The mechanical world of bacteria

Cell

Volumn 161, Issue 5, 2015, Pages 988-997

  Persat, Alexandre ^a   Nadell, Carey D ^a,b   Kim, Minyoung Kevin ^a   Ingremeau, Francois ^c   Siryaporn, Albert ^a   Drescher, Knut ^b   Wingreen, Ned S ^a   Bassler, Bonnie L ^a,d   Gitai, Zemer ^a   Stone, Howard A ^c  

^a PRINCETON UNIVERSITY   (United States)

^b MAX PLANCK INSTITUTE FOR TERRESTRIAL MICROBIOLOGY   (Germany)

^c Princeton University   (United States)

^d HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BACTERIAL CELL; BACTERIUM; BIOFILM; CELL ADHESION; CELL DIVISION; CELL MOTILITY; CELL SHAPE; CELL WALL; FLOW KINETICS; FLOW RATE; FLUID FLOW; MECHANICAL STRESS; MECHANICS; MICROBIAL COMMUNITY; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; QUORUM SENSING; SHEAR STRESS; SURFACE AREA; SURFACE PROPERTY; TWITCHING MOTILITY; VISCOSITY; BACTERIUM ADHERENCE; BIOMECHANICS; CYTOLOGY; ESCHERICHIA COLI; LOCOMOTION; PHYSIOLOGY; PSEUDOMONAS AERUGINOSA; TRANSPORT AT THE CELLULAR LEVEL;

BACTERIA (MICROORGANISMS);

BACTERIAL ADHESION; BIOFILMS; BIOLOGICAL TRANSPORT; BIOMECHANICAL PHENOMENA; ESCHERICHIA COLI; LOCOMOTION; PSEUDOMONAS AERUGINOSA;

EID: 84930225961     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2015.05.005     Document Type: Review

References (93)

1. M. Asally, M. Kittisopikul, P. Rué, Y. Du, Z. Hu, T. Çaʇatay, A.B. Robinson, H. Lu, J. Garcia-Ojalvo, and G.M. Süel Localized cell death focuses mechanical forces during 3D patterning in a biofilm Proc. Natl. Acad. Sci. USA 109 2012 18891 18896
2. D.P. Bakker, B.R. Postmus, H.J. Busscher, and H.C. van der Mei Bacterial strains isolated from different niches can exhibit different patterns of adhesion to substrata Appl. Environ. Microbiol. 70 2004 3758 3760
3. R. Belas Biofilms, flagella, and mechanosensing of surfaces by bacteria Trends Microbiol. 22 2014 517 527
4. H.C. Berg Random Walks in Biology, Expanded Edition 1993 Princeton University Press
5. H.C. Berg The rotary motor of bacterial flagella Annu. Rev. Biochem. 72 2003 19 54
6. H.C. Berg, and E.M. Purcell Physics of chemoreception Biophys. J. 20 1977 193 219
7. V. Berk, J.C. Fong, G.T. Dempsey, O.N. Develioglu, X. Zhuang, J. Liphardt, F.H. Yildiz, and S. Chu Molecular architecture and assembly principles of Vibrio cholerae biofilms Science 337 2012 236 239
8. K.M. Blair, L. Turner, J.T. Winkelman, H.C. Berg, and D.B. Kearns A molecular clutch disables flagella in the Bacillus subtilis biofilm Science 320 2008 1636 1638
9. L.L. Burrows Pseudomonas aeruginosa twitching motility: type IV pili in action Annu. Rev. Microbiol. 66 2012 493 520
10. S.C. Chew, B. Kundukad, T. Seviour, J.R. van der Maarel, L. Yang, S.A. Rice, P. Doyle, and S. Kjelleberg Dynamic remodeling of microbial biofilms by functionally distinct exopolysaccharides mBio 5 2014 e01536-01514
11. J.C. Comolli, A.R. Hauser, L. Waite, C.B. Whitchurch, J.S. Mattick, and J.N. Engel Pseudomonas aeruginosa gene products PilT and PilU are required for cytotoxicity in vitro and virulence in a mouse model of acute pneumonia Infect. Immun. 67 1999 3625 3630
12. D.M. Cornforth, R. Popat, L. McNally, J. Gurney, T.C. Scott-Phillips, A. Ivens, S.P. Diggle, and S.P. Brown Combinatorial quorum sensing allows bacteria to resolve their social and physical environment Proc. Natl. Acad. Sci. USA 111 2014 4280 4284
13. J.W. Costerton, Z. Lewandowski, D.E. Caldwell, D.R. Korber, and H.M. Lappin-Scott Microbial biofilms Annu. Rev. Microbiol. 49 1995 711 745
14. D. de Beer, P. Stoodley, and Z. Lewandowski Liquid flow in heterogeneous biofilms Biotechnol. Bioeng. 44 1994 636 641
15. T.R. De Kievit, R. Gillis, S. Marx, C. Brown, and B.H. Iglewski Quorum-sensing genes in Pseudomonas aeruginosa biofilms: their role and expression patterns Appl. Environ. Microbiol. 67 2001 1865 1873
16. L. De La Fuente, E. Montanes, Y. Meng, Y. Li, T.J. Burr, H.C. Hoch, and M. Wu Assessing adhesion forces of type I and type IV pili of Xylella fastidiosa bacteria by use of a microfluidic flow chamber Appl. Environ. Microbiol. 73 2007 2690 2696
17. K. Drescher, Y. Shen, B.L. Bassler, and H.A. Stone Biofilm streamers cause catastrophic disruption of flow with consequences for environmental and medical systems Proc. Natl. Acad. Sci. USA 110 2013 4345 4350
18. K. Drescher, C.D. Nadell, H.A. Stone, N.S. Wingreen, and B.L. Bassler Solutions to the public goods dilemma in bacterial biofilms Curr. Biol. 24 2014 50 55
19. W.W. Driscoll, and J.W. Pepper Theory for the evolution of diffusible external goods Evolution 64 2010 2682 2687
20. W.M. Dunne Jr. Bacterial adhesion: seen any good biofilms lately? Clin. Microbiol. Rev. 15 2002 155 166
21. H.C. Flemming, and J. Wingender The biofilm matrix Nat. Rev. Microbiol. 8 2010 623 633
22. S.P. Fritton, and S. Weinbaum Fluid and solute transport in bone: flow-induced mechanotransduction Annu. Rev. Fluid Mech. 41 2009 347 374
23. T.R. Garrett, M. Bhakoo, and Z. Zhang Bacterial adhesion and biofilms on surfaces Prog. Nat. Sci. 18 2008 1049 1056
24. M.L. Gibiansky, J.C. Conrad, F. Jin, V.D. Gordon, D.A. Motto, M.A. Mathewson, W.G. Stopka, D.C. Zelasko, J.D. Shrout, and G.C. Wong Bacteria use type IV pili to walk upright and detach from surfaces Science 330 2010 197
25. A.J. Goldman, R.G. Cox, and H. Brenner Slow Viscous motion of a sphere parallel to a plane wall. i. motion through a quiescent fluid Chem. Eng. Sci. 22 1967 637
26. J.S. Guasto, R. Rusconi, and R. Stocker Fluid mechanics of planktonic microorganisms Annu. Rev. Fluid Mech. 44 2012 373 400
27. S.B. Guttenplan, K.M. Blair, and D.B. Kearns The EpsE flagellar clutch is bifunctional and synergizes with EPS biosynthesis to promote Bacillus subtilis biofilm formation PLoS Genet. 6 2010 e1001243
28. L. Hall-Stoodley, J.W. Costerton, and P. Stoodley Bacterial biofilms: from the natural environment to infectious diseases Nat. Rev. Microbiol. 2 2004 95 108
29. R.M. Harshey Bacterial motility on a surface: many ways to a common goal Annu. Rev. Microbiol. 57 2003 249 273
30. B.D. Hoffman, C. Grashoff, and M.A. Schwartz Dynamic molecular processes mediate cellular mechanotransduction Nature 475 2011 316 323
31. C.P. Kempes, C. Okegbe, Z. Mears-Clarke, M.J. Follows, and L.E. Dietrich Morphological optimization for access to dual oxidants in biofilms Proc. Natl. Acad. Sci. USA 111 2014 208 213
32. M.K. Kim, K. Drescher, O.S. Pak, B.L. Bassler, and H.A. Stone Filaments in curved streamlines: Rapid formation of Staphylococcus aureus biofilm streamers New J. Phys. 16 2014 065024
33. V. Kostenko, M.M. Salek, P. Sattari, and R.J. Martinuzzi Staphylococcus aureus biofilm formation and tolerance to antibiotics in response to oscillatory shear stresses of physiological levels FEMS Immunol. Med. Microbiol. 59 2010 421 431
34. P.V. Krasteva, J.C. Fong, N.J. Shikuma, S. Beyhan, M.V. Navarro, F.H. Yildiz, and H. Sondermann Vibrio cholerae VpsT regulates matrix production and motility by directly sensing cyclic di-GMP Science 327 2010 866 868
35. I. Le Trong, P. Aprikian, B.A. Kidd, M. Forero-Shelton, V. Tchesnokova, P. Rajagopal, V. Rodriguez, G. Interlandi, R. Klevit, and V. Vogel Structural basis for mechanical force regulation of the adhesin FimH via finger trap-like beta sheet twisting Cell 141 2010 645 655
36. S. Lecuyer, R. Rusconi, Y. Shen, A. Forsyth, H. Vlamakis, R. Kolter, and H.A. Stone Shear stress increases the residence time of adhesion of Pseudomonas aeruginosa Biophys. J. 100 2011 341 350
37. P.P. Lele, B.G. Hosu, and H.C. Berg Dynamics of mechanosensing in the bacterial flagellar motor Proc. Natl. Acad. Sci. USA 110 2013 11839 11844
38. G. Li, P.J. Brown, J.X. Tang, J. Xu, E.M. Quardokus, C. Fuqua, and Y.V. Brun Surface contact stimulates the just-in-time deployment of bacterial adhesins Mol. Microbiol. 83 2012 41 51
39. J.A. Lichter, M.T. Thompson, M. Delgadillo, T. Nishikawa, M.F. Rubner, and K.J. Van Vliet Substrata mechanical stiffness can regulate adhesion of viable bacteria Biomacromolecules 9 2008 1571 1578
40. Y. Liu, and J.-H. Tay The essential role of hydrodynamic shear force in the formation of biofilm and granular sludge Water Res. 36 2002 1653 1665
41. R.M. Macnab How bacteria assemble flagella Annu. Rev. Microbiol. 57 2003 77 100
42. J.S. Mattick Type IV pili and twitching motility Annu. Rev. Microbiol. 56 2002 289 314
43. D. McDougald, S.A. Rice, N. Barraud, P.D. Steinberg, and S. Kjelleberg Should we stay or should we go: mechanisms and ecological consequences for biofilm dispersal Nat. Rev. Microbiol. 10 2012 39 50
44. Y. Meng, Y. Li, C.D. Galvani, G. Hao, J.N. Turner, T.J. Burr, and H.C. Hoch Upstream migration of Xylella fastidiosa via pilus-driven twitching motility J. Bacteriol. 187 2005 5560 5567
45. M.B. Miller, and B.L. Bassler Quorum sensing in bacteria Annu. Rev. Microbiol. 55 2001 165 199
46. Y.A. Millet, D. Alvarez, S. Ringgaard, U.H. von Andrian, B.M. Davis, and M.K. Waldor Insights into Vibrio cholerae intestinal colonization from monitoring fluorescently labeled bacteria PLoS Pathog. 10 2014 e1004405
47. S. Mitri, and K.R. Foster The genotypic view of social interactions in microbial communities Annu. Rev. Genet. 47 2013 247 273
48. C.D. Nadell, and B.L. Bassler A fitness trade-off between local competition and dispersal in Vibrio cholerae biofilms Proc. Natl. Acad. Sci. USA 108 2011 14181 14185
49. C.D. Nadell, K. Drescher, N.S. Wingreen, and B.L. Bassler Extracellular matrix structure governs invasion resistance in bacterial biofilms ISME J. 2015 10.1038/ismej.2014.246 Published online January 20, 2015
50. L.M. Nilsson, W.E. Thomas, E. Trintchina, V. Vogel, and E.V. Sokurenko Catch bond-mediated adhesion without a shear threshold: trimannose versus monomannose interactions with the FimH adhesin of Escherichia coli J. Biol. Chem. 281 2006 16656 16663
51. G. O'Toole, H.B. Kaplan, and R. Kolter Biofilm formation as microbial development Annu. Rev. Microbiol. 54 2000 49 79
52. F.J. Odling-Smee, K.N. Laland, and M.W. Feldman Niche construction Am. Nat. 147 1996 641 648
53. K.I. Pappelbaum, C. Gorzelanny, S. Grässle, J. Suckau, M.W. Laschke, M. Bischoff, C. Bauer, M. Schorpp-Kistner, C. Weidenmaier, and R. Schneppenheim Ultralarge von Willebrand factor fibers mediate luminal Staphylococcus aureus adhesion to an intact endothelial cell layer under shear stress Circulation 128 2013 50 59
54. J.D. Parry Protozoan grazing of freshwater biofilms Adv. Appl. Microbiol. 54 2004 167 196
55. A. Persat, H.A. Stone, and Z. Gitai The curved shape of Caulobacter crescentus enhances surface colonization in flow Nat. Commun. 5 2014 3824
56. R. Phillips, T. Ursell, P. Wiggins, and P. Sens Emerging roles for lipids in shaping membrane-protein function Nature 459 2009 379 385
57. B.L. Pruitt, A.R. Dunn, W.I. Weis, and W.J. Nelson Mechano-transduction: from molecules to tissues PLoS Biol. 12 2014 e1001996
58. E.M. Purcell Life at low Reynolds-number Am. J. Phys. 45 1977 3 11
59. B. Purevdorj, J.W. Costerton, and P. Stoodley Influence of hydrodynamics and cell signaling on the structure and behavior of Pseudomonas aeruginosa biofilms Appl. Environ. Microbiol. 68 2002 4457 4464
60. D.E. Rangel, N. Marín-Medina, J.E. Castro, A. González-Mancera, and M. Forero-Shelton Observation of bacterial type I pili extension and contraction under fluid flow PLoS ONE 8 2013 e65563
61. S.S. Rogers, C. van der Walle, and T.A. Waigh Microrheology of bacterial biofilms in vitro: Staphylococcus aureus and Pseudomonas aeruginosa Langmuir 24 2008 13549 13555
62. R. Rusconi, S. Lecuyer, L. Guglielmini, and H.A. Stone Laminar flow around corners triggers the formation of biofilm streamers J. R. Soc. Interface 7 2010 1293 1299
63. R. Rusconi, S. Lecuyer, N. Autrusson, L. Guglielmini, and H.A. Stone Secondary flow as a mechanism for the formation of biofilm streamers Biophys. J. 100 2011 1392 1399
64. R. Rusconi, M. Garren, and R. Stocker Microfluidics expanding the frontiers of microbial ecology Annu. Rev. Biophys. 43 2014 65 91
65. Y. Shen, A. Siryaporn, S. Lecuyer, Z. Gitai, and H.A. Stone Flow directs surface-attached bacteria to twitch upstream Biophys. J. 103 2012 146 151
66. A. Siryaporn, S.L. Kuchma, G.A. O'Toole, and Z. Gitai Surface attachment induces Pseudomonas aeruginosa virulence Proc. Natl. Acad. Sci. USA 111 2014 16860 16865
67. A. Siryaporn, M.K. Kim, Y. Shen, H.A. Stone, and Z. Gitai Colonization, competition, and dispersal of pathogens in fluid flow networks Curr. Biol. 25 2015 1201 1207
68. J.M. Skerker, and H.C. Berg Direct observation of extension and retraction of type IV pili Proc. Natl. Acad. Sci. USA 98 2001 6901 6904
69. T.M. Squires, R.J. Messinger, and S.R. Manalis Making it stick: convection, reaction and diffusion in surface-based biosensors Nat. Biotechnol. 26 2008 417 426
70. P.S. Stewart Diffusion in biofilms J. Bacteriol. 185 2003 1485 1491
71. P.S. Stewart Mini-review: convection around biofilms Biofouling 28 2012 187 198
72. P.S. Stewart, and M.J. Franklin Physiological heterogeneity in biofilms Nat. Rev. Microbiol. 6 2008 199 210
73. P. Stoodley, Z. Lewandowski, J.D. Boyle, and H.M. Lappin-Scott Structural deformation of bacterial biofilms caused by short-term fluctuations in fluid shear: an in situ investigation of biofilm rheology Biotechnol. Bioeng. 65 1999 83 92
74. P. Stoodley, R. Cargo, C.J. Rupp, S. Wilson, and I. Klapper Biofilm material properties as related to shear-induced deformation and detachment phenomena J. Ind. Microbiol. Biotechnol. 29 2002 361 367
75. L.K. Sycuro, T.J. Wyckoff, J. Biboy, P. Born, Z. Pincus, W. Vollmer, and N.R. Salama Multiple peptidoglycan modification networks modulate Helicobacter pylori's cell shape, motility, and colonization potential PLoS Pathog. 8 2012 e1002603
76. V. Tchesnokova, A.L. McVeigh, B. Kidd, O. Yakovenko, W.E. Thomas, E.V. Sokurenko, and S.J. Savarino Shear-enhanced binding of intestinal colonization factor antigen I of enterotoxigenic Escherichia coli Mol. Microbiol. 76 2010 489 502
77. W. Thomas Catch bonds in adhesion Annu. Rev. Biomed. Eng. 10 2008 39 57
78. W.E. Thomas, L.M. Nilsson, M. Forero, E.V. Sokurenko, and V. Vogel Shear-dependent 'stick-and-roll' adhesion of type 1 fimbriated Escherichia coli Mol. Microbiol. 53 2004 1545 1557
79. W.E. Thomas, V. Vogel, and E. Sokurenko Biophysics of catch bonds Annu. Rev. Biophys. 37 2008 399 416
80. M. Trejo, C. Douarche, V. Bailleux, C. Poulard, S. Mariot, C. Regeard, and E. Raspaud Elasticity and wrinkled morphology of Bacillus subtilis pellicles Proc. Natl. Acad. Sci. USA 110 2013 2011 2016
81. P.H. Tsang, G. Li, Y.V. Brun, L.B. Freund, and J.X. Tang Adhesion of single bacterial cells in the micronewton range Proc. Natl. Acad. Sci. USA 103 2006 5764 5768
82. A. Typas, M. Banzhaf, C.A. Gross, and W. Vollmer From the regulation of peptidoglycan synthesis to bacterial growth and morphology Nat. Rev. Microbiol. 10 2012 123 136
83. J. van Gestel, F.J. Weissing, O.P. Kuipers, and A.T. Kovács Density of founder cells affects spatial pattern formation and cooperation in Bacillus subtilis biofilms ISME J. 8 2014 2069 2079
84. V. Vogel, and M. Sheetz Local force and geometry sensing regulate cell functions Nat. Rev. Mol. Cell Biol. 7 2006 265 275
85. W.M. Weaver, S. Dharmaraja, V. Milisavljevic, and D. Di Carlo The effects of shear stress on isolated receptor-ligand interactions of Staphylococcus epidermidis and human plasma fibrinogen using molecularly patterned microfluidics Lab Chip 11 2011 883 889
86. S.A. West, A.S. Griffin, A. Gardner, and S.P. Diggle Social evolution theory for microorganisms Nat. Rev. Microbiol. 4 2006 597 607
87. M.J. Whitfield, J.P. Luo, and W.E. Thomas Yielding elastic tethers stabilize robust cell adhesion PLoS Comput. Biol. 10 2014 e1003971
88. J.N. Wilking, T.E. Angelini, A. Seminara, M.P. Brenner, and D.A. Weitz Biofilms as complex fluids MRS Bull. 36 2011 385 391
89. J.N. Wilking, V. Zaburdaev, M. De Volder, R. Losick, M.P. Brenner, and D.A. Weitz Liquid transport facilitated by channels in Bacillus subtilis biofilms Proc. Natl. Acad. Sci. USA 110 2013 848 852
90. M. Wloka, H. Rehage, H.C. Flemming, and J. Wingender Rheological properties of viscoelastic biofilm extracellular polymeric substances and comparison to the behavior of calcium alginate gels Colloid Polym. Sci. 282 2004 1067 1076
91. K.D. Xu, P.S. Stewart, F. Xia, C.T. Huang, and G.A. McFeters Spatial physiological heterogeneity in Pseudomonas aeruginosa biofilm is determined by oxygen availability Appl. Environ. Microbiol. 64 1998 4035 4039
92. K.D. Young The selective value of bacterial shape Microbiol. Mol. Biol. Rev. 70 2006 660 703
93. K. Zhao, B.S. Tseng, B. Beckerman, F. Jin, M.L. Gibiansky, J.J. Harrison, E. Luijten, M.R. Parsek, and G.C. Wong Psl trails guide exploration and microcolony formation in Pseudomonas aeruginosa biofilms Nature 497 2013 388 391