Atomic force microscopy: A powerful tool for studying bacterial swarming motility

Micron

Volumn 43, Issue 12, 2012, Pages 1304-1311

  Gillis, Annika ^a   Dupres, Vincent ^a   Mahillon, Jacques ^a   Dufrêne, Yves F ^a  

^a UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

Author keywords

Atomic force microscopy; Bacterial motility; Flagella; Imaging; Swarming

Indexed keywords

AFM IMAGING; BACILLUS THURINGIENSIS; BACTERIAL MOTILITY; BACTERIAL POPULATION; CELL MORPHOLOGY; CELL SHAPES; FASCINATING PHENOMENA; FAST IMAGING; FLAGELLA; GRAM-POSITIVE BACTERIUM; HIGH RESOLUTION; MOLECULAR MECHANISM; MOTILITY STUDIES; ROD-SHAPED; SOFT AGAR; SOLID SURFACE; SWARMING; SWARMING BEHAVIOR;

ALGAE; ATOMIC FORCE MICROSCOPY; BACTERIA; BACTERIOLOGY; CYTOLOGY; ELECTRON MICROSCOPY; IMAGING TECHNIQUES; POLYSACCHARIDES;

CELLS;

ARTICLE; ATOMIC FORCE MICROSCOPY; BACILLUS THURINGIENSIS; CHEMISTRY; CULTURE MEDIUM; FLAGELLUM; GROWTH, DEVELOPMENT AND AGING; LOCOMOTION; PHYSIOLOGY; ULTRASTRUCTURE;

BACILLUS THURINGIENSIS; CULTURE MEDIA; FLAGELLA; LOCOMOTION; MICROSCOPY, ATOMIC FORCE;

BACILLUS THURINGIENSIS; BACTERIA (MICROORGANISMS); POSIBACTERIA;

EID: 84865813842     PISSN: 09684328     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.micron.2012.01.014     Document Type: Article

References (56)

1. Balaban N.Q., Merrin J., Chait R., Kowalik L., Leiber S. Bacterial persistence as a phenotypic switch. Science 2004, 305:1622-1625.
2. Be'er A., Harshey R.M. Collective motion of surfactant-producing bacteria imparts superdiffusivity to their upper surface. Biophys. J. 2011, 101:1017-1024.
3. Berg H.C. The rotary motor of bacterial flagella. Annu. Rev. Biochem. 2003, 72:19-54.
4. Blair D.F. Flagellar movement driven by proton translocation. FEBS Lett. 2003, 545:86-95.
5. Blair K.M., Turner L., Winkelman J.T., Berg H., Kearns D.B. A molecular clutch disables flagella in the Bacillus subtilis biofilm. Science 2008, 320:1636-1638.
6. Bottone E.J. Bacillus cereus, a volatile human pathogen. Clin. Microbiol. Rev. 2010, 23:382-398.
7. Branda S.S., González-Pastor J.E., Dervyn E., Ehlich D., Losick R., Kolter R. Genes involved in formation of structured multicellular communities by Bacillus subtilis. J. Bacteriol. 2004, 186:3970-3979.
8. Bravo A., Gill S.S., Soberon M. Mode of action of Bacillus thuringiensis Cry and Cyt toxins and their potential for insect control. Toxicon 2007, 49:423-435.
9. Butler M., Wang Q., Harshey R.M. Cell density and mobility protect swarming bacteria against antibiotics. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:3776-3781.
10. 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. 2010, 76:1241-1250.
11. Copeland M.F., Weibel D.B. Bacterial swarming: a model system for studying dynamics self-assembly. Soft Matter. 2009, 5:1174-1187.
12. Deligianni E., Pattison S., Berrar D., Ternan N.G., Haylock R.W., Moore J.E., Elborn S.J., Dooley J.S. Pseudomonas aeruginosa cystic fibrosis isolates of similar RAPD genotype exhibit diversity in biofilm forming ability in vitro. BMC Microbiol. 2010, 10:38.
13. de Maagd R.A., Bravo A., Crickmore N. How Bacillus thuringiensis has evolved specific toxins to colonize the insect world. Trends Gent. 2001, 17:193-199.
14. Fouet A., Mock M. Regulatory networks for virulence and persistence of Bacillus anthracis. Curr. Opin. Microbiol. 2006, 9:160-166.
15. Fraser G.M., Hughes C. Swarming motility. Curr. Opin. Microbiol. 1999, 2:630-635.
16. Ghelardi E., Celandroni F., Salvetti S., Beecher D.J., Gominet M., Lereclus D., Wong A.C.L., Sensi S. Requirement of flhA for swarming differentiation, flagellin export, and secretion of virulence-associated proteins in Bacillus thuringiensis. J. Bacteriol. 2002, 184:6424-6433.
17. Ghelardi E., Celandroni F., Salvetti S., Ceragioli M., Beecher D.J., Senesi S., Wong A.C.L. Swarming behaviour of and hemolysin BL secretion by Bacillus cereus. Appl. Environ. Microbiol. 2007, 73:4089-4093.
18. Gillis, A., Dupres, V., Delestrait, G., Mahillon, J., Dufrêne, Y.F., 2012. Nanoscale imaging of Bacillus thuringiensis flagella using atomic force microscopy. Nanoscale, doi:10.1039/C1NR11161B.
19. Girgis H.S., Liu Y., Ryu W.S., Tavazoie S. A comprehensive genetic characterization of bacterial motility. PLoS Genet. 2007, 3:e154.
20. Harshey R.M. Bees aren't the only ones: swarming in Gram-negative bacteria. Mol. Microbiol. 1994, 13:389-394.
21. Harshey R.M. Bacterial motility on a surface: many ways to a common goal. Annu. Rev. Microbiol. 2003, 57:249-273.
22. Harshey R.M., Matsuyama T. Dimorphic transition in Escherichia coli and Salmonella typhimurium: surface-induced differentiation into hyperflagellate swarmer cells. Proc. Natl. Acad. Sci. U.S.A. 1994, 91:8631-8635.
23. Hayward N.J., Incledon G.M., Spragg J.E. Effect of firm agar on the swarming of Proteus and Clostridium species and on the colonies of clinically important bacteria. J. Med. Microbiol. 1978, 11:155-164.
24. Henrichsen J. Bacterial surface translocation: a survey and a classification. Bacteriol. Rev. 1972, 36:478-503.
25. Höfte H., Whiteley H.R. Insecticidal crystal proteins of Bacillus thuringiensis. Microbiol. Rev. 1989, 53:242-255.
26. Jensen G.B., Hansen B.M., Eilenberg J., Mahillon J. The hidden lifestyles of Bacillus cereus and relatives. Environ. Microbiol. 2003, 5:631-640.
27. Jones B.V., Young R., Mahenthiralingam E., Stickler D.J. Ultrastructure of Proteus mirabilis swarmer cell rafts and role of swarming in catheter-associated unirary tract infection. Infect. Immun. 2004, 72:3941-3950.
28. Julkowska D., Obuchowski M., Holland I.B., Séror S.J. Branched swarming patterns on a synthetic medium formed by wild-type Bacillus subtilis strain 3610: detection of different cellular morphologies and constellations of cells as the complex architecture develops. Microbiology 2004, 150:1839-1849.
29. Kailas L., Terry C., Abbott N., Taylor R., Mullin N., Tzokov S.B., Todd S.J., Wallace B.A., Hobbs J.K., Moir A., Bullough P.A. Surface architecture of endospores of the Bacillus cereus/anthracis/thuringiensis family at the subnanometer scale. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:16014-16019.
30. Kearns D.B. A field guide to bacterial swarming motility. Nat. Rev. Microbiol. 2010, 8:634-644.
31. Kearns D.B., Losick R. Swarming motility in undomesticated Bacillus subtilis. Mol. Microbiol. 2003, 49:581-590.
32. Kearns D.B., Losick R. Cell population heterogeneity during growth of Bacillus subtilis. Genes Dev. 2005, 19:3083-3094.
33. Kobayashi K. Gradual activation of the response regulator DegU controls serial expression of genes for flagellum formation and biofilm in Bacillus subtilis. Mol. Microbiol. 2007, 66:395-409.
34. López D., Kolter R. Extracellular signals that define distinct and coexisting cell fates in Bacillus subtilis. FEMS Microbiol. Rev. 2010, 34:134-149.
35. López D., Vlamakis H., Kolter R. Generation of multiple cell types in Bacillus subtilis. FEMS Microbiol. Rev. 2009, 33:152-163.
36. Macfarlane S., Hopkins M.J., Macfarlane G.T. Toxin synthesis and mucin breakdown are related to swarming phenomenon in Clostridium septicum. Infect. Immun. 2001, 69:1120-1126.
37. Macnab R.M. How bacteria assemble flagella. Annu. Rev. Microbiol. 2003, 57:77-100.
38. McCarter L.L. Regulation of flagella. Curr. Opin. Microbiol. 2006, 9:180-186.
39. Mobley H.L., Belas R. Swarming and pathogenicity of Proteus mirabilis in the urinary tract. Trends Microbiol. 1995, 3:280-284.
40. Müller D.J., Dufrêne Y.F. Force nanoscopy of living cells. Curr. Biol. 2011, 21:R212-R216.
41. Müller D.J., Dufrêne Y.F. Atomic force microscopy: a nanoscopic window on the cell surface. Trends Cell. Biol. 2011, 21:461-469.
42. Ochsner U.A., Reiser J. Autoinducer-mediated regulation of rhamnolipid biosurfactant synthesis in Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. U.S.A. 1995, 92:6424-6428.
43. Overhage J., Bains M., Brazas M., Hancock R.E.W. Swarming of Pseudomonas aeruginosa is a complex adaptation leading to increased production of virulence factors and antibiotic resistance. J. Bacteriol. 2008, 190:2671-2679.
44. Patrick, J.E., Kearns, D.B., 2011. Swarming motility and the control of master regulators of flagellar biosynthesis, Mol. Microbiol., doi:10.1111/j.%201365-2958.2011.07917.x.
45. Senesi S., Celandroni F., Salvetti S., Beecher D.J., Wong A.C.L., Ghelardi E. Swarming motility in Bacillus cereus and characterization of a fliY mutant impaired in swarm cell differentiation. Microbiology 2002, 148:1785-1794.
46. Senesi S., Salvetti S., Celandroni F., Ghelardi E. Features of Bacillus cereus swarm cells. Res. Microbiol. 2010, 161:743-749.
47. Shrout J.D., Chopp D.L., Just C.L., Hentzer M., Givskov M., Parsek M.R. The impact of quorum sensing and swarming motility on Pseudomonas aeruginosa biofilm formation is nutritionally conditional. Mol. Microbiol. 2006, 62:1264-1277.
48. Taylor T.B., Buckling A. Competition and dispersal in Pseudomonas aeruginosa. Am. Nat. 2010, 176:83-89.
49. Turner L., Zhang R., Darnton N.C., Berg H.C. Visualization of flagella during bacterial swarming. J. Bacteriol. 2010, 192:3259-3267.
50. Verhamme D.T., Kiley T.B., Stanley-Wall N.R. DegU co-ordinates multicellular behaviour exhibited by Bacillus subtilis. Mol. Microbiol. 2007, 65:554-568.
51. 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.
52. Vilas-Bôas G.T., Peruca A.P., Arantes O.M. Biology and taxonomy of Bacillus cereus, Bacillus anthracis, and Bacillus thuringiensis. Can. J. Microbiol. 2007, 53:673-687.
53. Vlamakis H., Aguilar C., Losick R., Kolter R. Control of the cell fate by the formation of an architecturally complex bacterial community. Genes Dev. 2008, 22:945-953.
54. Wei Y., Wang X., Liu J., Nememan I., Singh A., Weiss H., Levin B.R. The population dynamics of bacteria in physically structured habitats and the adaptive virtue of random motility. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:4047-4052.
55. Wolfe A.J., Berg H.C. Migration of bacteria in semisolid agar. Proc. Natl. Acad. Sci. U.S.A. 1989, 86:6973-6977.
56. Zhdankin V., Sprott J.C. Simple predator-prey swarming model. Phys. Rev. E. Stat. Nonlin. Soft Matter. Phys. 2010, 82:056209.