1932

Abstract

Microfluidics has significantly contributed to the expansion of the frontiers of microbial ecology over the past decade by allowing researchers to observe the behaviors of microbes in highly controlled microenvironments, across scales from a single cell to mixed communities. Spatially and temporally varying distributions of organisms and chemical cues that mimic natural microbial habitats can now be established by exploiting physics at the micrometer scale and by incorporating structures with specific geometries and materials. In this article, we review applications of microfluidics that have resulted in insightful discoveries on fundamental aspects of microbial life, ranging from growth and sensing to cell-cell interactions and population dynamics. We anticipate that this flexible multidisciplinary technology will continue to facilitate discoveries regarding the ecology of microorganisms and help uncover strategies to control microbial processes such as biofilm formation and antibiotic resistance.

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2014-05-06
2024-06-19
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Literature Cited

  1. Adler M, Erickstad M, Gutierrez E, Groisman A. 1.  2012. Studies of bacterial aerotaxis in a microfluidic device. Lab Chip 12:4835–47 [Google Scholar]
  2. Adler M, Polinkovsky M, Gutierrez E, Groisman A. 2.  2010. Generation of oxygen gradients with arbitrary shapes in a microfluidic device. Lab Chip 10:388–91 [Google Scholar]
  3. Ahmed T, Shimizu TS, Stocker R. 3.  2010. Bacterial chemotaxis in linear and nonlinear steady microfluidic gradients. Nano Lett. 10:3379–85 [Google Scholar]
  4. Ahmed T, Shimizu TS, Stocker R. 4.  2010. Microfluidics for bacterial chemotaxis. Integr. Biol. 2:604–29 [Google Scholar]
  5. Ahmed T, Stocker R. 5.  2008. Experimental verification of the behavioral foundation of bacterial transport parameters using microfluidics. Biophys. J. 95:4481–93 [Google Scholar]
  6. Akin D, Li H, Bashir R. 6.  2004. Real-time virus trapping and fluorescent imaging in microfluidic devices. Nano Lett. 4:257–59 [Google Scholar]
  7. Altshuler E, Miño G, Pérez-Penichet C, Río LD, Lindner A. 7.  et al. 2013. Flow-controlled densification and anomalous dispersion of E. coli through a constriction. Soft Matter 9:1864–70 [Google Scholar]
  8. Anselme K, Davidson P, Popa AM, Giazzon M, Liley M, Ploux L. 8.  2010. The interaction of cells and bacteria with surfaces structured at the nanometre scale. Acta Biomater. 6:3824–46 [Google Scholar]
  9. Balaban NQ, Merrin J, Chait R, Kowalik L, Leibler S. 9.  2004. Bacterial persistence as a phenotypic switch. Science 305:1622–25Single-cell microfluidic confinement reveals that cells that become persisters initially exhibit a phenotype of slow growth. [Google Scholar]
  10. Balagaddé FK, You L, Hansen CL, Arnold FH, Quake SR. 10.  2005. Long-term monitoring of bacteria undergoing programmed population control in a microchemostat. Science 309:137–40 [Google Scholar]
  11. Battin TJ, Kaplan LA, Newbold JD, Hansen CME. 11.  2003. Contributions of microbial biofilms to ecosystem processes in stream mesocosms. Nature 426:439–42 [Google Scholar]
  12. Bennett MR, Hasty J. 12.  2009. Microfluidic devices for measuring gene network dynamics in single cells. Nat. Rev. Genet. 10:628–38 [Google Scholar]
  13. Boedicker JQ, Vincent ME, Ismagilov RF. 13.  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. 48:5908–11Exploits microfluidic confinement to show that quorum sensing can also occur among few cells, provided these are suitably confined. [Google Scholar]
  14. Cheng SY, Heilman S, Wasserman M, Archer S, Shuler ML, Wu M. 14.  2007. A hydrogel-based microfluidic device for the studies of directed cell migration. Lab Chip 7:763–69 [Google Scholar]
  15. Cho H, Jönsson H, Campbell K, Melke P, Williams JW. 15.  et al. 2007. Self-organization in high-density bacterial colonies: efficient crowd control. PLoS Biol. 5:e302 [Google Scholar]
  16. Choi J, Jung Y-G, Kim J, Kim S, Jung Y. 16.  et al. 2013. Rapid antibiotic susceptibility testing by tracking single cell growth in a microfluidic agarose channel system. Lab Chip 13:280–87 [Google Scholar]
  17. Churski K, Kaminski TS, Jakiela S, Kamysz W, Baranska-Rybak W. 17.  et al. 2012. Rapid screening of antibiotic toxicity in an automated microdroplet system. Lab Chip 12:1629–37 [Google Scholar]
  18. Cimetta E, Franzoso M, Trevisan M, Serena E, Zambon A. 18.  et al. 2012. Microfluidic-driven viral infection on cell cultures: theoretical and experimental study. Biomicrofluidics 6:24127 [Google Scholar]
  19. Cira NJ, Ho JY, Dueck ME, Weibel DB. 19.  2012. A self-loading microfluidic device for determining the minimum inhibitory concentration of antibiotics. Lab Chip 12:1052–59 [Google Scholar]
  20. Connell JL, Ritschdorff ET, Whiteley M, Shear JB. 20.  2013. 3D printing of microscopic bacterial communities. Proc. Natl. Acad. Sci. USA 110:18380–85 [Google Scholar]
  21. Danino T, Mondragón-Palomino O, Tsimring L, Hasty J. 21.  2010. A synchronized quorum of genetic clocks. Nature 463:326–30 [Google Scholar]
  22. De La Fuente L, Montanes E, Meng Y, Li Y, Burr TJ. 22.  et al. 2007. Assessing adhesion forces of type I and type IV pili of Xylella fastidiosa bacteria by use of a microfluidic flow chamber. Appl. Environ. Microbiol. 73:2690–96 [Google Scholar]
  23. Demir M, Douarche C, Yoney A, Libchaber A, Salman H. 23.  2011. Effects of population density and chemical environment on the behavior of Escherichia coli in shallow temperature gradients. Phys. Biol. 8:063001 [Google Scholar]
  24. Demir M, Salman H. 24.  2012. Bacterial thermotaxis by speed modulation. Biophys. J. 103:1683–90 [Google Scholar]
  25. Diao J, Young L, Kim S, Fogarty EA, Heilman SM. 25.  et al. 2006. A three-channel microfluidic device for generating static linear gradients and its application to the quantitative analysis of bacterial chemotaxis. Lab Chip 6:381–88 [Google Scholar]
  26. DiLuzio WR, Turner L, Mayer M, Garstecki P, Weibel DB. 26.  et al. 2005. Escherichia coli swim on the right-hand side. Nature 435:1271–74 [Google Scholar]
  27. Drescher K, Shen Y, Bassler BL, Stone HA. 27.  2013. Biofilm streamers cause catastrophic disruption of flow with consequences for environmental and medical systems. Proc. Natl. Acad. Sci. USA 110:4345–50 [Google Scholar]
  28. Durham WM, Tranzer O, Leombruni A, Stocker R. 28.  2012. Division by fluid incision: biofilm patch development in porous media. Phys. Fluids 24:091107 [Google Scholar]
  29. Elowitz MB, Leibler S. 29.  2000. A synthetic oscillatory network of transcriptional regulators. Nature 403:335–38 [Google Scholar]
  30. Englert DL, Manson MD, Jayaraman A. 30.  2010. Investigation of bacterial chemotaxis in flow-based microfluidic devices. Nat. Protoc. 5:864–72 [Google Scholar]
  31. Eun Y-J, Utada AS, Copeland MF, Takeuchi S, Weibel DB. 31.  2011. Encapsulating bacteria in agarose microparticles using microfluidics for high-throughput cell analysis and isolation. ACS Chem. Biol. 6:260–66 [Google Scholar]
  32. Gachelin J, Miño G, Berthet H, Lindner A, Rousselet A, Clément E. 32.  2013. Non-Newtonian viscosity of Escherichia coli suspensions. Phys. Rev. Lett. 110:268103 [Google Scholar]
  33. Galajda P, Keymer J, Chaikin P, Austin R. 33.  2007. A wall of funnels concentrates swimming bacteria. J. Bacteriol. 189:8704–7 [Google Scholar]
  34. Garcia X, Rafaï S, Peyla P. 34.  2013. Light control of the flow of phototactic microswimmer suspensions. Phys. Rev. Lett. 110:138106 [Google Scholar]
  35. Garren M, Son K, Raina J-B, Rusconi R, Menolascina F. 35.  et al. 2014. A bacterial pathogen uses dimethylsulfoniopropionate as a cue to target heat-stressed corals. ISME J 8999–1007 [Google Scholar]
  36. Gefen O, Gabay C, Mumcuoglu M, Engel G, Balaban NQ. 36.  2008. Single-cell protein induction dynamics reveals a period of vulnerability to antibiotics in persister bacteria. Proc. Natl. Acad. Sci. USA 105:6145–49 [Google Scholar]
  37. Groisman A, Lobo C, Cho H, Campbell JK, Dufour YS. 37.  et al. 2005. A microfluidic chemostat for experiments with bacterial and yeast cells. Nat. Methods 2:685–89 [Google Scholar]
  38. Guasto JS, Rusconi R, Stocker R. 38.  2012. Fluid mechanics of planktonic microorganisms. Annu. Rev. Fluid Mech. 44:373–400 [Google Scholar]
  39. Guglielmini L, Rusconi R, Lecuyer S, Stone HA. 39.  2011. Three-dimensional features in low-Reynolds-number confined corner flows. J. Fluid Mech. 668:33–57 [Google Scholar]
  40. Guo P, Rotem A, Heyman JA, Weitz DA. 40.  2012. Droplet microfluidics for high-throughput biological assays.. Lab Chip 12:2146–55 [Google Scholar]
  41. Hiratsuka Y, Miyata M, Uyeda TQP. 41.  2005. Living microtransporter by uni-directional gliding of Mycoplasma along microtracks. Biochem. Biophys. Res. Commun. 331:318–24 [Google Scholar]
  42. Hochbaum AI, Aizenberg J. 42.  2010. Bacteria pattern spontaneously on periodic nanostructure arrays. Nano Lett. 10:3717–21Microfabricated nanoscale topographic features cause distinct bacterial ordering and oriented attachment. [Google Scholar]
  43. Holz C, Opitz D, Mehlich J, Ravoo BJ, Maier B. 43.  2009. Bacterial motility and clustering guided by microcontact printing. Nano Lett. 9:4553–57 [Google Scholar]
  44. Hudson SD, Phelan FR, Handler MD, Cabral JT, Migler KB, Amis EJ. 44.  2004. Microfluidic analog of the four-roll mill. Appl. Phys. Lett. 85:335–37 [Google Scholar]
  45. Hulme SE, DiLuzio WR, Shevkoplyas SS, Turner L, Mayer M. 45.  et al. 2008. Using ratchets and sorters to fractionate motile cells of Escherichia coli by length. Lab Chip 8:1888–95 [Google Scholar]
  46. Jeon NL, Dertinger SKW, Chiu DT, Choi IS, Stroock AD, Whitesides GM. 46.  2000. Generation of solution and surface gradients using microfluidic systems. Langmuir 16:8311–16 [Google Scholar]
  47. Kalashnikov M, Lee JC, Campbell J, Sharon A, Sauer-Budge AF. 47.  2012. A microfluidic platform for rapid, stress-induced antibiotic susceptibility testing of Staphylococcus aureus. Lab Chip 12:4523–32 [Google Scholar]
  48. Kalinin Y, Neumann S, Sourjik V, Wu M. 48.  2010. Responses of Escherichia coli bacteria to two opposing chemoattractant gradients depend on the chemoreceptor ratio. J. Bacteriol. 192:1796–800 [Google Scholar]
  49. Kalinin YV, Jiang L, Tu Y, Wu M. 49.  2009. Logarithmic sensing in Escherichia coli bacterial chemotaxis. Biophys. J. 96:2439–48Harvests the precision of microfluidic gradient generators to demonstrate that E. coli responds to logarithms of concentration gradients (log-sensing). [Google Scholar]
  50. Kantsler V, Dunkel J, Polin M, Goldstein RE. 50.  2013. Ciliary contact interactions dominate surface scattering of swimming eukaryotes. Proc. Natl. Acad. Sci. USA 110:1187–92 [Google Scholar]
  51. Kargar M, Wang J, Nain AS, Behkam B. 51.  2012. Controlling bacterial adhesion to surfaces using topographical cues: a study of the interaction of Pseudomonas aeruginosa with nanofiber-textured surfaces. Soft Matter 8:10254–59 [Google Scholar]
  52. Kastrup CJ, Boedicker JQ, Pomerantsev AP, Moayeri M, Bian Y. 52.  et al. 2008. Spatial localization of bacteria controls coagulation of human blood by ‘quorum acting’. Nat. Chem. Biol. 4:742–50Demonstrates that the spatial distribution of bacteria, modulated by microfluidic surface patterning, affects blood coagulation in humans and mice. [Google Scholar]
  53. Kaya T, Koser H. 53.  2012. Direct upstream motility in Escherichia coli. Biophys. J. 102:1514–23 [Google Scholar]
  54. Keymer JE, Galajda P, Lambert G, Liao D, Austin RH. 54.  2008. Computation of mutual fitness by competing bacteria. Proc. Natl. Acad. Sci. USA 105:20269–73Shows that in nanofabricated heterogeneous landscapes two otherwise competing strains of bacteria actually cooperate. [Google Scholar]
  55. Keymer JE, Galajda P, Muldoon C, Park S, Austin RH. 55.  2006. Bacterial metapopulations in nanofabricated landscapes. Proc. Natl. Acad. Sci. USA 103:17290–95 [Google Scholar]
  56. Kim D, Liu A, Diller E, Sitti M. 56.  2012. Chemotactic steering of bacteria propelled microbeads. Biomed. Microdevices 14:1009–17 [Google Scholar]
  57. Kim HJ, Boedicker JQ, Choi JW, Ismagilov RF. 57.  2008. Defined spatial structure stabilizes a synthetic multispecies bacterial community. Proc. Natl. Acad. Sci. USA 105:18188–93 [Google Scholar]
  58. Kim HJ, Huh D, Hamilton G, Ingber DE. 58.  2012. Human gut-on-a-chip inhabited by microbial flora that experiences intestinal peristalsis-like motions and flow. Lab Chip 12:2165–74Recreates the symbiotic interaction between bacteria and human cells in a microfluidic device. [Google Scholar]
  59. Kim M, Kim SH, Lee SK, Kim T. 59.  2011. Microfluidic device for analyzing preferential chemotaxis and chemoreceptor sensitivity of bacterial cells toward carbon sources. Analyst 136:3238–43 [Google Scholar]
  60. Kim MJ, Breuer KS. 60.  2004. Enhanced diffusion due to motile bacteria. Phys. Fluids 16:L78 [Google Scholar]
  61. Kim MJ, Breuer KS. 61.  2007. Use of bacterial carpets to enhance mixing in microfluidic systems. J. Fluids Eng. 129:319–24 [Google Scholar]
  62. Kim MJ, Breuer KS. 62.  2008. Microfluidic pump powered by self-organizing bacteria. Small 4:111–18 [Google Scholar]
  63. Kim T, Pinelis M, Maharbiz MM. 63.  2009. Generating steep, shear-free gradients of small molecules for cell culture. Biomed. Microdevices 11:65–73 [Google Scholar]
  64. Kumar A, Karig D, Acharya R, Neethirajan S, Mukherjee PP. 64.  et al. 2012. Microscale confinement features can affect biofilm formation. Microfluid. Nanofluid. 14:895–902 [Google Scholar]
  65. Lambert G, Liao D, Austin RH. 65.  2010. Collective escape of chemotactic swimmers through microscopic ratchets. Phys. Rev. Lett. 104:168102 [Google Scholar]
  66. Lauga E, DiLuzio WR, Whitesides GM, Stone HA. 66.  2006. Swimming in circles: motion of bacteria near solid boundaries. Biophys. J. 90:400–12 [Google Scholar]
  67. Lazova MD, Ahmed T, Bellomo D, Stocker R, Shimizu TS. 67.  2011. Response scaling in bacterial chemotaxis. Proc. Natl. Acad. Sci. USA 108:13870–75 [Google Scholar]
  68. Lecuyer S, Rusconi R, Shen Y, Forsyth A, Vlamakis H. 68.  et al. 2011. Shear stress increases the residence time of adhesion of Pseudomonas aeruginosa. Biophys. J. 100:341–50 [Google Scholar]
  69. Liu W, Kim HJ, Lucchetta EM, Du W, Ismagilov RF. 69.  2009. Isolation, incubation, and parallel functional testing and identification by FISH of rare microbial single-copy cells from multi-species mixtures using the combination of chemistrode and stochastic confinement. Lab Chip 9:2153–62 [Google Scholar]
  70. Locsei JT, Pedley TJ. 70.  2009. Run and tumble chemotaxis in a shear flow: the effect of temporal comparisons, persistence, rotational diffusion, and cell shape. Bull. Math. Biol. 71:1089–116 [Google Scholar]
  71. Long T, Ford RM. 71.  2009. Enhanced transverse migration of bacteria by chemotaxis in a porous T-sensor. Environ. Sci. Technol. 43:1546–52 [Google Scholar]
  72. Long Z, Nugent E, Javer A, Cicuta P, Sclavi B. 72.  et al. 2013. Microfluidic chemostat for measuring single cell dynamics in bacteria. Lab Chip 13:947–54 [Google Scholar]
  73. Männik J, Driessen R, Galajda P, Keymer JE, Dekker C. 73.  2009. Bacterial growth and motility in sub-micron constrictions. Proc. Natl. Acad. Sci. USA 106:14861–66 [Google Scholar]
  74. Männik J, Wu F, Hol FJH, Bisicchia P, Sherratt DJ. 74.  et al. 2012. Robustness and accuracy of cell division in Escherichia coli in diverse cell shapes. Proc. Natl. Acad. Sci. USA 109:6957–62 [Google Scholar]
  75. Mao H, Cremer PS, Manson MD. 75.  2003. A sensitive, versatile microfluidic assay for bacterial chemotaxis. Proc. Natl. Acad. Sci. USA 100:5449–54Provides the first demonstration of the potential of microfluidic approaches for studies of bacterial chemotaxis. [Google Scholar]
  76. Marcos, Fu HC, Powers TR, Stocker R. 76.  2009. Separation of microscale chiral objects by shear flow. Phys. Rev. Lett. 102:158103 [Google Scholar]
  77. Marcos, Fu HC, Powers TR, Stocker R. 77.  2012. Bacterial rheotaxis. Proc. Natl. Acad. Sci. USA 109:4780–85 [Google Scholar]
  78. Marcos, Stocker R. 78.  2006. Microorganisms in vortices: a microfluidic setup. Limnol. Oceanogr. Methods 4:392–98 [Google Scholar]
  79. Marcy Y, Ouverney C, Bik EM, Lösekann T, Ivanova N. 79.  et al. 2007. Dissecting biological “dark matter” with single-cell genetic analysis of rare and uncultivated TM7 microbes from the human mouth. Proc. Natl. Acad. Sci. USA 104:11889–94 [Google Scholar]
  80. Martel S. 80.  2012. Bacterial microsystems and microrobots. Biomed. Microdevices 14:1033–45 [Google Scholar]
  81. Marty A, Roques C, Causserand C, Bacchin P. 81.  2012. Formation of bacterial streamers during filtration in microfluidic systems. Biofouling 28:551–62 [Google Scholar]
  82. Masson J-B, Voisinne G, Wong-Ng J, Celani A, Vergassola M. 82.  2012. Noninvasive inference of the molecular chemotactic response using bacterial trajectories. Proc. Natl. Acad. Sci. USA 109:1802–7 [Google Scholar]
  83. Mather W, Mondragón-Palomino O, Danino T, Hasty J, Tsimring LS. 83.  2010. Streaming instability in growing cell populations. Phys. Rev. Lett. 104:208101 [Google Scholar]
  84. Meng Y, Li Y, Galvani CD, Hao G. 84.  2005. Upstream migration of Xylella fastidiosa via pilus-driven twitching motility. J. Bacteriol. 187:5560–67 [Google Scholar]
  85. Park S, Kim D, Mitchell RJ, Kim T. 85.  2011. A microfluidic concentrator array for quantitative predation assays of predatory microbes. Lab Chip 11:2916–23 [Google Scholar]
  86. Park S, Wolanin PM, Yuzbashyan EA, Lin H, Darnton NC. 86.  et al. 2003. Influence of topology on bacterial social interaction. Proc. Natl. Acad. Sci. USA 100:13910–15 [Google Scholar]
  87. Park S, Wolanin PM, Yuzbashyan EA, Silberzan P, Stock JB, Austin RH. 87.  2003. Motion to form a quorum. Science 301:188 [Google Scholar]
  88. Rang CU, Peng AY, Chao L. 88.  2011. Temporal dynamics of bacterial aging and rejuvenation. Curr. Biol. 21:1813–16 [Google Scholar]
  89. Rusconi R, Guasto JS, Stocker R. 89.  2014. Bacterial transport is suppressed by fluid shear. Nat. Phys. 10:212–17 [Google Scholar]
  90. Rusconi R, Lecuyer S, Autrusson N, Guglielmini L, Stone HA. 90.  2011. Secondary flow as a mechanism for the formation of biofilm streamers. Biophys. J. 100:1392–99 [Google Scholar]
  91. Rusconi R, Lecuyer S, Guglielmini L, Stone HA. 91.  2010. Laminar flow around corners triggers the formation of biofilm streamers. J. R. Soc. Interface 7:1293–99 [Google Scholar]
  92. Salman H, Zilman A, Loverdo C, Jeffroy M, Libchaber A. 92.  2006. Solitary modes of bacterial culture in a temperature gradient. Phys. Rev. Lett. 97:118101 [Google Scholar]
  93. Saragosti J, Calvez V, Bournaveas N, Buguin A, Silberzan P, Perthame B. 93.  2010. Mathematical description of bacterial traveling pulses. PLoS Comput. Biol. 6:e1000890 [Google Scholar]
  94. Saragosti J, Calvez V, Bournaveas N, Perthame B, Buguin A, Silberzan P. 94.  2011. Directional persistence of chemotactic bacteria in a traveling concentration wave. Proc. Natl. Acad. Sci. USA 108:16235–40Microfluidic experiments show that E. coli can modulate their reorientations, increasing their chemotactic velocity. [Google Scholar]
  95. Seymour JR, Ahmed T, Durham WM, Stocker R. 95.  2010. Chemotactic response of marine bacteria to the extracellular products of Synechococcus and Prochlorococcus. Aquat. Microb. Ecol. 59:161–68 [Google Scholar]
  96. Seymour JR, Ahmed T, Marcos, Stocker R. 96.  2008. A microfluidic chemotaxis assay to study microbial behavior in diffusing nutrient patches. Limnol. Oceanogr. Methods 6:477–88 [Google Scholar]
  97. Seymour JR, Ahmed T, Stocker R. 97.  2009. Bacterial chemotaxis towards the extracellular products of the toxic phytoplankton Heterosigma akashiwo. J. Plankton Res. 31:1557–61 [Google Scholar]
  98. Seymour JR, Marcos, Stocker R. 98.  2009. Resource patch formation and exploitation throughout the marine microbial food web. Am. Nat. 173:E15–29 [Google Scholar]
  99. Seymour JR, Simó R, Ahmed T, Stocker R. 99.  2010. Chemoattraction to dimethylsulfoniopropionate throughout the marine microbial food web. Science 329:342–45 [Google Scholar]
  100. Shen Y, Siryaporn A, Lecuyer S, Gitai Z, Stone HA. 100.  2012. Flow directs surface-attached bacteria to twitch upstream. Biophys. J. 103:146–51 [Google Scholar]
  101. Siegal-Gaskins D, Crosson S. 101.  2008. Tightly regulated and heritable division control in single bacterial cells. Biophys. J. 95:2063–72 [Google Scholar]
  102. Singh R, Olson MS. 102.  2012. Transverse chemotactic migration of bacteria from high to low permeability regions in a dual permeability microfluidic device. Environ. Sci. Technol. 46:3188–95 [Google Scholar]
  103. Sokolov A, Apodaca MM, Grzybowski BA, Aranson IS. 103.  2010. Swimming bacteria power microscopic gears. Proc. Natl. Acad. Sci. USA 107:969–74 [Google Scholar]
  104. Stewart EJ, Madden R, Paul G, Taddei F. 104.  2005. Aging and death in an organism that reproduces by morphologically symmetric division. PLoS Biol. 3:e45 [Google Scholar]
  105. Stocker R, Seymour JR, Samadani A, Hunt DE, Polz MF. 105.  2008. Rapid chemotactic response enables marine bacteria to exploit ephemeral microscale nutrient patches. Proc. Natl. Acad. Sci. USA 105:4209–14 [Google Scholar]
  106. Sun P, Liu Y, Sha J, Zhang Z, Tu Q. 106.  et al. 2011. High-throughput microfluidic system for long-term bacterial colony monitoring and antibiotic testing in zero-flow environments. Biosens. Bioelectron. 26:1993–99 [Google Scholar]
  107. Tadmor AD, Ottesen EA, Leadbetter JR, Phillips R. 107.  2011. Probing individual environmental bacteria for viruses by using microfluidic digital PCR. Science 333:58–62 [Google Scholar]
  108. Takeuchi S, DiLuzio WR, Weibel DB, Whitesides GM. 108.  2005. Controlling the shape of filamentous cells of Escherichia coli. Nano Lett. 5:1819–23 [Google Scholar]
  109. Taylor JR, Stocker R. 109.  2012. Trade-offs of chemotactic foraging in turbulent water. Science 338:675–79 [Google Scholar]
  110. Valiei A, Kumar A, Mukherjee PP, Liu Y, Thundat T. 110.  2012. A web of streamers: biofilm formation in a porous microfluidic device. Lab Chip 12:5133–37 [Google Scholar]
  111. Vega NM, Allison KR, Khalil AS, Collins JJ. 111.  2012. Signaling-mediated bacterial persister formation. Nat. Chem. Biol. 8:431–33 [Google Scholar]
  112. Volfson D, Cookson S, Hasty J, Tsimring LS. 112.  2008. Biomechanical ordering of dense cell populations. Proc. Natl. Acad. Sci. USA 105:15346–51 [Google Scholar]
  113. Vrouwenvelder JS, Buiter J, Riviere M, van der Meer WGJ, van Loosdrecht MCM, Kruithof JC. 113.  2010. Impact of flow regime on pressure drop increase and biomass accumulation and morphology in membrane systems. Water Res. 44:689–702 [Google Scholar]
  114. Walker GM, Ozers MS, Beebe DJ. 114.  2004. Cell infection within a microfluidic device using virus gradients. Sens. Actuators B 98:347–55 [Google Scholar]
  115. Wang P, Robert L, Pelletier J, Dang WL, Taddei F. 115.  et al. 2010. Robust growth of Escherichia coli. Curr. Biol. 20:1099–103 [Google Scholar]
  116. Weibel DB, Diluzio WR, Whitesides GM. 116.  2007. Microfabrication meets microbiology. Nat. Rev. Microbiol. 5:209–18 [Google Scholar]
  117. Weibel DB, Garstecki P, Ryan D, DiLuzio WR, Mayer M. 117.  et al. 2005. Microoxen: microorganisms to move microscale loads. Proc. Natl. Acad. Sci. USA 102:11963–67 [Google Scholar]
  118. Wessel AK, Hmelo L, Parsek MR, Whiteley M. 118.  2013. Going local: technologies for exploring bacterial microenvironments. Nat. Rev. Microbiol. 11:337–48 [Google Scholar]
  119. Whitesides GM. 119.  2006. The origins and the future of microfluidics. Nature 442:368–73 [Google Scholar]
  120. Wu H, Huang B, Zare RN. 120.  2006. Generation of complex, static solution gradients in microfluidic channels. J. Am. Chem. Soc. 128:4194–95 [Google Scholar]
  121. Xu N, Zhang Z-F, Wang L, Gao B, Pang D-W. 121.  et al. 2012. A microfluidic platform for real-time and in situ monitoring of virus infection process. Biomicrofluidics 6:034122 [Google Scholar]
  122. Yazdi S, Ardekani AM. 122.  2012. Bacterial aggregation and biofilm formation in a vortical flow. Biomicrofluidics 6:044114 [Google Scholar]
  123. Yawata Y, Cordero OX, Menolascina F, Hehemann J-H, Polz MF, Stocker R. 123.  2014. A competition-dispersal trade-off ecologically differentiates recently speciated marine bacterioplankton populations. Proc. Natl. Acad. Sci. 1115622–27 [Google Scholar]
  124. Zare RN, Kim S. 124.  2010. Microfluidic platforms for single-cell analysis. Annu. Rev. Biomed. Eng. 12:187–201 [Google Scholar]
  125. Zhang Q, Lambert G, Liao D, Kim H, Robin K. 125.  et al. 2011. Acceleration of emergence of bacterial antibiotic resistance in connected microenvironments. Science 333:1764–67Connected microhabitats exposed to an antibiotic gradient create the conditions for the rapid evolution of resistant mutants. [Google Scholar]
  126. Zhu X, Si G, Deng N, Ouyang Q, Wu T. 126.  et al. 2012. Frequency-dependent Escherichia coli chemotaxis behavior. Phys. Rev. Lett. 108:128101 [Google Scholar]
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