Cited by 1,483Bacterial biofilms and quorum sensingBacterial Genetics and BiotechnologyMicro and Nano Robotics

A field guide to bacterial swarming motility

Open access
Kearns, Daniel B.·2010·Nature Reviews Microbiology

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.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1038/nrmicro2405

Cites

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • It is difficult to monitor or capture living bacteria, which are small and move by swimming, swarming, gliding, and twitching in solution.

    “However, it is difficult to monitor or capture living bacteria, which are small and move by swimming, swarming, gliding, and twitching in solution14.”

    From Label-Free Detection of Single Living Bacteria via Electrochemical Collision Event (2016) · cites this paper as [14]

    The paper’s section on studying swarming motility in the laboratory says swarming occurs over a solid surface and distinguishes it from swimming in water. That contradicts the claim that all four forms of movement occur in solution. The passages found also do not say that living bacteria are difficult to monitor or capture because they are small. (LLM, conf=0.86)

    Checked by a reasoning model — may be wrong.

    Experimental — accuracy not yet measured

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

No references could be resolved yet.

Research works printed but not linked: 131

  1. [1]Verstraeten N Braeken K Debkumari B Fauvart M Fransaer J Vermant J Michiels J Living on a surface: swarming and biofilm formation Trends Microbiol 2008 16 496 506 18775660
  2. [2]Henrichsen J Bacterial surface translocation: a survey and a classification Bacteriol. Rev 1972 36 478 503 4631369 PMC408329
  3. [3]Jarrell KF McBride MJ The surprisingly diverse ways that prokaryotes move Nat. Rev. Microbiol 2008 6 466 476 18461074
  4. [4]Mattick JS Type IV pili and twitching motility Annu. Rev. Biochem 2002 56 289 314 12142488
  5. [5]Mignot T The elusive engine in Myxococcus xanthus gliding motility Cell Mol. Life Sci 2007 64 2733 2745 17653507 PMC11136220
  6. [6]Matsuyama T Kaneda K Nakagawa Y Isa K Hara-Hotta H Yano I A novel extracellular cyclic lipopeptide which promotes flagellum-dependent and – independent spreading growth of Serratia marcescens J. Bacteriol 1992 174 1769 1776 1548227 PMC205777
  7. [7]Kinsinger RF Kearns DB Hale M Fall R Genetic requirements for potassium ion-dependent colony spreading in Bacillus subtilis J. Bacteriol 2005 187 8462 8469 16321950 PMC1317027
  8. [8]Murray TS Kazmierczak BI Pseudomonas aeruginosa exhibits sliding motiliy in the absence of type IV pili and flagella J. Bacteriol 2008 190 2700 2708 18065549 PMC2293233
  9. [9]Matsuyama T Bhasin A Harshey RM Mutational analysis of flagellum-independent surface spreading of Serratia marcescens 274 on a low-agar medium J. Bacteriol 1995 177 987 991 7860610 PMC176693
  10. [10]Be'er A Smith RS Zhang HP Florin EL Payne SM Swinney HL Paenibacillus dendritiformis bacterial colony growth depends on surfactant but not on bacterial motion J. Bacteriol 2009 191 5758 5764 19617369 PMC2737951
  11. [11]Kearns DB Losick R Swarming motility in undomesticated Bacillus subtilis Mol. Microbiol 2003 49 581 590 12864845
  12. [12]Patrick JE Kearns DB Laboratory strains of Bacillus subtilis do not exhibit swarming motility J. Bacteriol 2009 191 7129 7133 19749039 PMC2772471
  13. [13]Ghelardi E Celandroni F Salvetti S Ceragioli M Beecher DJ Senesi S Wong ACL Swarming behavior of and hemolysins BL secretion by Bacillus cereus Appl. Env. Microbiol 2007 73 4089 4093 17449693 PMC1932716
  14. [14]Kim W Surette MG Prevalence of surface swarming behavior in Salmonella J. Bacteriol 2005 187 6580 6583 16159794 PMC1236657
  15. [15]Velicer GJ Kroos L Lenski RE Loss of social behaviors by Myxococcus xanthus during evolution in an unstructured habitat Proc. Natl. Acad. Sci. USA 1998 95 12376 12380 9770494 PMC22839
  16. [16]Julkowska D Obuchowski M Holland BI Séror SJ 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 2005 187 65 76 15601689 PMC538812
  17. [17]Young GM Smith MJ Minnich SA Miller VL The Yersinia enterocolitica motility master regulatory operon, flhDC, is required for flagellin production, swimming motility, and swarming motility J. Bacteriol 1999 181 2823 2833 10217774 PMC93725
  18. [18]Harshey RM Matsuyama T Dimorphic transition in Escherichia coli and Salmonella typhimurium: surface-induced differentiation into hyperflagellate swarmer cells Proc. Natl. Acad. Sci. USA 1994 91 8631 8635 8078935 PMC44660
  19. [19]Jones HE Park RWA The influence of medium composition on the growth and swarming of Proteus J. Gen. Microbiol 1967b 47 369 378 6035678
  20. [20]Eberl L Molin S Givskov M Surface motility of Serratia liquefaciens MG1 J. Bacteriol 1999 181 1703 1712 10074060 PMC93566
  21. [21]Tremblay J Déziel E Improving the reproducibility of Pseudomonas aeruginosa swarming motility assays J. Basic Microbiol 2008 48 509 515 18785657
  22. [22]Mayfield CI Inniss WE A rapid, simple method for staining bacterial flagella Can. J. Microbiol 1977 23 1311 1313 71191
  23. [23]Turner L Ryu WS Berg HC Real-time imaging of fluorescent flagellar filaments J. Bacteriol 2000 182 2793 2801 10781548 PMC101988
  24. [24]Copeland MF Flickinger ST Tuson HH Weibel DB Studying the dynamics of flagella in multicellular communities of Escherichia coli by using biarsenical dyes Appl. Environ. Microbiol 2010 76 1241 1250 20023074 PMC2820973
  25. [26]Jones BV Young R Mahenthiralingam E Stickler DJ Ultrastructure of Proteus mirabilis swarmer cell rafts and role of swarming in catheter-associated urinary tract infection Infect. Immun 2004 72 3941 3950 15213138 PMC427392
  26. [27]Chevance FFV Hughes KT Coordinating assembly of a bacterial macromolecular machine Nat. Rev. Microbiol 2008 6 455 465 18483484 PMC5963726
  27. [28]Shinoda S Okamoto K Formation and function of Vibrio parahaemolyticus lateral flagella J. Bacteriol 1977 129 1266 1271 845115 PMC235098
  28. [29]Alberti L Harshey RM Differentiation of Serratia marcescens 274 into swimmer and swarmer cells J. Bacteriol 1990 172 4322 4328 2198253 PMC213257
  29. [30]Merino S Shaw JG Tomás JM Bacterial lateral flagella: an inducible flagella system FEMS Microbiol. Lett 2006 263 127 135 16978346
  30. [31]Ulitzur S Kessel M Giant flagellar bundles of Vibrio alginolyticus (NCMB 1803) Arch. Mikrobiol 1973 94 331 339 4131532
  31. [32]Schneider WR Doetsch RN Effect of viscosity on bacterial motility J. Bacteriol 1974 117 696 701 4204439 PMC285562
  32. [33]Berg HC Turner L Movement of microorganisms in viscous environments Nature 1979 278 349 351 370610
  33. [34]Atsumi T Maekawa Y Yamada T Kawagishi I Imae Y Homma M Effect of viscosity on swimming by the lateral and polar flagella of Vibrio alginolyticus J. Bacteriol 1996 178 5024 5026 8759871 PMC178290
  34. [35]Zhang R Turner L Berg HC The upper surfaces of an Escherichia coli swarm is stationary Proc. Natl. Acad. Sci. USA 2010 107 288 290 19966294 PMC2806745
  35. [36]Darnton NC Turner L Rojevsky S Berg HC Dyanmics of bacterial swarming Biophys. J in press PMC2872219 20483315
  36. [37]Turner L Zhang R Darnton NC Berg HC Visualization of flagella during bacterial swarming J. Bacteriol in press PMC2897679 20363932
  37. [38]Ragatz L Jiang Z-Y Bauer C Gest H Macroscopic phototactic behavior of the purple photosynthetic bacterium Rhodospirillum centenum Arch. Microbiol 1995 163 1 6 7710317
  38. [39]Gavín R Rabaan AA Merino S Tomas JM Gryllos I Shaw JG Lateral flagella of Aeromonas species are essential for epithelial cell adherence and biofilm formation Mol. Microbiol 2002 43 383 397 11985716
  39. [40]Kirov SM Tassell BC Semmler ABT O'Donovan LA Rabaan AA Shaw JG Lateral flagella and swarming motility in Aeromonas species J. Bacteriol 2002 184 547 555 11751834 PMC139559
  40. [41]McCarter LL Wright ME Identification of genes encoding components of the swarmer cell flagellar motor and propeller and a sigma factor controlling differentiation of Vibrio parahaemolyticus J. Bacteriol 1993 175 3361 3371 8501040 PMC204733
  41. [42]Kim Y-K McCarter LL Analysis of the polar flagellar gene system of V. parahaemolyticus J. Bacteriol 2000 182 3693 3704 10850984 PMC94540
  42. [43]Doyle TB Hawkins AC McCarter LL The complex flagellar torque generator of Pseudomonas aeruginosa J. Bacteriol 2004 186 6341 6350 15375113 PMC516612
  43. [44]Toutain CM Zegans ME O'Toole GA Evidence for two flagellar stators and their role in the motility of Pseudomonas aeruginosa J. Bacteriol 2005 187 771 777 15629949 PMC543560
  44. [45]Senesi S Celandroni F Salvetti S Beecher DJ Wong ACL Ghelardi E Swarming motility in Bacillus cereus and characterization of a fliY mutant impaired in swarm cell differentiation Microbiol 2002 148 1785 1794 12055298
  45. [46]Lai HC Gygi D Fraser GM Hughes C A swarming defective mutant of Proteus mirabilis lacking a putative cation-transporting membrane P-type ATPase Microbiol 1998 144 1957 1961 9695928
  46. [47]Furness RB Fraser GM Hay NA 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 1997 179 5585 5588 9287017 PMC179433
  47. [48]Köhler T Curty LK 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 2000 182 5990 5996 11029417 PMC94731
  48. [49]Rashid MH Kornberg A Inorganic polyphosphate is needed for swimming, swarming, and twitching motilities of Pseudomonas aeruginosa Proc. Natl. Acad. Sci. USA 2000 97 4885 4890 10758151 PMC18327
  49. [50]Hay NA Tipper DJ Gygi D Hughes C A nonswarming mutant of Proteus mirabilis lacks the Lrp global transcriptional regulator J. Bacteriol 1997 179 4741 4746 9244260 PMC179319
  50. [51]Dufour A Furness RB Hughes C Novel genes that upregulate the Proteus mirabilis master operon controlling flagellar biogenesis and swarming Mol. Microbiol 1998 29 741 751 9723914
  51. [52]Kearns DB Chu F Rudner R Losick R Genes governing swarming in Bacillus subtilis and evidence for a phase variation mechanism controlling surface motility Mol. Microbiol 2004 52 35 369 15066026
  52. [53]Calvio C Celandroni F Ghelardi E Amati G Salvetti S Ceciliani F Galizzi A Senesi S Swarming differentiation and swimming motility in Bacillus subtilis are controlled by swrA, a newly identified dicistronic operon J. Bacteriol 2005 187 5356 5366 16030230 PMC1196031
  53. [54]Kearns DB Losick R Cell population heterogeneity during growth of Bacillus subtilis Genes Dev 2005 19 3083 3094 16357223 PMC1315410
  54. [55]Wang Q Suzuki A Mariconda S Powollik S Harshey RM Sensing wetness: a new role for the bacterial flagellum EMBO J 2005 24 2034 2042 15889148 PMC1142604
  55. [56]Morgenstein RM Clemmer KM Rather PN Loss of the WaaL O-antigen ligase prevents surface activation of the flagellar gene cascase in Proteus mirabilis J. Bacteriol in press PMC2901702 20382766
  56. [57]Soo P-C Horng Y-T Wei J-R Shu J-C Lu C-C Lai H-C Regulation of swarming motility and flhDCSm expression by RssAB signaling in Serratia marcescens J. Bacteriol 2008 190 2496 2504 18223092 PMC2293207
  57. [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 1998 180 6126 6139 9829920 PMC107696
  58. [59]Stevenson LG Rather PN A novel gene involved in regulating the flagellar gene cascade in Proteus mirabilis J. Bacteriol 2006 188 7830 7839 16980463 PMC1636314
  59. [60]Claret L Hughes C Rapid turnover of FlhD and FlhC, the flagellar regulon transcriptional activator proteins, during Proteus swarming J. Bacteriol 2000 182 833 836 10633123 PMC94352
  60. [61]Morrison RB Scott A Swarming of Proteus – a solution to an old problem Nature 1966 211 255 257 5965543
  61. [62]O'Rear J Alberti L Harshey RM Mutations that impair swarming motility in Serratia marcescens 274 include but are not limited to those affecting chemotaxis or flagellar function J. Bacteriol 1992 174 6125 6137 1400161 PMC207679
  62. [63]Girgis HS Liu Y Ryu WS Tavazoie S A comprehensive genetic characterization of bacterial motility PLOS Genet 2007 3 e154 166 PMC1976333 17941710
  63. [64]Julkowska D Obuchowski M Holland BI Séror SJ 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 Microbiol 2004 150 1839 1849 15184570
  64. [65]Toguchi A Siano M Burkart M Harshey RM Genetics of swarming motility in Salmonella enterica serovar typhimurium: critical role for lipopolysaccharide J. Bacteriol 2000 182 6308 6321 11053374 PMC94776
  65. [67]Chen BG Turner L Berg HC The wetting agent required for swarming in Salmonella enterica serovar typhimurium is not a surfactant J. Bacteriol 2007 189 8750 8753 17905988 PMC2168935
  66. [68]Lindum PW Anthoni U Christophersen C Eberl L Molin S Givskov M N-acyl-L-homoserine lactone autoinducers control production of an extracellular lipopeptide biosurfactant required for swarming motility in Serratia liquefaciens MG1 J. Bacteriol 1988 180 6384 6388 9829950 PMC107727
  67. [69]Peypoux F Bonmatin JM Wallach J Recent trends in the biochemistry of surfactin Appl. Microbiol. Biotechnol 1999 51 553 563 10390813
  68. [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 1968 31 488 494 4968234
  69. [71]Cosamina P Rodriguez F de Ferra F Grandi G Perego M Venema G van Sinderen D Sequence and analysis of the genetic locus responsible for surfactin synthesis in Bacillus subtilis Mol. Microbiol 1993 8 821 831 8355609
  70. [72]Caiazza NC Shanks RM O'Toole GA Rhamnolipids modulate swarming patterns of Pseudomonas aeruginosa J. Bacteriol 2005 187 7351 7361 16237018 PMC1273001
  71. [73]Ochsner UA 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 1994 31 19787 19795 8051059
  72. [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 2003 149 2005 2013 12904540
  73. [75]Ochsner UA Reiser J Autoinducer-mediated regulation of rhamnolipid biosurfactant synthesis in Pseudomonas aeruginosa Proc. Natl. Acad. Sci. USA 1995 92 6424 6428 7604006 PMC41530
  74. [76]Eberl L Winson MK Sternberg C Stewart GSAB Christiansen G Chhabra SR Bycroft B Williams P Molin S Givskov M Involvement of N-acyl-L-homoserine lactone autoinducers in controlling the multicellular behavior of Serratia liquefaciens Mol. Microbiol 1996 20 127 136 8861211
  75. [77]Magnuson R Solomon J Grossman AD Biochemical and genetic characterization of a competence pheromone from B. subtilis Cell 1994 77 207 216 8168130
  76. [78]Francez-Charlot A Laugel B Van Gemert A Dubarry N Wiorowski F Castanié-Cornet M-P Gutierrez C Cam K RcsCDB His-Asp phosphorelay system negatively regulates the flhDC operon in Escherichia coli Mol. Microbiol 2003 49 823 832 12864862
  77. [79]Belas R Simon M Silverman M Regulation of lateral flagella gene transcription in Vibrio parahaemolyticus J. Bacteriol 1986 167 210 218 3013835 PMC212863
  78. [80]Hoeniger JFM Cellular changes accompanying the swarming of Proteus mirabilis. I. Observation of living cultures Can. J. Microbiol 1964 10 1 9 14124856
  79. [81]Rauprich O Matsushita M Weijer CJ Siegert F Esipov SE Shapiro JA Periodic phenomena in Proteus mirabilis swarm colony development J. Bacteriol 1996 178 6525 6538 8932309 PMC178539
  80. [82]Williams FD Anderson DM Hoffman PS Schwarzhoff RH Leonard S Evidence against the involvement of chemotaxis in swarming Proteus mirabilis J. Bacteriol 1976 127 237 248 776927 PMC233056
  81. [83]Chen R Guttenplan SB Blair KM Kearns DB Role of the σD-dependent autolysins in Bacillus subtilis population heterogeneity J. Bacteriol 2009 191 5775 5784 19542270 PMC2737971
  82. [84]Zheng Y Wong ML Alberts B Mitchison Nucleation of microtubule assembly by a γ-tubulin-containing ring complex Nature 1995 378 578 583 8524390
  83. [85]Mitchison T Kirschner M Dynamic instability of microtubule growth Nature 1984 312 237 242 6504138
  84. [86]Hoeniger JFM Cellular changes accompanying the swarming of Proteus mirabilis. II. Observations of stained organisms Can. J. Microbiol 1965 12 113 123 4162515
  85. [87]Tolker-Nielsen T Christiansen AB Holmstrøm K Eberl L Rasmussen TB Sternberg C Heydorn A Molin S Givskov M Assessment of flhDC mRNA levels in Serratia liquefaciens swarm cells J. Bacteriol 2000 182 2680 2686 10781533 PMC101962
  86. [88]Belas R Colwell RR Scanning electron microscope observation of the swarming phenomenon of Vibrio parahaemolyticus J. Bacteriol 1982 150 956 959 7068539 PMC216449
  87. [89]Ingham CJ Ben Jacob E Swarming and complex pattern formation in Paenibacillus vortex studied by imaging and tracking cells BMC Microbiol 2008 8 36 18298829 PMC2268691
  88. [90]Mariconda S Wang Q Harshey RM A mechanical role for the chemotaxis system in swarming motility Mol. Microbiol 2006 60 1590 1602 16796690
  89. [93]Matsuyama T Takagi Y Nakagawa Y Itoh H Wakita J Matsushita M Dynamic aspects of the structured cell population in swarming colony of Proteus mirabilis J. Bacteriol 2000 182 385 393 10629184 PMC94287
  90. [94]Bisset KA Douglas CWI A continuous study of morphological phase in the swarm of Proteus J. Med. Microbiol 1975 9 229 231 778391
  91. [95]Douglas CWI Bisset KA Development of concentric zones in the Proteus swarm colony J. Med. Microbiol 1976 9 497 500 794478
  92. [96]Tremblay J Richardson A-P Lepine F Déziel E Self-produced extracellular stimuli modulate the Pseudomonas aeruginosa swarming motility behavior Environ. Microbiol 2007 9 2622 2630 17803784
  93. [97]Rudner R Martsinkevich O Leung W Jarvis ED Classification and genetic characterization of pattern forming Bacilli Mol. Microbiol 1998 27 687 703 9515696
  94. [98]Patrick JE Kearns DB MinJ (YvjD) is a topological determinant of cell division in Bacillus subtilis Mol. Microbiol 2008 70 1166 1179 18976281
  95. [99]Wadhams GH Armitage JP Making sense of it all: bacterial chemotaxis Nat. Rev. Mol. Cell Biol 2004 5 1024 1037 15573139
  96. [100]Adler J Chemotaxis in bacteria Science 1966 153 708 716 4957395
  97. [101]Hughes H A reconsideration of the swarming of Proteus vulgaris J. Gen. Microbiol 1957 17 49 58 13475671
  98. [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 2007 64 57 67 17376072
  99. [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 1993 8 53 60 8497197
  100. [104]Sar N McCarter L Simon M Silverman M Chemotactic control of the two flagellar systems of Vibrio parahaemolyticus J. Bacteriol 1990 172 334 341 2294089 PMC208437
  101. [106]Burkhart M Toguchi A Harshey RM The chemotaxis system, but not chemotaxis, is essential for swarming motility in Escherichia coli Proc. Natl. Acad. Sci. USA 1998 95 2568 2573 9482927 PMC19416
  102. [107]Jiang ZY Gest H Bauer CE Chemosensory and photosensory perception in purple photosynthetic bacteria utilize common signal transduction components J. Bacteriol 1997 179 5720 5727 9294427 PMC179459
  103. [108]Berleman JE Bauer CE A che-like signal transduction cascade involved in controlling flagella biosynthesis in Rhodospirillum centenum Mol. Microbiol 2005 55 1390 1402 15720548
  104. [109]McCarter L Hilmen M Silverman M Flagellar dynamometer controls swarmer cell differentiation of V. parahaemolyticus Cell 1988 54 345 351 3396074
  105. [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 1996 20 693 699 8793868
  106. [111]Jaques S Kim Y-K McCarter LL Mutations conferring resistance to phenamil and amiloride, inhibitors of sodium-driven motility of Vibrio parahaemolyticus Proc. Natl. Acad. Sci. USA 1999 96 5740 5745 10318954 PMC21930
  107. [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 2005 187 6789 6803 16166542 PMC1251568
  108. [113]Attmannspacher U Scharf BE Harshey RM FliL is essential for swarming: motor rotation in absence of FliL fractures the flagellar rod in swarmer cells of Salmonella enterica Mol. Microbiol 2008 68 328 341 18284590
  109. [114]Darnton NC Berg HC Bacterial flagella are firmly anchored J. Bacteriol 2008 190 8223 8224 18849436 PMC2593247
  110. [115]Jones HE Park RWA The short forms and long forms of Proteus J. Gen. Microbiol 1967 47 359 367 6035677
  111. [116]Falkinham JO III Hoffman PS Unique developmental characteristics of the swarm and short cells of Proteus vulgaris and Proteus mirabilis J. Bacteriol 1984 158 1037 1040 6427187 PMC215547
  112. [117]Wang Q Frye JG McClelland M Harshey RM Gene expression patterns during swarming in Salmonella typhimurium: genes specific to surface growth and putative new motility and pathogenicity genes Mol. Microbiol 2004 52 169 187 15049819
  113. [118]Overhage J Bains M Brazas MD Hancock REW Swarming of Pseudomonas aeruginosa is a complex adaptation leading to increased production of virulence factors and antibiotic resistance J. Bacteriol 2008 190 2671 2679 18245294 PMC2293252
  114. [119]Kim W Surette MG Metabolic differentiation in actively swarming Salmonella Mol. Microbiol 2004 54 702 714 15491361
  115. [120]Andersen JB Koch B Harder Nielsen T Sørensen D Hansen M Nybroe O Christophersen C Sørensen J Molin S Givskov M Surface motility in Pseudomonas sp., DSS73 is required for efficient biological containment of the root-pathogenic microfungi Rhizoctonia solani and Pythium ultimum Microbiol 2003 149 37 46 12576578
  116. [122]Carrillo C Teruel JA Aranda FJ Ortiz A Molecular mechanism of membrane permeabilization by the peptide antibiotic surfactin Biochim. Biophys. Acta 2003 1611 91 97 12659949
  117. [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 1998 84 769 776 9674130
  118. [124]Zhang Y Miller RA Enhanced octadecane dispersion and biodegradation by a Pseudomonas rhamnolipid surfactant (biosurfactant) Appl. Environ. Microbiol 1992 58 3276 3282 1444363 PMC183091
  119. [125]Zhang Y Miller RA Effect of a Pseudomonas rhamnolipid biosurfactant on cell hydrophobicity and biodegradation of octadecane Appl. Environ. Microbiol 1994 60 2101 2106 8031099 PMC201607
  120. [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 1992 6 1583 1591 1495387
  121. [127]Callegan MC Novosad BD Ramtrez R Ghelardi E Senesi S Role of swarming migration in the pathogenesis of Bacillus endophthalmitis Investig. Opthalmol. Vis. Sci 2006 47 4461 4467 17003440
  122. [128]Ammendola A Geisenberger O Andersen JB Givskov M Schleifer K-H Eberl L Serratia liquefaciens swarm cells exhibit enhanced resistance to predation by Tetrahymena sp. FEMS Microbiol. Lett 1998 164 69 75 9675853
  123. [129]Givskov M Eberl L Christiansen G Benedik MJ Molin S Induction of phospholipase- and flagellar synthesis in Serratia liquefaciens is controlled by expression of the flagellar master operon flhD Mol. Microbiolx 1995 15 445 454 7783615
  124. [130]Lai S Tremblay J Déziel E Swarming motility: a multicellular behavior conferring antimicrobial resistance Environ. Microbiol 2009 11 126 136 18793317
  125. [131]Kim W Killam T Sood V Surette MG Swarm-cell differentiation in Salmonella enterica serovar typhimurium results in elevated resistance to multiple antibiotics J. Bacteriol 2003 185 3111 3117 12730171 PMC154059
  126. [132]Butler MT Wang Q Harshey RM Cell density and mobility protect swarming bacteria against antibiotics Proc. Natl. Acad. Sci. USA 2010 PMC2840483 20133590
  127. [133]Tsuge K Ohata Y Shoda M Gene yerP, involved in surfactin self-resistance in Bacillus subtilis Antimicrob. Agents Chemother 2001 45 3566 3573 11709341 PMC90870
  128. [134]Gooderham WJ Bains M McPhee JB Wiegard I Hancock REW 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 2008 190 5624 5634 18556795 PMC2519372
  129. [135]Skerker JM Laub MT Cell-cycle progression and the generation of asymmetry in Caulobacter crescentus Nat. Rev. Microbiol 2 325 337 15031731
  130. [136]Berleman JE Kirby JR Deciphering the hunting strategy of a bacterial wolfpack FEMS Microbiol. Rev 2009 33 942 957 19519767 PMC2774760
  131. [137]Stickler DJ Feneley RC The encrustation and blockage of long-term indwelling bladder catheters: a way forward in prevention and control Spinal Cord in press 20368711

Cited by

Sorted by citations

Authors
Kearns, D. B.
Affiliations
Indiana University Bloomington (US)
Corresponding author
Kearns, Daniel B.
Venue
Nature Reviews Microbiology
Published
2010-08-09
Volume
8
Issue
9
Pages
634-644
ISSN
  • 1740-1526 (ISSN-L)
  • 1740-1534
OpenAlex
W1978436399
Cited by
1,483
References
0
Citations by year
2026: 75 · 2025: 109 · 2024: 135 · 2023: 112 · 2022: 142 · 2021: 118 · 2020: 136 · 2019: 121 · 2018: 82 · 2017: 95 · 2016: 87 · 2015: 75 · 2014: 62 · 2013: 57 · 2012: 37
FWCI
3.76
Type
journal article
Language
en
Open access
Locations
  • Nature Reviews Microbiology (publishedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
Funders
National Institute of General Medical Sciences (GM-093030, R01GM093030)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Bacterial biofilms and quorum sensing
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
  • Physical Sciences › Physics and Astronomy › Condensed Matter Physics › Micro and Nano Robotics
Keywords
flagella, flagellar assembly, flagellar rotation, surfactant secretion, surface tension, bacterial motility
MeSH terms
Bacteria, Flagella, Movement, Bacterial Physiological Phenomena

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review