A field guide to bacterial swarming motility

Nature Reviews Microbiology

Volumn 8, Issue 9, 2010, Pages 634-644

  Kearns, Daniel B ^a  

^a INDIANA UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

SURFACTANT;

BACTERIOLOGY; BACTERIUM; CELL MOTILITY; CELL MOTION; FLAGELLUM; NONHUMAN; PHENOTYPE; PLANKTON; PRIORITY JOURNAL; REVIEW; SURFACE TENSION; SWARMING MOTILITY;

BACTERIA; BACTERIAL PHYSIOLOGICAL PHENOMENA; FLAGELLA; MOVEMENT;

BACTERIA (MICROORGANISMS);

EID: 77955652704     PISSN: 17401526     EISSN: None     Source Type: Journal    
DOI: 10.1038/nrmicro2405     Document Type: Review

References (137)

1. Verstraeten, N. et al. Living on a surface: swarming and biofilm formation. Trends Microbiol. 16, 496-506 (2008).
2. Henrichsen, J. Bacterial surface translocation: a survey and a classification. Bacteriol. Rev. 36, 478-503 (1972).
3. Jarrell, K. F. & McBride, M. J. The surprisingly diverse ways that prokaryotes move. Nature Rev. Microbiol. 6, 466-476 (2008).
4. Mattick, J. S. Type IV pili and twitching motility. Annu. Rev. Biochem. 56, 289-314 (2002).
5. Mignot, T. The elusive engine in Myxococcus xanthus gliding motility. Cell. Mol. Life Sci. 64, 2733-2745 (2007).
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).
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).
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).
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).
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).
11. Kearns, D. B. & Losick, R. Swarming motility in undomesticated Bacillus subtilis. Mol. Microbiol. 49, 581-590 (2003).
12. Patrick, J. E. & Kearns, D. B. Laboratory strains of Bacillus subtilis do not exhibit swarming motility. J. Bacteriol. 191, 7129-7133 (2009).
13. Ghelardi, E. et al. Swarming behavior of and hemolysin BL secretion by Bacillus cereus. Appl. Env. Microbiol. 73, 4089-4093 (2007).
14. Kim, W. & Surette, M. G. Prevalence of surface swarming behavior in Salmonella. J. Bacteriol. 187, 6580-6583 (2005).
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).
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).
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).
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).
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).
20. Eberl, L., Molin, S. & Givskov, M. Surface motility of Serratia liquefaciens MG1. J. Bacteriol. 181, 1703-1712 (1999).
21. Tremblay, J. & Déziel, E. Improving the reproducibility of Pseudomonas aeruginosa swarming motility assays. J. Basic Microbiol. 48, 509-515 (2008).
22. Mayfield, C. I. & Inniss, W. E. A rapid, simple method for staining bacterial flagella. Can. J. Microbiol. 23, 1311-1313 (1977).
23. Turner, L., Ryu, W. S. & Berg, H. C. Real-time imaging of fluorescent flagellar filaments. J. Bacteriol. 182, 2793-2801 (2000).
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).
25. Hoeniger, J. F. M. Development of flagella by Proteus mirabilis. J. Gen. Microbiol. 40, 29-42 (1965).
26. Jones, B. V., Young, R., Mahenthiralingam, E. &Stickler, D. J. Ultrastructure of Proteus mirabilis swarmer cell rafts and role of swarming in catheterassociated urinary tract infection. Infect. Immun. 72, 3941-3950 (2004).
27. Chevance, F. F. V. & Hughes, K. T. Coordinating assembly of a bacterial macromolecular machine. Nature Rev. Microbiol. 6, 455-465 (2008).
28. Shinoda, S. & Okamoto, K. Formation and function of Vibrio parahaemolyticus lateral flagella. J. Bacteriol. 129, 1266-1271 (1977).
29. Alberti, L. & Harshey, R. M. Differentiation of Serratia marcescens 274 into swimmer and swarmer cells. J. Bacteriol. 172, 4322-4328 (1990).
30. Merino, S., Shaw, J. G. & Tomás, J. M. Bacterial lateral flagella: an inducible flagella system. FEMS Microbiol. Lett. 263, 127-135 (2006).
31. Ulitzur, S. & Kessel, M. Giant flagellar bundles of Vibrio alginolyticus (NCMB 1803). Arch. Mikrobiol. 94, 331-339 (1973).
32. Schneider, W. R. & Doetsch, R. N. Effect of viscosity on bacterial motility. J. Bacteriol. 117, 696-701 (1974).
33. Berg, H. C. & Turner, L. Movement of microorganisms in viscous environments. Nature 278, 349-351 (1979).
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).
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).
36. Darnton, N. C., Turner, L., Rojevsky, S. & Berg, H. C. Dyanmics of bacterial swarming. Biophys. J. 98, 2082-2090 (2010).
37. Turner, L., Zhang, R., Darnton, N. C. & Berg, H. C. Visualization of flagella during bacterial swarming. J. Bacteriol. 192, 3259-3267 (2010).
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).
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).
40. Kirov, S. M. et al. Lateral flagella and swarming motility in Aeromonas species. J. Bacteriol. 184, 547-555 (2002).
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).
42. Kim, Y. K. & McCarter, L. L. Analysis of the polar flagellar gene system of V. parahaemolyticus. J. Bacteriol. 182, 3693-3704 (2000).
43. Doyle, T. B., Hawkins, A. C. & McCarter, L. L. The complex flagellar torque generator of Pseudomonas aeruginosa. J. Bacteriol. 186, 6341-6350 (2004).
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).
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).
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).
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).
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).
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).
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).
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).
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).
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).
54. Kearns, D. B. & Losick, R. Cell population heterogeneity during growth of Bacillus subtilis. Genes Dev. 19, 3083-3094 (2005).
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).
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).
57. Soo, P. C. et al. Regulation of swarming motility and flhDCSm expression by RssAB signaling in Serratia marcescens. J. Bacteriol. 190, 2496-2504 (2008).
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).
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).
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).
61. Morrison, R. B. & Scott, A. Swarming of Proteus\a solution to an old problem. Nature 211, 255-257 (1966).
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).
63. Girgis, H. S., Liu, Y., Ryu, W. S. & Tavazoie, S. A comprehensive genetic characterization of bacterial motility. PLOS Genet. 3, 154-166 (2007).
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).
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).
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).
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).
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).
69. Peypoux, F., Bonmatin, J. M. & Wallach, J. Recent trends in the biochemistry of surfactin. Appl. Microbiol. Biotechnol. 51, 553-563 (1999).
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).
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).
72. Caiazza, N. C., Shanks, R. M. & O'Toole, G. A. Rhamnolipids modulate swarming patterns of Pseudomonas aeruginosa. J. Bacteriol. 187, 7351-7361 (2005).
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).
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).
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).
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).
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).
78. Magnuson, R., Solomon, J. & Grossman, A. D. Biochemical and genetic characterization of a competence pheromone from B. subtilis. Cell 77, 207-216 (1994).
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).
80. Belas, R., Simon, M. & Silverman, M. Regulation of lateral flagella gene transcription in Vibrio parahaemolyticus. J. Bacteriol. 167, 210-218 (1986).
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).
82. Rauprich, O. et al. Periodic phenomena in Proteus mirabilis swarm colony development. J. Bacteriol. 178, 6525-6538 (1996)
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).
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).
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).
86. Mitchison, T. & Kirschner, M. Dynamic instability of microtubule growth. Nature 312, 237-242 (1984).
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).
88. Tolker-Nielsen, T. et al. Assessment of flhDC mRNA levels in Serratia liquefaciens swarm cells. J. Bacteriol. 182, 2680-2686 (2000).
89. Belas, R. & Colwell, R. R. Scanning electron microscope observation of the swarming phenomenon of Vibrio parahaemolyticus. J. Bacteriol. 150, 956-959 (1982).
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).
91. Mariconda, S., Wang, Q. & Harshey, R. M. A mechanical role for the chemotaxis system in swarming motility. Mol. Microbiol. 60, 1590-1602 (2006).
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).
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).
94. Matsuyama, T. et al. Dynamic aspects of the structured cell population in swarming colony of Proteus mirabilis. J. Bacteriol. 182, 385-393 (2000).
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).
96. Douglas, C. W. I. & Bisset, K. A. Development of concentric zones in the Proteus swarm colony. J. Med. Microbiol. 9, 497-500 (1976).
97. Rudner, R., Martsinkevich, O, Leung, W. & Jarvis, E. D. Classification and genetic characterization of pattern forming Bacilli. Mol. Microbiol. 27, 687-703 (1998).
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).
99. Wadhams, G. H. & Armitage, J. P. Making sense of it all: bacterial chemotaxis. Nature Rev. Mol. Cell Biol. 5, 1024-1037 (2004).
100. Adler, J. Chemotaxis in bacteria. Science 153, 708-716 (1966).
101. Hughes, H. A reconsideration of the swarming of Proteus vulgaris. J. Gen. Microbiol. 17, 49-58 (1957).
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).
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).
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).
105. Ragatz, L., Jiang, Z. Y., Bauer, C. & Gest, H. Phototactic purple bacteria. Nature 370, 104 (1994).
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).
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).
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).
109. McCarter, L., Hilmen, M. & Silverman, M. Flagellar dynamometer controls swarmer cell differentiation of V. parahaemolyticus. Cell 54, 345-351 (1988).
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).
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).
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).
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).
114. Darnton, N. C. & Berg, H. C. Bacterial flagella are firmly anchored. J. Bacteriol. 190, 8223-8224 (2008).
115. Jones, H. E. & Park, R. W. A. The short forms and long forms of Proteus. J. Gen. Microbiol. 47, 359-367 (1967).
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).
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).
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).
119. Kim, W. & Surette, M. G. Metabolic differentiation in actively swarming Salmonella. Mol. Microbiol. 54, 702-714 (2004).
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).
121. Wasserman, H. H., Keggi, J. J. & McKeon, J. E. Serratamolide, a metabolic product of Serratia. J. Am. Chem. Soc. 83, 4107-4108 (1961).
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).
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).
124. Zhang, Y. & Miller, R. A. Enhanced octadecane dispersion and biodegradation by a Pseudomonas rhamnolipid surfactant (biosurfactant). Appl. Environ. Microbiol. 58, 3276-3282 (1992).
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).
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).
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).
128. Ammendola, A., et al. Serratia liquefaciens swarm cells exhibit enhanced resistance to predation by Tetrahymena sp. FEMS Microbiol. Lett. 164, 69-75 (1998).
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).
130. Lai, S., Tremblay, J. & Déziel, E. Swarming motility: a multicellular behavior conferring antimicrobial resistance. Environ. Microbiol. 11, 126-136 (2009).
131. Kim, W., Killam, T., Sood, V. & Surette, M. G. Swarmcell differentiation in Salmonella enterica serovar Typhimurium results in elevated resistance to multiple antibiotics. J. Bacteriol. 185, 3111-3117 (2003).
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).
133. Tsuge, K., Ohata, Y. & Shoda, M. Gene yerP, involved in surfactin self-resistance in Bacillus subtilis. Antimicrob. Agents Chemother. 45, 3566-3573 (2001).
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).
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).
136. Berleman, J. E & Kirby, J. R. Deciphering the hunting strategy of a bacterial wolfpack. FEMS Microbiol. Rev. 33, 942-957 (2009).
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).