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Annual Review of Chemical and Biomolecular Engineering

Volume 9, 2018

Confined Flow: Consequences and Implications for Bacteria and Biofilms

Abstract

Bacteria overwhelmingly live in geometrically confined habitats that feature small pores or cavities, narrow channels, or nearby interfaces. Fluid flows through these confined habitats are ubiquitous in both natural and artificial environments colonized by bacteria. Moreover, these flows occur on time and length scales comparable to those associated with motility of bacteria and with the formation and growth of biofilms, which are surface-associated communities that house the vast majority of bacteria to protect them from host and environmental stresses. This review describes the emerging understanding of how flow near surfaces and within channels and pores alters physical processes that control how bacteria disperse, attach to surfaces, and form biofilms. This understanding will inform the development and deployment of technologies for drug delivery, water treatment, and antifouling coatings and guide the structuring of bacterial consortia for production of chemicals and pharmaceuticals.

Keyword(s): biofilm mechanics, mass transport, quorum sensing, surface attachment, swimming, twitching
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/content/journals/10.1146/annurev-chembioeng-060817-084006
2018-06-07
2024-04-26
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Literature Cited

  1. 1.  Baeshen NA, Baeshen MN, Sheikh A, Bora RS, Ahmed MMM et al. 2014. Cell factories for insulin production. Microb. Cell Fact. 13:141
     [Google Scholar]
  2. 2.  Sanchez-Garcia L, Martín L, Mangues R, Ferrer-Miralles N, Vázquez E, Villaverde A 2016. Recombinant pharmaceuticals from microbial cells: a 2015 update. Microb. Cell Fact. 15:33
     [Google Scholar]
  3. 3.  Hammes F, Egli T 2010. Cytometric methods for measuring bacteria in water: advantages, pitfalls and applications. Anal. Bioanal. Chem. 397:1083–95
     [Google Scholar]
  4. 4.  Hegab HM, ElMekawy A, Stakenborg T 2013. Review of microfluidic microbioreactor technology for high-throughput submerged microbiological cultivation. Biomicrofluidics 7:1–14
     [Google Scholar]
  5. 5.  Tuson HH, Weibel DB 2013. Bacteria-surface interactions. Soft Matter 9:4368–80
     [Google Scholar]
  6. 6.  Fernandes R, Zuniga M, Sassine FR, Karakoy M, Gracias DH 2011. Enabling cargo-carrying bacteria via surface attachment and triggered release. Small 7:588–92
     [Google Scholar]
  7. 7.  Rozhok S, Shen CF, Littler PL, Fan Z, Liu C et al. 2005. Methods for fabricating microarrays of motile bacteria. Small 1:445–51
     [Google Scholar]
  8. 8.  Hochbaum AI, Aizenberg J 2010. Bacteria pattern spontaneously on periodic nanostructure arrays. Nano Lett 10:3717–21
     [Google Scholar]
  9. 9.  Mee MT, Wang HH 2012. Engineering ecosystems and synthetic ecologies. Mol. BioSyst. 8:2470–83
     [Google Scholar]
  10. 10.  Schinner T, Letzner A, Liedtke S, Castro FD, Eydelnant IA, Tufenkji N 2010. Transport of selected bacterial pathogens in agricultural soil and quartz sand. Water Res 44:1182–92
     [Google Scholar]
  11. 11.  Ribet D, Cossart P 2015. How bacterial pathogens colonize their hosts and invade deeper tissues. Microbes Infect 17:173–83
     [Google Scholar]
  12. 12.  Sahari A, Traore MA, Scharf BE, Behkam B 2014. Directed transport of bacteria-based drug delivery vehicles: Bacterial chemotaxis dominates particle shape. Biomed. Microdevices 16:717–25
     [Google Scholar]
  13. 13.  Guasto JS, Rusconi R, Stocker R 2012. Fluid mechanics of planktonic microorganisms. Annu. Rev. Fluid Mech. 44:373–400
     [Google Scholar]
  14. 14.  Rusconi R, Stocker R 2015. Microbes in flow. Curr. Opin. Microbiol. 25:1–8
     [Google Scholar]
  15. 15.  Lauga E 2016. Bacterial hydrodynamics. Annu. Rev. Fluid Mech. 48:105–30
     [Google Scholar]
  16. 16.  Stewart PS 2012. Mini-review: convection around biofilms. Biofouling 28:187–98
     [Google Scholar]
  17. 17.  Persat A, Nadell CD, Kim MK, Ingremeau F, Siryaporn A et al. 2015. The mechanical world of bacteria. Cell 161:988–97
     [Google Scholar]
  18. 18.  Wessel AK, Hmelo L, Parsek MR, Whiteley M 2013. Going local: technologies for exploring bacterial microenvironments. Nat. Rev. Microbiol. 11:337–48
     [Google Scholar]
  19. 19.  Frank M, Anderson D, Weeks ER, Morris JF 2003. Particle migration in pressure-driven flow of a Brownian suspension. J. Fluid Mech. 493:363–78
     [Google Scholar]
  20. 20.  Morris JF, Brady JF 1998. Pressure-driven flow of a suspension: buoyancy effects. Int. J. Multiphase Flow 24:105–30
     [Google Scholar]
  21. 21.  Pandey R, Conrad JC 2012. Effects of attraction strength on microchannel flow of colloid-polymer depletion mixtures. Soft Matter 8:10695–703
     [Google Scholar]
  22. 22.  Nikoubashman A, Mahynski NA, Pirayandeh AH, Panagiotopoulos AZ 2014. Flow-induced demixing of polymer-colloid mixtures in microfluidic channels. J. Chem. Phys. 140:094903
     [Google Scholar]
  23. 23.  Huang LR, Cox EC, Austin RH, Sturm JC 2004. Continuous particle separation through deterministic lateral displacement. Science 304:987–90
     [Google Scholar]
  24. 24.  He K, Retterer ST, Srijanto BR, Conrad JC, Krishnamoorti R 2014. Transport and dispersion of nanoparticles in periodic nanopost arrays. ACS Nano 8:4221–27
     [Google Scholar]
  25. 25.  Auset M, Keller AA 2004. Pore-scale processes that control dispersion of colloids in saturated porous media. Water Resour. Res. 40:W03503
     [Google Scholar]
  26. 26.  Bales R, Gerba C, Grondin G, Jensen S 1989. Bacteriophage transport in sandy soil and fractured tuff. Appl. Environ. Microbiol. 55:2061–67
     [Google Scholar]
  27. 27.  Mason TG, Weitz DA 1995. Optical measurements of frequency-dependent linear viscoelastic moduli of complex fluids. Phys. Rev. Lett. 74:1250–53
     [Google Scholar]
  28. 28.  Cai LH, Panyukov S, Rubinstein M 2011. Mobility of nonsticky nanoparticles in polymer liquids. Macromolecules 44:7853–63
     [Google Scholar]
  29. 29.  Poling-Skutvik R, Krishnamoorti R, Conrad JC 2015. Size-dependent dynamics of nanoparticles in unentangled polyelectrolyte solutions. ACS Macro Lett 4:1169–73
     [Google Scholar]
  30. 30.  Berry H, Chaté H 2014. Anomalous diffusion due to hindering by mobile obstacles undergoing Brownian motion or Orstein-Ulhenbeck processes. Phys. Rev. E 89:022708
     [Google Scholar]
  31. 31.  Babayekhorasani F, Dunstan DE, Krishnamoorti R, Conrad JC 2016. Nanoparticle diffusion in crowded and confined media. Soft Matter 12:8407–16
     [Google Scholar]
  32. 32.  Scholz C, Wirner F, Gomez-Solano JR, Bechinger C 2014. Enhanced dispersion by elastic turbulence in porous media. EPL 107:054003
     [Google Scholar]
  33. 33.  Jacob JDC, Krishnamoorti R, Conrad JC 2017. Particle dispersion in porous media: differentiating effects of fluid rheology and geometry. Phys. Rev. E 96:022610
     [Google Scholar]
  34. 34.  Babayekhorasani F, Dunstan DE, Krishnamoorti R, Conrad JC 2016. Nanoparticle dispersion in disordered porous media with and without polymer additives. Soft Matter 12:5676–83
     [Google Scholar]
  35. 35.  Purcell EM 1977. Life at low Reynolds number. Am. J. Phys. 45:3–11
     [Google Scholar]
  36. 36.  Misselwitz B, Barrett N, Kreibich S, Vonaesch P, Andritschke D et al. 2012. Near surface swimming of Salmonella Typhimurium explains target-site selection and cooperative invasion. PLOS Pathog 8:e1002810
     [Google Scholar]
  37. 37.  Lane MC, Lockatell V, Monterosso G, Lamphier D, Weinert J et al. 2005. Role of motility in the colonization of uropathogenic Escherichia coli in the urinary tract. Infect. Immun. 73:7644–56
     [Google Scholar]
  38. 38.  Yawata Y, Nguyen J, Stocker R, Rusconi R 2016. Microfluidic studies of biofilm formation in dynamic environments. J. Bacteriol. 198:2589–95
     [Google Scholar]
  39. 39.  Lauga E, Powers TR 2009. The hydrodynamics of swimming microorganisms. Rep. Prog. Phys. 72:096601
     [Google Scholar]
  40. 40.  Frymier PD, Ford RM, Berg HC, Cummings PT 1995. Three-dimensional tracking of motile bacteria near a solid planar surface. PNAS 92:6195–99
     [Google Scholar]
  41. 41.  Lauga E, DiLuzio WR, Whitesides GM, Stone HA 2006. Swimming in circles: motion of bacteria near solid boundaries. Biophys. J. 90:400–12
     [Google Scholar]
  42. 42.  DiLuzio WR, Turner L, Mayer M, Garstecki P, Weibel DB et al. 2005. Escherichia coli swim on the right hand side. Nature 435:1271–74
     [Google Scholar]
  43. 43.  Di Leonardo R, Dell'Arciprete D, Angelani L, Iebba V 2011. Swimming with an image. Phys. Rev. Lett. 106:038101
     [Google Scholar]
  44. 44.  Hu J, Wysocki A, Winkler RG, Gompper G 2015. Physical sensing of surface properties by microswimmers directing bacterial motion via wall slip. Sci. Rep. 5:9586
     [Google Scholar]
  45. 45.  Lemelle L, Palierne JF, Chatre E, Vaillant C, Place C 2013. Curvature reversal of the circular motion of swimming bacteria probes for slip at solid/liquid interfaces. Soft Matter 9:9759–62
     [Google Scholar]
  46. 46.  Berke AP, Turner L, Berg HC, Lauga E 2008. Hydrodynamic attraction of swimming microorganisms by surfaces. Phys. Rev. Lett. 101:038102
     [Google Scholar]
  47. 47.  Li G, Bensson J, Nisimova L, Munger D, Mahautmr P et al. 2011. Accumulation of swimming bacteria near a solid surface. Phys. Rev. E 84:041932
     [Google Scholar]
  48. 48.  Vigeant MAS, Ford RM, Wagner M, Tamm LK 2002. Reversible and irreversible adhesion of motile Escherichia coli cells analyzed by total internal reflection aqueous fluorescence microscopy. Appl. Environ. Microbiol. 68:2794–801
     [Google Scholar]
  49. 49.  Hernandez-Ortiz JP, Stoltz CG, Graham MD 2005. Transport and collective dynamics in suspensions of confined swimming particles. Phys. Rev. Lett. 95:204501
     [Google Scholar]
  50. 50.  Drescher K, Dunkel J, Cisneros LH, Ganguly S, Goldstein RE 2011. Fluid dynamics and noise in bacterial cell-cell and cell-surface scattering. PNAS 108:10940–45
     [Google Scholar]
  51. 51.  Li G, Tang JX 2009. Accumulation of microswimmers near a surface mediated by collision and rotational Brownian motion. Phys. Rev. Lett. 103:078101
     [Google Scholar]
  52. 52.  Li G, Tam LK, Tang JX 2008. Amplified effect of Brownian motion in bacterial near-surface swimming. PNAS 105:18355–59
     [Google Scholar]
  53. 53.  Bianchi S, Saglimbeni F, Di Leonardo R 2017. Holographic imaging reveals the mechanism of wall entrapment in swimming bacteria. Phys. Rev. X 7:011010
     [Google Scholar]
  54. 54.  Spagnolie SE, Lauga E 2012. Hydrodynamics of self-propulsion near a boundary: predictions and accuracy of far-field approximations. J. Fluid Mech. 700:105147
     [Google Scholar]
  55. 55.  Sipos O, Nagy K, Di Leonardo R, Galajda P 2015. Hydrodynamic trapping of swimming bacteria by convex walls. Phys. Rev. Lett. 114:258104
     [Google Scholar]
  56. 56.  Kaya T, Koser H 2009. Characterization of hydrodynamic surface interactions of Escherichia coli cell bodies in shear flow. Phys. Rev. Lett. 103:138103
     [Google Scholar]
  57. 57.  Jeffery GB 1922. The motion of ellipsoidal particles immersed in a viscous fluid. Proc. R. Soc. Lond. A 102:161–79
     [Google Scholar]
  58. 58.  Kaya T, Koser H 2012. Direct upstream motility in Escherichia coli. . Biophys. J. 102:1514–23
     [Google Scholar]
  59. 59.  Marcos, Fu HC, Powers TR, Stocker R 2012. Bacterial rheotaxis. PNAS 109:4780–85
     [Google Scholar]
  60. 60.  Hill J, Kalkanci O, McMurry JL, Koser H 2007. Hydrodynamic surface interactions enable Escherichia coli to seek efficient routes to swim upstream. Phys. Rev. Lett. 98:068101
     [Google Scholar]
  61. 61.  Figueroa-Morales N, Miño G, Rivera A, Caballero R, Clément E et al. 2015. Living on the edge: transfer and traffic of E. coli in a confined flow. Soft Matter 11:6284–93
     [Google Scholar]
  62. 62.  Costanzo A, Di Leonardo R, Ruocco G, Angelani L 2012. Transport of self-propelling bacteria in micro-channel flow. J. Phys. Condens. Matter 24:065101
     [Google Scholar]
  63. 63.  Molaei M, Barry M, Stocker R, Sheng J 2014. Failed escape: Solid surfaces prevent tumbling of Escherichia coli. . Phys. Rev. Lett. 113:068103
     [Google Scholar]
  64. 64.  Molaei M, Sheng J 2016. Succeed escape: Flow shear promotes tumbling of Escherichia coli near a solid surface. Sci. Rep. 6:35290
     [Google Scholar]
  65. 65.  Mathijssen AJTM, Doostmohammadi A, Yeomans JM, Shendruk TN 2016. Hotspots of boundary accumulation: dynamics and statistics of micro-swimmers in flowing films. J. R. Soc. Interface 13:20150936
     [Google Scholar]
  66. 66.  Rusconi R, Guasto JS, Stocker R 2014. Bacterial transport suppressed by fluid shear. Nat. Phys. 10:212–17
     [Google Scholar]
  67. 67.  Sokolov A, Aranson IS 2012. Physical properties of collective motion in suspensions of bacteria. Phys. Rev. Lett. 109:248109
     [Google Scholar]
  68. 68.  López HM, Gachelin J, Douarche C, Auradou H, Clément E 2015. Turning bacteria suspensions into superfluids. Phys. Rev. Lett. 115:028301
     [Google Scholar]
  69. 69.  Sokolov A, Apodaca MM, Grzybowski BA, Aranson IS 2010. Swimming bacteria power microscopic gears. PNAS 107:969–74
     [Google Scholar]
  70. 70.  Kaiser A, Peshkov A, Sokolov A, Ten Hagen B, Löwen H, Aranson IS 2014. Transport powered by bacterial turbulence. Phys. Rev. Lett. 112:158101
     [Google Scholar]
  71. 71.  Hernandez-Ortiz JP, Underhill PT, Graham MD 2009. Dynamics of confined suspensions of swimming particles. J. Phys. Condens. Matter 21:204107
     [Google Scholar]
  72. 72.  Dombrowski C, Cisneros L, Chatkaew S, Goldstein RE, Kessler JO 2004. Self-concentration and large-scale coherence in bacterial dynamics. Phys. Rev. Lett. 93:098103
     [Google Scholar]
  73. 73.  Wioland H, Woodhouse FG, Dunkel J, Kessler JO, Goldstein RE 2013. Confinement stabilizes a bacterial suspension into a spiral vortex. Phys. Rev. Lett. 110:268102
     [Google Scholar]
  74. 74.  Lushi E, Wioland H, Goldstein RE 2014. Fluid flows created by swimming bacteria drive self-organization in confined suspensions. PNAS 111:9733–38
     [Google Scholar]
  75. 75.  Wioland H, Lushi E, Goldstein RE 2016. Directed collective motion of bacteria under channel confinement. New J. Phys. 18:075002
     [Google Scholar]
  76. 76.  Licata NA, Mohari B, Fuqua C, Setayeshgar S 2016. Diffusion of bacterial cells in porous media. Biophys. J. 110:247–57
     [Google Scholar]
  77. 77.  Liu J, Ford RM, Smith JA 2011. Idling time of motile bacteria contributes to retardation and dispersion in sand porous medium. Environ. Sci. Technol. 45:3945–51
     [Google Scholar]
  78. 78.  Maennik J, Driessen R, Galajda P, Keymer JE, Dekker C 2009. Bacterial growth and motility in sub-micron constrictions. PNAS 106:14861–66
     [Google Scholar]
  79. 79.  Cisneros L, Dombrowski C, Goldstein RE, Kessler JO 2006. Reversal of bacterial locomotion at an obstacle. Phys. Rev. E 73:030901
     [Google Scholar]
  80. 80.  Magariyama Y, Ichiba M, Nakata K, Baba K, Ohtani T et al. 2008. Difference in bacterial motion between forward and backward swimming caused by the wall effect. Biophys. J. 88:3648–58
     [Google Scholar]
  81. 81.  Sosa-Hernández JE, Santillán M, Santana-Solano J 2017. Motility of Escherichia coli in a quasi-two-dimensional porous medium. Phys. Rev. E 95:032404
     [Google Scholar]
  82. 82.  Raatz M, Hintsche M, Bahrs M, Theves M, Beta C 2015. Swimming patterns of a polarly flagellated bacterium in environments of increasing complexity. Eur. Phys. J. Spec. Top. 224:1185–98
     [Google Scholar]
  83. 83.  Jabbarzadeh M, Hyon Y, Fu HC 2014. Swimming fluctuations of micro-organisms due to heterogeneous microstructure. Phys. Rev. E 90:043021
     [Google Scholar]
  84. 84.  Schneider WR, Doetsch RN 1974. Effect of viscosity on bacterial motility. J. Bacteriol. 117:696–701
     [Google Scholar]
  85. 85.  Martinez VA, Schwarz-Linek J, Reufer M, Wilson LG, Morozov AN, Poon WCK 2014. Flagellated bacterial motility in polymer solutions. PNAS 111:17771–76
     [Google Scholar]
  86. 86.  Patteson AE, Gopinath A, Goulian M, Arratia PE 2015. Running and tumbling with E. coli in polymeric solutions. Sci. Rep. 5:15761
     [Google Scholar]
  87. 87.  Li GJ, Karimi A, Ardekani AM 2014. Effect of solid boundaries on swimming dynamics of microorganisms in a viscoelastic fluid. Rheol. Acta 53:911–26
     [Google Scholar]
  88. 88.  Li G, Ardekani AM 2016. Collective motion of microorganisms in a viscoelastic fluid. Phys. Rev. Lett. 117:118001
     [Google Scholar]
  89. 89.  Celli JP, Turner BS, Afdhal NH, Keates S, Ghiran I et al. 2009. Helicobacter pylori moves through mucus by reducing mucin viscoelasticity. PNAS 106:14321–26
     [Google Scholar]
  90. 90.  Kimsey RB, Spielman A 1990. Motility of Lyme disease spirochetes in fluids as viscous as the extracellular matrix. J. Infect. Dis. 162:1205–8
     [Google Scholar]
  91. 91.  Mathijssen AJTM, Shendruk TN, Yeomans JM, Doostmohammadi A 2016. Upstream swimming in microbiological flows. Phys. Rev. Lett. 116:028104
     [Google Scholar]
  92. 92.  Bakker DP, Busscher HJ, van der Mei HC 2002. Bacterial deposition in a parallel plate and a stagnation point flow chamber: Microbial adhesion mechanisms depend on the mass transport conditions. Microbiology 148:597–603
     [Google Scholar]
  93. 93.  Swartjes JJTM, Veeregowda DH, van der Mei HC, Busscher HJ, Sharma PK 2014. Normally oriented adhesion versus friction forces in bacterial adhesion to polymer-brush functionalized surfaces under fluid flow. Adv. Funct. Mater. 24:4435–41
     [Google Scholar]
  94. 94.  O'Toole GA, Wong GCL 2016. Sensational biofilms: surface sensing in bacteria. Curr. Opin. Microbiol. 30:139–46
     [Google Scholar]
  95. 95.  Janissen R, Murillo DM, Niza B, Sahoo PK, Nobrega MM et al. 2015. Spatiotemporal distribution of different extracellular polymeric substances and filamentation mediate Xylella fastidiosa adhesion and biofilm formation. Sci. Rep. 5:9856
     [Google Scholar]
  96. 96.  Perni S, Preedy EC, Prokopovich P 2014. Success and failure of colloidal approaches in adhesion of microorganisms to surfaces. Adv. Colloid Interface Sci. 206:265–74
     [Google Scholar]
  97. 97.  Forero M, Thomas WE, Bland C, Nilsson LM, Sokurenko EV, Vogel V 2004. A catch-bond based nanoadhesive sensitive to shear stress. Nano Lett 4:1593–97
     [Google Scholar]
  98. 98.  Thomas WE, Trintchina E, Forero M, Vogel V, Sokurenko EV 2002. Bacterial adhesion to target cells enhanced by shear force. Cell 109:913–23
     [Google Scholar]
  99. 99.  Lecuyer S, Rusconi R, Shen Y, Forsyth AM, Vlamakis H et al. 2011. Shear stress increases the residence time of adhesion of Pseudomonas aeruginosa. . Biophys. J. 100:341–50
     [Google Scholar]
  100. 100.  Sharma S, Jaimes-Lizcano YA, McLay RB, Cirino PC, Conrad JC 2016. Subnanometric roughness affects the deposition and mobile adhesion of Escherichia coli on silanized glass surfaces. Langmuir 32:5422–33
     [Google Scholar]
  101. 101.  Thomas WE, Nilsson LM, Forero M, Sokurenko EV, Vogel V 2004. Shear-dependent “stick-and-roll” adhesion of type 1 fimbriated Escherichia coli. . Mol. Microbiol. 53:1545–57
     [Google Scholar]
  102. 102.  Anderson BN, Ding AM, Nilsson LM, Kusuma K, Tchesnokova V et al. 2007. Weak rolling adhesion enhances bacterial surface colonization. J. Bacteriol. 189:1794–802
     [Google Scholar]
  103. 103.  Boks NP, Kaper HJ, Norde W, van der Mei HC, Busscher HJ 2009. Mobile and immobile adhesion of staphylococcal strains to hydrophilic and hydrophobic surfaces. J. Colloid Interface Sci. 331:60–64
     [Google Scholar]
  104. 104.  McClaine JW, Ford RM 2002. Characterizing the adhesion of motile and nonmotile Escherichia coli to a glass surface using a parallel-plate flow chamber. Biotechnol. Bioeng. 78:179–89
     [Google Scholar]
  105. 105.  de Kerchove AJ, Elimelech M 2008. Bacterial swimming motility enhances cell deposition and surface coverage. Environ. Sci. Technol. 42:4371–77
     [Google Scholar]
  106. 106.  Lu N, Massoudieh A, Liang X, Hu D, Kamai T et al. 2015. Swimming motility reduces Azotobacter vinelandii deposition to silica surfaces. J. Environ. Qual. 44:1366–75
     [Google Scholar]
  107. 107.  Friedlander RS, Vlamakis H, Kim P, Khan M, Kolter R, Aizenberg J 2013. Bacterial flagella explore microscale hummocks and hollows to increase adhesion. PNAS 110:5624–29
     [Google Scholar]
  108. 108.  Neuman KC, Chadd EH, Liou G, Bergman K, Block SM 1999. Characterization of photodamage to Escherichia coli in optical traps. Biophys. J. 77:2856–63
     [Google Scholar]
  109. 109.  Conrad JC, Gibiansky ML, Jin F, Gordon VD, Motto DA et al. 2011. Flagella and pili-mediated near-surface single-cell motility mechanisms in P. . aeruginosa. Biophys. J. 100:1608–16
     [Google Scholar]
  110. 110.  Bennett RR, Lee CK, De Anda J, Nealson KH, Yildiz FH et al. 2016. Species-dependent hydrodynamics of flagellum-tethered bacteria in early biofilm development. J. R. Soc. Interface 13:20150966
     [Google Scholar]
  111. 111.  Sharma S, Conrad JC 2014. Attachment from flow of Escherichia coli bacteria onto silanized glass substrates. Langmuir 30:11147–55
     [Google Scholar]
  112. 112.  de Anda J, Lee EY, Lee CK, Bennett RR, Ji X et al. 2017. High-speed “4D” computational microscopy of bacterial suspensions. ACS Nano 11:9340–51
     [Google Scholar]
  113. 113.  Skerker JM, Berg HC 2001. Direction observation of extension and retraction of type IV pili. PNAS 98:6901–4
     [Google Scholar]
  114. 114.  Utada AS, Bennett RR, Fong JCN, Gibiansky ML, Yildiz FH et al. 2014. Vibrio cholerae use pili and flagella synergistically to effect motility switching and conditional surface attachment. Nat. Commun. 5:4913
     [Google Scholar]
  115. 115.  Golovkine G, Lemelle L, Burny C, Vaillant C, Palierne JF et al. 2016. Host cell surfaces induce a type IV pili-dependent alteration of bacterial swimming. Sci. Rep. 6:38950
     [Google Scholar]
  116. 116.  Gibiansky ML, Conrad JC, Jin F, Gordon VD, Motto DA et al. 2010. Bacteria use type IV pili to walk upright and detach from surfaces. Science 330:197
     [Google Scholar]
  117. 117.  Shen Y, Siryaporn A, Lecuyer S, Gitai Z, Stone HA 2012. Flow directs surface-attached bacteria to twitch upstream. Biophys. J. 103:146–51
     [Google Scholar]
  118. 118.  Meng Y, Li Y, Galvani CD, Hao G, Turner JN et al. 2005. Upstream migration of Xylella fastidiosa via pilus-driven twitching motility. J. Bacteriol. 187:5560–67
     [Google Scholar]
  119. 119.  Bahar O, De La Fuente L, Burdman S 2010. Assessing adhesion, biofilm formation and motility of Acidovorax citrulli using microfluidic flow chambers. FEMS Microbiol. Lett. 312:33–39
     [Google Scholar]
  120. 120.  Siryaporn A, Kim MK, Shen Y, Stone HA, Gitai Z 2015. Colonization, competition, and dispersal of pathogens in fluid flow networks. Curr. Biol. 25:1201–7
     [Google Scholar]
  121. 121.  Jin F, Conrad JC, Gibiansky ML, Wong GCL 2011. Bacteria use type-IV pili to slingshot on surfaces. PNAS 108:12617–22
     [Google Scholar]
  122. 122.  Meel C, Kouzel N, Oldewurtel ER, Maier B 2012. Three-dimensional obstacles for bacterial surface motility. Small 8:530–34
     [Google Scholar]
  123. 123.  Holz C, Opitz D, Mehlich J, Ravoo BJ, Maier B 2009. Bacterial motility and clustering guided by microcontact printing. Nano Lett 9:4553–57
     [Google Scholar]
  124. 124.  Zhang R, Ni L, Jin Z, Li J, Jin F 2014. Bacteria slingshot more on soft surfaces. Nat. Commun. 5:5541
     [Google Scholar]
  125. 125.  Persat A, Inclan YF, Engel JN, Stone HA, Gitai Z 2015. Type IV pili mechanochemically regulate virulence factors in Pseudomonas aeruginosa. . PNAS 112:7563–68
     [Google Scholar]
  126. 126.  Rodesney CA, Roman B, Dhamani N, Cooley BJ, Touhami A, Gordon VD 2017. Mechanosensing of shear by Pseudomonas aeruginosa leads to increased levels of the cyclic-di-GMP signal initiating biofilm development. PNAS 114:5906–11
     [Google Scholar]
  127. 127.  Epstein AK, Wong TS, Belisle RA, Boggs EM, Aizenberg J 2012. Liquid-infused structured surfaces with exceptional anti-biofouling performance. PNAS 109:13182–87
     [Google Scholar]
  128. 128.  Wloka M, Rehage H, Flemming HC, Wingender J 2004. Rheological properties of viscoelastic biofilm extracellular polymeric substances and comparison to the behavior of calcium alginate gels. Colloid Polymer Sci 282:1067–76
     [Google Scholar]
  129. 129.  Ganesan M, Knier S, Younger JG, Solomon MJ 2016. Associative and entanglement contributions to the solution rheology of a bacterial polysaccharide. Macromolecules 49:8313–21
     [Google Scholar]
  130. 130.  Zhao K, Tseng BS, Beckerman B, Jin F, Gibiansky ML et al. 2013. Psl trails guide exploration and microcolony formation in Pseudomonas aeruginosa biofilms. Nature 497:388–92
     [Google Scholar]
  131. 131.  Wang H, Sodagari M, Ju LK, Newby BMZ 2013. Effects of shear on initial bacterial attachment in slow flowing systems. Colloid Surf. B 109:32–39
     [Google Scholar]
  132. 132.  Haznedaroglu BZ, Bolster CH, Walker SL 2008. The role of starvation on Escherichia coli adhesion and transport in saturated porous media. Water Res 42:1547–54
     [Google Scholar]
  133. 133.  Song L, Sjollema J, Sharma PK, Kaper HJ, van der Mei HC, Busscher HJ 2014. Nanoscopic vibrations of bacteria with different cell-wall properties adhering to surfaces under flow and static conditions. ACS Nano 8:8457–67
     [Google Scholar]
  134. 134.  Weiss TH, Mills AL, Hornberger GM, Herman JS 1995. Effect of bacterial cell shape on transport of bacteria in porous media. Environ. Sci. Technol. 29:1737–40
     [Google Scholar]
  135. 135.  Persat A, Stone HA, Gitai Z 2014. The curved shape of Caulobacter crescentus enhances surface colonization in flow. Nat. Commun. 5:3824
     [Google Scholar]
  136. 136.  Picioreanu C, Van Loosdrecht MCM, Heijnen JJ 2000. Effect of diffusive and convective substrate transport on biofilm structure formation: a two-dimensional modeling study. Biotechnol. Bioeng. 69:504–15
     [Google Scholar]
  137. 137.  Weaver WM, Milisavljevic V, Miller JF, Di Carlo D 2012. Fluid flow induces biofilm formation in Staphylococcus epidermidis polysaccharide intracellular adhesin-positive clinical isolates. Appl. Environ. Microbiol. 78:5890–96
     [Google Scholar]
  138. 138.  Maier B, Potter L, So M, Long CD, Seifert HS, Sheetz MP 2002. Single pilus motor forces exceed 100 pN. PNAS 99:16012–17
     [Google Scholar]
  139. 139.  Billings N, Birjiniuk A, Samad TS, Doyle PS, Ribbeck K 2015. Material properties of biofilms: a review of methods for understanding permeability and mechanics. Rep. Prog. Phys. 78:036601–18
     [Google Scholar]
  140. 140.  Shaw T, Winston M, Rupp CJ, Klapper I, Stoodley P 2004. Commonality of elastic relaxation times in biofilms. Phys. Rev. Lett. 93:098102
     [Google Scholar]
  141. 141.  Pavlovsky L, Younger JG, Solomon MJ 2013. In situ rheology of Staphylococcus epidermidis bacterial biofilms. Soft Matter 9:122–31
     [Google Scholar]
  142. 142.  Chen M, Zhang Z, Bott T 1998. Direct measurement of the adhesive strength of biofilms in pipes by micromanipulation. Biotechnol. Tech. 12:875–80
     [Google Scholar]
  143. 143.  Kostenko V, Salek MM, Sattari P, Martinuzzi RJ 2010. Staphylococcus aureus biofilm formation and tolerance to antibiotics in response to oscillatory shear stresses of physiological levels. FEMS Immunol. Med. Microbiol. 59:421–31
     [Google Scholar]
  144. 144.  Vieira MJ, Melo LF, Pinheiro MM 1993. Biofilm formation: hydrodynamic effects on internal diffusion and structure. Biofouling 7:67–80
     [Google Scholar]
  145. 145.  Stoodley P, Jacobsen A, Dunsmore BC, Purevdorj B, Wilson S et al. 2001. The influence of fluid shear and AlCl3 on the material properties of Pseudomonas aeruginosa PAO1 and Desulfovibrio sp. EX265 biofilms. Water Sci. Technol. 43:113–20
     [Google Scholar]
  146. 146.  Dunsmore BC, Jacobsen A, Hall-Stoodley L, Bass CJ, Lappin-Scott HM, Stoodley P 2002. The influence of fluid shear on the structure and material properties of sulphate-reducing bacterial biofilms. J. Ind. Microbiol. Biotechnol. 29:347–53
     [Google Scholar]
  147. 147.  Paramonova E, Kalmykowa OJ, van der Mei HC, Busscher HJ, Sharma PK 2009. Impact of hydrodynamics on oral biofilm strength. J. Dent. Res. 88:922–26
     [Google Scholar]
  148. 148.  Purevdorj B, Costerton JW, Stoodley P 2002. Influence of hydrodynamics and cell signaling on the structure and behavior of Pseudomonas aeruginosa biofilms. Appl. Environ. Microbiol. 68:4457–64
     [Google Scholar]
  149. 149.  Choi YC, Morgenroth E 2003. Monitoring biofilm detachment under dynamic changes in shear stress using laser-based particle size analysis and mass fractionation. Water Sci. Technol. 47:69–76
     [Google Scholar]
  150. 150.  Stoodley P, Cargo R, Rupp CJ, Wilson S, Klapper I 2002. Biofilm material properties as related to shear-induced deformation and detachment phenomena. J. Ind. Microbiol. Biotechnol. 29:361–67
     [Google Scholar]
  151. 151.  Rupp CJ, Fux CA, Stoodley P 2005. Viscoelasticity of Staphylococcus aureus biofilms in response to fluid shear allows resistance to detachment and facilitates rolling migration. Appl. Environ. Microbiol. 71:2175–78
     [Google Scholar]
  152. 152.  Rusconi R, Lecuyer S, Autrusson N, Guglielmini L, Stone HA 2011. Secondary flow as a mechanism for the formation of biofilm streamers. Biophys. J. 100:1392–99
     [Google Scholar]
  153. 153.  Hassanpourfard M, Ghosh R, Thundat T, Kumar A 2016. Dynamics of bacterial streamers induced clogging in microfluidic devices. Lab Chip 16:4091–96
     [Google Scholar]
  154. 154.  Stoodley P, Lewandowski Z, Boyle JD, Lappin-Scott HM 1999. Structural deformation of bacterial biofilms caused by short-term fluctuations in fluid shear: an in situ investigation of biofilm rheology. Biotechnol. Bioeng. 65:83–92
     [Google Scholar]
  155. 155.  Kim MK, Drescher K, Pak OS, Bassler BL, Stone HA 2014. Filaments in curved streamlines: rapid formation of Staphylococcus aureus biofilm streamers. New J. Phys. 16:065204
     [Google Scholar]
  156. 156.  Yazdi S, Ardekani AM 2012. Bacterial aggregation and biofilm formation in a vortical flow. Biomicrofluidics 6:044114
     [Google Scholar]
  157. 157.  Rusconi R, Lecuyer S, Guglielmini L, Stone HA 2010. Laminar flow around corners triggers the formation of biofilm streamers. J. R. Soc. Interface 7:1293–99
     [Google Scholar]
  158. 158.  Hassanpourfard M, Nikakhtari Z, Ghosh R, Das S, Thundat T et al. 2015. Bacterial floc mediated rapid streamer formation in creeping flows. Sci. Rep. 5:13070
     [Google Scholar]
  159. 159.  Drescher K, Shen Y, Bassler BL, Stone HA 2013. Biofilm streamers cause catastrophic disruption of flow with consequences for environmental and medical systems. PNAS 110:4345–50
     [Google Scholar]
  160. 160.  Kumar A, Karig D, Acharya R, Neethirajan S, Mukherjee PP et al. 2013. Microscale confinement features can affect biofilm formation. Microfluid. Nanofluid. 14:895–902
     [Google Scholar]
  161. 161.  Bottero S, Storck T, Heimovaara TJ, van Loosdrecht MC, Enzien MV, Picioreanu C 2013. Biofilm development and the dynamics of preferential flow paths in porous media. Biofouling 29:1069–86
     [Google Scholar]
  162. 162.  Peszynska M, Trykozko A, Iltis G, Schlueter S, Wildenschild D 2016. Biofilm growth in porous media: experiments, computational modeling at the porescale, and upscaling. Adv. Water Resour. 95:288–301
     [Google Scholar]
  163. 163.  Coyte KZ, Tabuteau H, Gaffney EA, Foster KR, Durham WM 2017. Microbial competition in porous environments can select against rapid biofilm growth. PNAS 114:E161–70
     [Google Scholar]
  164. 164.  Nadell CD, Ricaurte D, Yan J, Drescher K, Bassler BL 2017. Flow environment and matrix structure interact to determine spatial competition in Pseudomonas aeruginosa biofilms. eLife 6:e21855
     [Google Scholar]
  165. 165.  Stewart PS 2003. Diffusion in biofilms. J. Bacteriol. 185:1485–91
     [Google Scholar]
  166. 166.  Stoodley P, Yang S, Lappin-Scott H, Lewandowski Z 1997. Relationship between mass transfer coefficient and liquid flow velocity in heterogenous biofilms using microelectrodes and confocal microscopy. Biotechnol. Bioeng. 56:681–88
     [Google Scholar]
  167. 167.  Beyenal H, Lewandowski Z 2002. Internal and external mass transfer in biofilms grown at various flow velocities. Biotechnol. Prog. 18:55–61
     [Google Scholar]
  168. 168.  Stanley NR, Lazazzera BA 2004. Environmental signals and regulatory pathways that influence biofilm formation. Mol. Microbiol. 52:917–24
     [Google Scholar]
  169. 169.  Waters CM, Bassler BL 2005. Quorum sensing: cell-to-cell communication in bacteria. Annu. Rev. Cell Dev. Biol. 21:319–46
     [Google Scholar]
  170. 170.  Connell JL, Wessel AK, Parsek MR, Ellington AD, Whiteley M, Shear JB 2010. Probing prokaryotic social behaviors with bacterial “lobster traps. .” mBio 1:e00202
     [Google Scholar]
  171. 171.  Dulla G, Lindow SE 2008. Quorum size of Pseudomonas syringae is small and dictated by water availability on the leaf surface. PNAS 105:3082–87
     [Google Scholar]
  172. 172.  Ribbe J, Maier B 2016. Density-dependent differentiation of bacteria in spatially structured open systems. Biophys. J. 110:1648–60
     [Google Scholar]
  173. 173.  Boedicker JQ, Vincent ME, Ismagilov RF 2009. Microfluidic confinement of single cells of bacteria in small volumes initiates high-density behavior of quorum sensing and growth and reveals its variability. Angew. Chem. Int. Ed. 48:5908–11
     [Google Scholar]
  174. 174.  Carnes EC, Lopez DM, Donegan NP, Cheung A, Gresham H et al. 2010. Confinement-induced quorum sensing of individual Staphylococcus aureus bacteria. Nat. Chem. Biol. 6:41–45
     [Google Scholar]
  175. 175.  Kirisits MJ, Margolis JJ, Purevdorj-Gage BL, Vaughan B, Chopp DL et al. 2007. Influence of the hydrodynamic environment on quorum sensing in Pseudomonas aeruginosa biofilms. J. Bacteriol. 189:8357–60
     [Google Scholar]
  176. 176.  Kim MK, Ingremeau F, Zhao A, Bassler BL, Stone HA 2016. Local and global consequences of flow on bacterial quorum sensing. Nat. Microbiol. 1:15005
     [Google Scholar]
  177. 177.  Emge P, Moeller J, Jang H, Rusconi R, Yawata Y et al. 2016. Resilience of bacterial quorum sensing against fluid flow. Sci. Rep. 6:33115
     [Google Scholar]
  178. 178.  Zhao J, Wang Q 2017. Three-dimensional numerical simulations of biofilm dynamics with quorum sensing in a flow cell. Bull. Math Biol. 79:884–919
     [Google Scholar]
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Confined Flow: Consequences and Implications for Bacteria and Biofilms
Annual Review of Chemical and Biomolecular Engineering 9, 175 (2018); https://doi.org/10.1146/annurev-chembioeng-060817-084006
/content/journals/10.1146/annurev-chembioeng-060817-084006
/content/journals/10.1146/annurev-chembioeng-060817-084006
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