS  PubMed  Article  Google Scholar 

  116. 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. 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).

    CAS  PubMed  Article  Google Scholar 

  118. 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).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  119. 119

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

    CAS  PubMed  Article  Google Scholar 

  120. 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).

    CAS  PubMed  Article  Google Scholar 

  121. 121

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

    CAS  Article  Google Scholar 

  122. 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).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  123. 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).

    CAS  PubMed  Article  Google Scholar 

  124. 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. 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. 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).

    CAS  PubMed  Article  Google Scholar 

  127. 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. 128

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

    CAS  PubMed  Article  Google Scholar 

  129. 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).

    CAS  PubMed  Article  Google Scholar 

  130. 130

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

    CAS  PubMed  Article  Google Scholar 

  131. 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).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  132. 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.

    CAS  PubMed  Article  Google Scholar 

  133. 133

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

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  134. 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).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  135. 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).

    CAS  Article  Google Scholar 

  136. 136

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

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  137. 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).

    CAS  PubMed  Article  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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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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