Physics of bacterial near-surface motility using flagella and type IV pili: Implications for biofilm formation

Research in Microbiology

Volumn 163, Issue 9-10, 2012, Pages 619-629

  Conrad, Jacinta C ^a  

^a UNIVERSITY OF HOUSTON   (United States)

Author keywords

Bacterial motility; Biofilm formation; Flagella; Type IV pili

Indexed keywords

BACTERIAL PROTEIN; PROTEIN TYPE 4 PILI; UNCLASSIFIED DRUG;

ARTICLE; BACILLUS SUBTILIS; BACTERIAL NEAR SURFACE MOTILITY; BACTERIAL PHENOMENA AND FUNCTIONS; BACTERIUM PILUS; BIOFILM; CAULOBACTER CRESCENTUS; ESCHERICHIA COLI; FLAGELLUM; HYDRODYNAMICS; MYXOCOCCUS XANTHUS; NEISSERIA GONORRHOEAE; NONHUMAN; OPTICAL TWEEZERS; PRIORITY JOURNAL; PROTEIN FUNCTION; PSEUDOMONAS AERUGINOSA; RHODOBACTER SPHAEROIDES; TWITCHING MOTILITY; VIBRIO ALGINOLYTICUS; WILD TYPE; XYLELLA FASTIDIOSA;

BACTERIAL PHYSIOLOGICAL PHENOMENA; BIOFILMS; FIMBRIAE, BACTERIAL; FLAGELLA; LOCOMOTION;

BACTERIA (MICROORGANISMS);

EID: 84870727772     PISSN: 09232508     EISSN: 17697123     Source Type: Journal    
DOI: 10.1016/j.resmic.2012.10.016     Document Type: Article

References (87)

1. Amako K., Umeda A. Flagellation of Pseudomonas aeruginosa during the cell division cycle. Microbiol. Immunol. 1982, 26:113-117.
2. Bahar O., Goffer T., Burdman S. Type IV pili are required for virulence, twitching motility, and biofilm formation of Acidovorax avenae subsp. citrulli. Mol. Plant Microbe Interact. 2009, 22:909-920.
3. Bahar O., De La Fuente L., Burdman S. Assessing adhesion, biofilm formation and motility of Acidovorax citrulli using microfluidic flow chambers. FEMS Microbiol. Lett. 2010, 312:33-39.
4. Barken K.B., Pamp S.J., Yang L., Gjermansen M., Bertrand J.J., Klausen M., Givskov M., Whitchurch C.B., et al. Roles of type IV pili, flagellum-mediated motility and extracellular DNA in the formation of mature multicellular structures in Pseudomonas aeruginosa biofilms. Environ. Microbiol. 2008, 10:2331-2343.
5. Berg H.C., Anderson R.A. Bacteria swim by rotating their flagellar filaments. Nature 1973, 245:380-382.
6. Berg H.C. Bacterial flagellar motor. Curr. Biol. 2008, 18:R689-R691.
7. Berk V., Fong J.C.N., Dempsey G.T., Develioglu O.N., Zhuang X., Liphardt J., Yildiz F.H., Chu S. Molecular architecture and assembly principles of Vibrio cholerae biofilms. Science 2012, 337:236-239.
8. Berke A.P., Turner L., Berg H.C., Lauga E. Hydrodynamic attraction of swimming microorganisms by surfaces. Phys. Rev. Lett. 2008, 101:038102.
9. Biais N., Ladoux B., Higashi D., So M., Sheetz M. Cooperative retraction of bundled type IV pili enables nanonewton force generation. PLoS Biol. 2008, 6(4):e87. 10.1371/journal.pbio.0060087.
10. Burrows L.L. Pseudomonas aeruginosa twitching motility: Type IV pili in action. Annu. Rev. Microbiol. 2012, 66:493-520.
11. Chen X., Berg H.C. Torque-speed relationship of the flagellar rotary motor of Escherichia coli. Biophys. J. 2000, 78:1036-1041.
12. Chen X., Dong X., Be'er A., Swinney H.L., Zhang H.P. Scale-invariant correlations in dynamic bacterial clusters. Phys. Rev. Lett. 2012, 108:148101.
13. Cisneros L.H., Kessler J.O., Ortiz R., Cortez R., Bees M.A. Unexpected bipolar flagellar arrangements and long-range flows driven by bacteria near solid boundaries. Phys. Rev. Lett. 2008, 101:168102.
14. Clausen M., Jakovljevic V., Søgaard-Andersen L., Maier B. High-force generation is a conserved property of type IV pilus systems. J. Bacteriol. 2009, 191:4633-4638.
15. Clausen M., Koomey M., Maier B. Dynamics of type IV pili is controlled by switching between multiple states. Biophys. J. 2009, 96:1169-1177.
16. Conrad J.C., Gibiansky M.L., Jin F., Gordon V.D., Motto D.A., Mathewson M.A., Stopka W.G., Zelasko D.C., et al. Flagella and pili-mediated near-surface single-cell motility mechanisms in P. aeruginosa. Biophys. J. 2011, 100:1608-1616.
17. 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.
18. Cowles K.N., Gitai Z. Surface association and the MreB cytoskeleton regulate pilus production, localization and function in Pseudomonas aeruginosa. Mol. Microbiol. 2010, 76:1411-1426.
19. Darnton N.C., Turner L., Rojevsky S., Berg H.C. On torque and tumbling in swimming Escherichia coli. J. Bacteriol. 2007, 189:1756-1764.
20. de Kerchove A.J., Elimelech M. Bacterial swimming motility enhances cell deposition and surface coverage. Environ. Sci. Technol. 2008, 42:4371-4377.
21. De La Fuente L., Montanes E., Meng Y., Li Y., Burr T.J., Hoch H.C., Wu M. Assessing adhesion forces of type I and type IV pili of Xylella fastidiosa bacteria by use of a microfluidic flow chamber. Appl. Environ. Microbiol. 2007, 73:2690-2696.
22. De La Fuente L., Burr T.J., Hoch H.C. Autoaggregation of Xylella fastidiosa cells is influenced by type I and type IV pili. Appl. Environ. Microbiol. 2008, 74:5579-5582.
23. Díaz C., Schilardi P.L., Salvarezza R.C., Fernández Lorenzo de Mele M. Nano/microscale order affects the early stages of biofilm formation on metal surfaces. Langmuir 2007, 23:11206-11210.
24. Díaz C., Schilardi P.L., dos Santos Claro P.C., Salvarezza R.C., Fernández Lorenzo de Mele M.A. Submicron trenches reduce the Pseudomonas fluorescens colonization rate on solid surfaces. ACS Appl. Mater. Interfaces 2009, 1:136-143.
25. Díaz C., Schilardi P.L., Salvarezza R.C., Fernández Lorenzo de Mele M.A. Have flagella a preferred orientation during early stages of biofilm formation?: AFM study using patterned substrates. Colloids Surf. B Biointerfaces 2011, 82:536-542.
26. DiLuzio W.R., Turner L., Mayer M., Garstecki P., Weibel D.B., Berg H.C., Whitesides G.M. Escherichia coli swim on the right-hand side. Nature 2005, 435:1271-1274.
27. Donlan R. Biofilms and device-associated infections. Emerg. Infect. Dis. 2001, 7:277-281.
28. Du H., Xu Z., Anyan M., Kim O., Leevy W.M., Shrout J.D., Alber M. High density waves of the bacterium Pseudomonas aeruginosa in propagating swarms result in efficient colonization of surfaces. Biophys. J. 2012, 103:601-609.
29. Frymier P.D., Ford R.M., Berg H.C., Cummings P.T. Three-dimensional tracking of motile bacteria near a solid planar surface. Proc. Natl. Acad. Sci. U.S.A. 1995, 92:6195-6199.
30. Fu H.C., Wolgemuth C.W., Powers T.R. Swimming speeds of filaments in nonlinearly viscoelastic fluids. Phys. Fluids 2009, 21:033102.
31. Geoghegan M., Andrews J.S., Biggs C.A., Eboigbodin K.E., Elliott D.R., Rolfe S., Scholes J., Ojeda J.J., et al. The polymer physics and chemistry of microbial cell attachment and adhesion. Faraday Discuss. 2008, 139:85-103.
32. Gibiansky M.L., Conrad J.C., Jin F., Gordon V.D., Motto D.A., Mathewson M.A., Stopka W.G., Zelasko D.C., et al. Bacteria use type IV pili to walk upright and detach from surfaces. Science 2010, 330:197.
33. Gómez-Suárez C., Pasma J., van der Borden A., Wingender J., Flemming H.-C., Busscher H.J., van der Mei H.C. Influence of extracellular polymeric substances on deposition and redeposition of Pseudomonas aeruginosa to surfaces. Microbiology 2002, 148:1161-1169.
34. Guasto J.S., Rusconi R., Stocker R. Fluid mechanics of planktonic microorganisms. Annu. Rev. Fluid Mech. 2012, 44:373-400.
35. Hall-Stoodley L., Costerton J.W., Stoodley P. Bacterial biofilms: from the natural environment to infectious diseases. Nat. Rev. Microbiol. 2004, 2:95-108.
36. Hernandez-Ortiz J.P., Stoltz C.G., Graham M.D. Transport and collective dynamics in suspensions of confined swimming particles. Phys. Rev. Lett. 2005, 95:204501.
37. Hernandez-Ortiz J.P., Underhill P.T., Graham M.D. Dynamics of confined suspensions of swimming particles. J. Phys. Condens. Matter 2009, 21:204107.
38. Hill J., Kalkanci O., Mcmurry J.L., Koser H. Hydrodynamic surface interactions enable Escherichia coli to seek efficient routes to swim upstream. Phys. Rev. Lett. 2007, 98:068101.
39. Hochbaum A.I., Aizenberg J. Bacteria pattern spontaneously on periodic nanostructure arrays. Nano Lett. 2010, 10:3717-3721.
40. Holz C., Opitz D., Mehlich J., Ravoo B.J., Maier B. Bacterial motility and clustering guided by microcontact printing. Nano Lett. 2009, 9:4553-4557.
41. Holz C., Opitz D., Greune L., Kurre R., Koomey M., Schmidt M.A., Maier B. Multiple pilus motors cooperate for persistent bacterial movement in two dimensions. Phys. Rev. Lett. 2010, 104:178104.
42. Hunter P.R., Colford J.M., LeChavellier M.W., Binder S., Berger P.S. Waterborne diseases. Emerg. Infect. Dis. 2001, 7:544-545.
43. Jin F., Conrad J.C., Gibiansky M.L., Wong G.C.L. Bacteria use type-IV pili to slingshot on surfaces. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:12617-12622.
44. Kaya T., Koser H. Characterization of hydrodynamic surface interactions of Escherichia coli cell bodies in shear flow. Phys. Rev. Lett. 2009, 103:138103.
45. Kaya T., Koser H. Direct upstream motility in Escherichia coli. Biophys. J. 2012, 102:1514-1523.
46. Klausen M., Aaes-Jørgensen A., Molin S., Tolker-Nielsen T. Involvement of bacterial migration in the development of complex multicellular structures in Pseudomonas aeruginosa biofilms. Mol. Microbiol. 2003, 50:61-68.
47. Klausen M., Heydorn A., Ragas P., Lambertsen L., Aaes-Jørgensen A., Molin S., Tolker-Nielsen T. Biofilm formation by Pseudomonas aeruginosa wild type, flagella and type IV pili mutants. Mol. Microbiol. 2003, 48:1511-1524.
48. Klausen M., Gjermansen M., Kreft J.U., Tolker-Nielsen T. Dynamics of development and dispersal in sessile microbial communities: examples from Pseudomonas aeruginosa and Pseudomonas putida model biofilms. FEMS Microbiol. Lett. 2006, 261:1-11.
49. Kudo S., Imai N., Nishitoba M., Sugiyama S., Magariyama Y. Asymmetric swimming pattern of Vibrio alginolyticus cells with single polar flagella. FEMS Microbiol. Lett. 2005, 242:221-225.
50. Lauga E., Powers T.R. The hydrodynamics of swimming microorganisms. Rep. Prog. Phys. 2009, 72:096601.
51. Lauga E., DiLuzio W.R., Whitesides G.M., Stone H.A. Swimming in circles: motion of bacteria near solid boundaries. Biophys. J. 2006, 90:400-412.
52. Lauga E. Life around the scallop theorem. Soft Matter 2011, 7:3060-3065.
53. Lecuyer S., Rusconi R., Shen Y., Forsyth A.M., Vlamakis H., Kolter R., Stone H.A. Shear stress increases the residence time of adhesion of Pseudomonas aeruginosa. Biophys. J. 2011, 100:341-350.
54. Li G., Tang J.X. Accumulation of microswimmers near a surface mediated by collision and rotational Brownian motion. Phys. Rev. Lett. 2009, 103:078101.
55. Li Y., Sun H., Ma X., Lu A., Lux R., Zusman D., Shi W. Extracellular polysaccharides mediate pilus retraction during social motility of Myxococcus xanthus. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:5443-5448.
56. Li G., Tam L.-K., Tang J.X. Amplified effect of Brownian motion in bacterial near-surface swimming. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:18355-18359.
57. Li G., Bensson J., Nisimova L., Munger D., Mahautmr P., Tang J.X., Maxey M.R., Brun Y.V. Accumulation of swimming bacteria near a solid surface. Phys. Rev. E 2011, 84:041932.
58. Li G., Brown P.J., Tang J.X., Xu J., Quardokus E.M., Fuqua C., Brun Y.V. Surface contact stimulates the just-in-time deployment of bacterial adhesins. Mol. Microbiol. 2012, 83:41-51.
59. Maennik J., Driessen R., Galajda P., Keymer J.E., Dekker C. Bacterial growth and motility in sub-micron constrictions. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:14861-14866.
60. Magariyama Y., Sugiyama S., Muramoto K., Kawagishi I., Imae Y., Kudo S. Simultaneous measurement of bacterial flagellar rotation rate and swimming speed. Biophys. J. 1995, 69:2154-2162.
61. Magariyama Y., Ichiba M., Nakata K., Baba K., Ohtani T., Kudo S., Goto T. Difference in bacterial motion between forward and backward swimming caused by the wall effect. Biophys. J. 2008, 88:3648-3658.
62. Maier B., Potter L., So M., Seifert H., Sheetz M.P. Single pilus motor forces exceed 100 pN. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:16012-16017.
63. Marcos, Fu H.C., Powers T.R., Stocker R. Separation of microscale chiral objects by shear flow. Phys. Rev. Lett. 2009, 102:158103.
64. Marcos, Fu H.C., Powers T.R., Stocker R. Bacterial rheotaxis. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:4780-4785.
65. Meel C., Kouzel N., Oldewurtel E.R., Maier B. Three-dimensional obstacles for bacterial surface motility. Small 2012, 8:530-534.
66. Meng Y., Li Y., Galvani C.D., Hao G., Turner J.N., Burr T.J., Hoch H.C. Upstream migration of Xylella fastidiosa via pilus-driven twitching motility. J. Bacteriol. 2005, 187:5560-5567.
67. Merz A.J., So M., Sheetz M.P. Pilus retraction powers bacterial twitching motility. Nature 2000, 407:98-102.
68. Monds R.D., O'Toole G.A. The developmental model of microbial biofilms: ten years of a paradigm up for review. Trends Microbiol. 2009, 17:73-87.
69. Neuman K.C., Chadd E.H., Liou G.F., Bergman K., Block S.M. Characterization of photodamage to Escherichia coli in optical traps. Biophys. J. 1999, 77:2856-2863.
70. O'Toole G.A., Kolter R. Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol. Microbiol. 1998, 30:295-304.
71. Petrova O.E., Sauer K. Sticky situations: key components that control bacterial surface attachment. J. Bacteriol. 2012, 194:2413-2425.
72. Purcell E.M. Life at low Reynolds number. Am. J. Phys. 1977, 45:3-11.
73. Sauer K., Camper A.K., Ehrlich G.D., Costerton J.W., Davies D.G. Pseudomonas aeruginosa displays multiple phenotypes during development as a biofilm. J. Bacteriol. 2002, 184:1140-1154.
74. Schultz M.P., Swain G.W. The influence of biofilms on skin friction drag. Biofouling 2000, 15:129-139.
75. Schwarz-Linek J., Dorken G., Winkler A., Wilson L.G., Pham N.T., French C.E., Schilling T., Poon W.C.K. Polymer-induced phase separation in suspensions of bacteria. Europhys. Lett. 2010, 89:68003.
76. Schwarz-Linek J., Winkler A., Wilson L.G., Pham N.T., Schilling T., Poon W.C.K. Polymer-induced phase separation in Escherichia coli suspensions. Soft Matter 2010, 6:4540-4549.
77. Shen Y., Siryaporn A., Lecuyer S., Gitai Z., Stone Howard A. Flow directs surface-attached bacteria to twitch upstream. Biophys. J. 2012, 103:146-151.
78. Skerker J.M., Berg H.C. Direct observation of extension and retraction of type IV pili. Proc. Natl. Acad. Sci. U.S.A. 2001, 98:6901-6904.
79. Sun H., Zusman D.R., Shi W. Type IV pilus of Myxococcus xanthus is a motility apparatus controlled by the frz chemosensory system. Curr. Biol. 2000, 10:1143-1146.
80. Toutain C.M., Caizza N.C., Zegans M.E., O'Toole G.A. Roles for flagellar stators in biofilm formation by Pseudomonas aeruginosa. Res. Microbiol. 2007, 158:471-477.
81. Tran V.B., Fleiszig S.M.J., Evans D.J., Radke C.J. Dynamics of flagellum- and pilus-mediated association of Pseudomonas aeruginosa with contact lens surfaces. Appl. Environ. Microbiol. 2011, 77:3644-3652.
82. Turner L., Ryu W.S., Berg H.C. Real-time imaging of fluorescent flagellar filaments. J. Bacteriol. 2000, 182:2793-2801.
83. Turner L., Zhang R., Darnton N.C., Berg H.C. Visualization of flagella during bacterial swarming. J. Bacteriol. 2010, 192:3259-3267.
84. Weibel D.B., DiLuzio W.R., Whitesides G.M. Microfabrication meets microbiology. Nat. Rev. Microbiol. 2007, 5:209-218.
85. Wood T.K., González Barrios A.F., Herzberg M., Lee J. Motility influences biofilm architecture in Escherichia coli. Appl. Microbiol. Biotechnol. 2006, 72:361-367.
86. Wu Y., Jiang Y., Kaiser A.D., Alber M. Self-organization in bacterial swarming: lessons from myxobacteria. Phys. Biol. 2011, 8:055003.
87. Zhang H.P., Be'er A., Florin E.-L., Swinney H.L. Collective motion and density fluctuations in bacterial colonies. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:13626-13630.