Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Live from under the lens: exploring microbial motility with dynamic imaging and microfluidics

Nature Reviews Microbiology volume 13, pages 761–775 (2015)Cite this article

Subjects

Key Points

  • Motility is one of the most dynamic features of the microbial world. The ability to swim in liquid or crawl on surfaces frequently governs how microorganisms interact with their physical and chemical environment, and underpins a myriad of microbial processes.

  • The ability to resolve temporal dynamics through time-lapse imaging and the precise control of the physicochemical microenvironment afforded by microfluidics offer powerful new opportunities to study the motility adaptations of microorganisms and thereby further our understanding of their ecology.

  • Dynamic microscale imaging has shown how individual swimming microorganisms disturb the fluid in their surroundings, and how this hydrodynamic signature affects their motility near surfaces as well as in dense-cell suspensions. The same technique has revealed new motility adaptations of microorganisms, in particular the flicking behaviour used by many marine bacteria to turn.

  • Tracking swimming microorganisms in precisely controlled chemical gradients created using microfluidic devices has revealed that microorganisms are capable of refined rescaling responses in their chemotactic behaviour, which ensure high performance under a wide range of environmental conditions. In the environment, and in particular in the ocean, the strong chemotactic responses of microorganisms can be important in determining associations with larger organisms, consuming dissolved organic matter and ultimately affecting biogeochemistry.

  • An important but often neglected set of microbial interactions are those between cells and their physical environment — chiefly, surfaces and fluid flow. Recent imaging-based microfluidic studies have revealed that hydrodynamic and surface-induced forces can strongly bias the direction of migration of microorganisms. These forces, for example, induce upstream swimming or preferential cell accumulations in regions of high-velocity gradients, affecting the transport of microorganisms and the colonization of surfaces that leads to biofilm formation.

Abstract

Motility is one of the most dynamic features of the microbial world. The ability to swim or crawl frequently governs how microorganisms interact with their physical and chemical environments, and underpins a myriad of microbial processes. The ability to resolve temporal dynamics through time-lapse video microscopy and the precise control of the physicochemical microenvironment afforded by microfluidics offer powerful new opportunities to study the many motility adaptations of microorganisms and thereby further our understanding of their ecology. In this Review, we outline recent insights into the motility strategies of microorganisms brought about by these techniques, including the hydrodynamic signature of microorganisms, their locomotion mechanics, chemotaxis, their motility near and on surfaces, swimming in moving fluids and motility in dense microbial suspensions.

This is a preview of subscription content, access via your institution

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Learn more

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Microbial flow fields and motility mechanics.
Figure 2: Microbial chemotaxis.
Figure 3: Microbial interactions with surfaces.
Figure 4: Microbial motility in moving fluids.
Figure 5: Upstream motility and downstream bending in flowing fluids.

Similar content being viewed by others

References

  1. Xie, L., Altindal, T., Chattopadhyay, S. & Wu, X.-L. Bacterial flagellum as a propeller and as a rudder for efficient chemotaxis. Proc. Natl Acad. Sci. USA 108, 2246–2251 (2011). This study reported the discovery of the 'flick', a new reorientation mechanism found among marine bacteria, which makes their motility drastically different from the run-and-tumble motility observed in E. coli.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Son, K., Guasto, J. S. & Stocker, R. Bacteria can exploit a flagellar buckling instability to change direction. Nat. Phys. 9, 494–498 (2013).

    Article  CAS  Google Scholar 

  3. Zhao, K. et al. Psl trails guide exploration and microcolony formation in Pseudomonas aeruginosa biofilms. Nature 497, 388–391 (2013). This study mapped the chemical trails of individual bacteria on a surface, demonstrating that matrix-rich regions are self-reinforcing and form the skeleton of biofilms.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Wang, P. et al. Robust growth of Escherichia coli. Curr. Biol. 20, 1099–1103 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Zhang, Q. et al. Acceleration of emergence of bacterial antibiotic resistance in connected microenvironments. Science 333, 1764–1767 (2011).

    Article  CAS  PubMed  Google Scholar 

  6. 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. USA 108, 12617–12622 (2011). This study revealed that P. aeruginosa twitching on surfaces are capable of a rapid slingshot motion that can efficiently reorient cells.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Gibiansky, M. L. et al. Bacteria use type IV pili to walk upright and detach from surfaces. Science 330, 197 (2010).

    Article  CAS  PubMed  Google Scholar 

  8. Persat, A., Stone, H. A. & Gitai, Z. The curved shape of Caulobacter crescentus enhances surface colonization in flow. Nat. Commun. 5, 3824 (2014).

    Article  CAS  PubMed  Google Scholar 

  9. Hol, F. J. H. & Dekker, C. Zooming in to see the bigger picture: microfluidic and nanofabrication tools to study bacteria. Science 346, 1251821 (2014).

    Article  PubMed  CAS  Google Scholar 

  10. Sackmann, E. K., Fulton, A. L. & Beebe, D. J. The present and future role of microfluidics in biomedical research. Nature 507, 181–189 (2014).

    CAS  PubMed  Google Scholar 

  11. Rusconi, R., Garren, M. & Stocker, R. Microfluidics expanding the frontiers of microbial ecology. Annu. Rev. Biophys. 43, 65–91 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Wessel, A. K., Hmelo, L., Parsek, M. R. & Whiteley, M. Going local: technologies for exploring bacterial microenvironments. Nat. Rev. Microbiol. 11, 337–348 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Guasto, J. S., Rusconi, R. & Stocker, R. Fluid mechanics of planktonic microorganisms. Annu. Rev. Fluid Mech. 44, 373–400 (2012).

    Article  Google Scholar 

  14. Elgeti, J., Winkler, R. G. & Gompper, G. Physics of microswimmers-single particle motion and collective behavior: a review. Rep. Prog. Phys. 78, 056601 (2015).

    Article  CAS  PubMed  Google Scholar 

  15. Drescher, K., Dunkel, J., Cisneros, L. H., Ganguly, S. & Goldstein, R. E. Fluid dynamics and noise in bacterial cell–cell and cell–surface scattering. Proc. Natl Acad. Sci. USA 108, 10940–10945 (2011). This study reported the first experimental quantification of the flow field around a single swimming E. coli bacterium.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Lighthill, M. J. Mathematical Biofluiddynamics (Society for Industrial and Applied Mathematics, 1975).

    Book  Google Scholar 

  17. Wu, X. L. & Liebchaber, A. Particle diffusion in a quasi-two-dimensional bacterial bath. Phys. Rev. Lett. 84, 3017–3020 (2010).

    Article  Google Scholar 

  18. Zhang, H.-P., Be'er, A., Florin, E.-L. & Swinney, H. L. Collective motion and density fluctuations in bacterial colonies. Proc. Natl Acad. Sci. USA 107, 13626–13630 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Dombrowski, C., Cisneros, L., Chatkaew, S., Goldstein, R. E. & Kessler, J. O. Self-concentration and large-scale coherence in bacterial dynamics. Phys. Rev. Lett. 93, 2–5 (2004).

    Article  CAS  Google Scholar 

  20. Berke, A. P., Turner, L., Berg, H. C. & Lauga, E. Hydrodynamic attraction of swimming microorganisms by surfaces. Phys. Rev. Lett. 101, 038102 (2008).

    Article  PubMed  CAS  Google Scholar 

  21. Berg, H. C. E. coli in Motion (Springer, 2004).

    Book  Google Scholar 

  22. Turner, L., Ryu, W. S. & Berg, H. C. Real-time imaging of fluorescent flagellar filaments. J. Bacteriol. 182, 2793–2801 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Stocker, R. Reverse and flick: hybrid locomotion in bacteria. Proc. Natl Acad. Sci. USA 108, 2635–2636 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Leifson, E., Cosenza, B. J., Murchelano, R. & Cleverdon, R. C. Motile marine bacteria I. techniques, ecology, and general characteristics. J. Bacteriol. 87, 652–666 (1964).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Xie, L. & Wu, X. L. Bacterial motility patterns reveal importance of exploitation over exploration in marine microhabitats. part I: theory. Biophys. J. 107, 1712–1720 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Taktikos, J., Stark, H. & Zaburdaev, V. How the motility pattern of bacteria affects their dispersal and chemotaxis. PLoS ONE 8, e81936 (2014).

    Article  CAS  Google Scholar 

  27. Wadhams, G. H. & Armitage, J. P. Making sense of it all: bacterial chemotaxis. Nat. Rev. Mol. Cell. Biol. 5, 1024–1037 (2004).

    Article  CAS  PubMed  Google Scholar 

  28. Tu, Y. H. Quantitative modeling of bacterial chemotaxis: Signal amplification and accurate adaptation. Annu. Rev. Biophys. 42, 337–359 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Stocker, R. & Seymour, J. R. Ecology and physics of bacterial chemotaxis in the ocean. Microbiol. Mol. Biol. Rev. 76, 792–812 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Stocker, R. Marine microbes see a sea of gradients. Science 338, 628–633 (2012).

    Article  CAS  PubMed  Google Scholar 

  31. Ahmed, T., Shimizu, T. S. & Stocker, R. Microfluidics for bacterial chemotaxis. Integr. Biol. 2, 604–629 (2010).

    Article  CAS  Google Scholar 

  32. Kalinin, Y. V., Jiang, L., Tu, Y. & Wu, M. Logarithmic sensing in Escherichia coli bacterial chemotaxis. Biophys. J. 96, 2439–2448 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Fechner, G. T., Adler, H. E., Howes, D. H. & Boring, E. G. Elementary Psychophysics (Holt, 1966).

    Google Scholar 

  34. Rieke, F. & Rudd, M. E. The challenges natural images pose for visual adaptation. Neuron 64, 605–616 (2009).

    Article  CAS  PubMed  Google Scholar 

  35. Lazova, M. D., Ahmed, T., Bellomo, D., Stocker, R. & Shimizu, T. S. Response rescaling in bacterial chemotaxis. Proc. Natl Acad. Sci. USA 108, 13870–13875 (2011). This study revealed experimentally that E. coli is capable of rescaling its chemotactic response, a process termed fold-change detection, which ensures high chemotactic sensitivity across a broad range of environmental conditions.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Zhu, X. et al. Frequency-dependent Escherichia coli chemotaxis behavior. Phys. Rev. Lett. 108, 128101 (2012).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  37. Kalinin, Y., Neumann, S., Sourjik, V. & Wu, M. Responses of Escherichia coli bacteria to two opposing chemoattractant gradients depend on the chemoreceptor ratio. J. Bacteriol. 192, 1796–1800 (2010). This study was the first to use microfluidics to examine the chemotactic decision-making process of E. coli cells that were exposed to two simultaneous chemical gradients.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Blackburn, N. Microscale nutrient patches in planktonic habitats shown by chemotactic bacteria. Science 282, 2254–2256 (1998).

    Article  CAS  PubMed  Google Scholar 

  39. Bell, W. & Mitchell, R. Chemotactic and growth responses of marine bacteria to algal extracellular products. Biol. Bull. 143, 265–277 (1972).

    Article  Google Scholar 

  40. Barbara, G. M. & Mitchell, J. G. Bacterial tracking of motile algae. FEMS Microbiol. Ecol. 44, 79–87 (2003).

    Article  CAS  PubMed  Google Scholar 

  41. Stocker, R., Seymour, J. R., Samadani, A., Hunt, D. E. & Polz, M. F. Rapid chemotactic response enables marine bacteria to exploit ephemeral microscale nutrient patches. Proc. Natl Acad. Sci. USA 105, 4209–4214 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Seymour, J. R., Ahmed, T., Durham, W. M. & Stocker, R. Chemotactic response of marine bacteria to the extracellular products of Synechococcus and Prochlorococcus. Aquat. Microb. Ecol. 59, 161–168 (2010).

    Article  Google Scholar 

  43. Seymour, J. R., Ahmed, T. & Stocker, R. Bacterial chemotaxis towards the extracellular products of the toxic phytoplankton Heterosigma akashiwo. J. Plank. Res. 31, 1557–1561 (2009).

    Article  CAS  Google Scholar 

  44. Seymour, J. R., Simó, R., Ahmed, T. & Stocker, R. Chemoattraction to dimethylsulfoniopropionate throughout the marine microbial food web. Science 329, 342–345 (2010).

    Article  CAS  PubMed  Google Scholar 

  45. Garren, M. et al. A bacterial pathogen uses dimethylsulfoniopropionate as a cue to target heat-stressed corals. ISME J. 8, 999–1007 (2014).

    Article  CAS  PubMed  Google Scholar 

  46. Seymour, J. R., Marcos & Stocker, R. Resource patch formation and exploitation throughout the marine microbial food web. Am. Nat. 173, E15–29 (2009).

    Article  CAS  PubMed  Google Scholar 

  47. Barbara, G. M. & Mitchell, J. G. Marine bacterial organisation around point-like sources of amino acids. FEMS Microbiol. Ecol. 43, 99–109 (2003).

    Article  CAS  PubMed  Google Scholar 

  48. Yawata, Y. et al. Competition–dispersal tradeoff ecologically differentiates recently speciated marine bacterioplankton populations. Proc. Natl Acad. Sci. USA 111, 5622–5627 (2014). This study revealed a competition–dispersal tradeoff among recently speciated sympatric marine bacteria, based on distinct behavioural interactions with particulate organic matter.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Persat, A. et al. The mechanical world of bacteria. Cell 161, 988–997 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. O'Toole, G., Kaplan, H. B. & Kolter, R. Biofilm formation as microbial development. Annu. Rev. Microbiol. 54, 49–79 (2000).

    Article  CAS  PubMed  Google Scholar 

  51. Karimi, A., Karig, D., Kumar, A. & Ardekani, A. M. Interplay of physical mechanisms and biofilm processes: review of microfluidic methods. Lab. Chip 15, 23–42 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Watnick, P. & Kolter, R. Biofilm, city of microbes. J. Bacteriol. 182, 2675–2679 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Kearns, D. B. A field guide to bacterial swarming motility. Nat. Rev. Microbiol. 8, 634–644 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Teschler, J. K. et al. Living in the matrix: assembly and control of Vibrio cholerae biofilms. Nat. Rev. Microbiol. 13, 255–268 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Magariyama, Y. et al. Difference in bacterial motion between forward and backward swimming caused by the wall effect. Biophys. J. 88, 3648–3658 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Molaei, M., Barry, M., Stocker, R. & Sheng, J. Failed escape: solid surfaces prevent tumbling of Escherichia coli. Phys. Rev. Lett. 113, 68103 (2014).

    Article  CAS  Google Scholar 

  57. Lauga, E., DiLuzio, W. R., Whitesides, G. M. & Stone, H. A. Swimming in circles: motion of bacteria near solid boundaries. Biophys. J. 90, 400–412 (2006). This study rationalized why many species of bacteria swim in circular trajectories when near a surface.

    Article  CAS  PubMed  Google Scholar 

  58. Utada, A. S. et al. Vibrio cholerae use pili and flagella synergistically to effect motility switching and conditional surface attachment. Nat. Commun. 5, 2913 (2014).

    Article  CAS  Google Scholar 

  59. Conrad, J. C. et al. Flagella and pili-mediated near-surface single-cell motility mechanisms in P. aeruginosa. Biophys. J. 100, 1608–1616 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Rusconi, R. & Stocker, R. Microbes in flow. Curr. Opin. Microbiol. 25, 1–8 (2015).

    Article  PubMed  Google Scholar 

  61. Durham, W. M., Kessler, J. O. & Stocker, R. Disruption of vertical motility by shear triggers formation of thin phytoplankton layers. Science 323, 1067–1070 (2009).

    Article  CAS  PubMed  Google Scholar 

  62. Durham, W. M. et al. Turbulence drives microscale patches of motile phytoplankton. Nat. Commun. 4, 2148 (2013).

    Article  PubMed  CAS  Google Scholar 

  63. Rusconi, R., Guasto, J. S. & Stocker, R. Bacterial transport suppressed by fluid shear. Nat. Phys. 10, 212–217 (2014). This study revealed that the coupling of motility and flow can result in high levels of bacterial accumulation in certain regions of the flow, hampering chemotaxis and favouring surface attachment.

    Article  CAS  Google Scholar 

  64. 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. 98, 68101 (2007).

    Article  CAS  Google Scholar 

  65. Kaya, T. & Koser, H. Direct upstream motility in Escherichia coli. Biophys. J. 102, 1514–1523 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Shen, Y., Siryaporn, A., Lecuyer, S., Gitai, Z. & Stone, H. A. Flow directs surface-attached bacteria to twitch upstream. Biophys. J. 103, 146–151 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Marcos, Fu, H. C., Powers, T. R. & Stocker, R. Bacterial rheotaxis. Proc. Natl Acad. Sci. USA 109, 4780–4785 (2012).

    Article  PubMed  Google Scholar 

  68. Meng, Y. Z. et al. Upstream migration of Xylella fastidiosa via pilus-driven twitching motility. J. Bacteriol. 187, 5560–5567 (2005). This study revealed that bacteria twitching on surfaces migrate upstream in the presence of fluid flow, owing to a hydrodynamic torque that orients them against the flow.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Bures, J. et al. Small intestinal bacterial overgrowth syndrome. World J. Gastroenterol. 16, 2978–2990 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Dunkel, J. et al. Fluid dynamics of bacterial turbulence. Phys. Rev. Lett. 110, 228102 (2013).

    Article  PubMed  CAS  Google Scholar 

  71. Sokolov, A., Goldstein, R., Feldchtein, F. & Aranson, I. Enhanced mixing and spatial instability in concentrated bacterial suspensions. Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 80, 1–8 (2009).

    Article  CAS  Google Scholar 

  72. Saintillan, D. & Shelley, M. J. Active suspensions and their nonlinear models. Comptes Rendus Phys. 14, 497–517 (2013).

    Article  CAS  Google Scholar 

  73. Kaiser, A. et al. Transport powered by bacterial turbulence. Phys. Rev. Lett. 112, 158101 (2014).

    Article  PubMed  CAS  Google Scholar 

  74. Butler, M. T., Wang, Q. & Harshey, R. M. Cell density and mobility protect swarming bacteria against antibiotics. Proc. Natl Acad. Sci. USA 107, 3776–3781 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Sitti, M. Miniature devices: voyage of the microrobots. Nature 458, 1121–1122 (2009).

    Article  CAS  PubMed  Google Scholar 

  76. Mesquita, A. R. & Hespanha, J. P. Jump control of probability densities with applications to autonomous vehicle motion. IEEE T. Automat. Contr. 57, 2588–2598 (2012).

    Article  Google Scholar 

  77. Rubenstein, M., Cornejo, A. & Nagpal, R. Programmable self-assembly in a thousand-robot swarm. Science 345, 795–799 (2014).

    Article  CAS  PubMed  Google Scholar 

  78. Rusconi, R., Lecuyer, S., Guglielmini, L. & Stone, H. A. Laminar flow around corners triggers the formation of biofilm streamers. J. R. Soc. Interface 7, 1293–1299 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  79. Drescher, K., Shen, Y., Bassler, B. L. & Stone, H. A. Biofilm streamers cause catastrophic disruption of flow with consequences for environmental and medical systems. Proc. Natl Acad. Sci. USA 110, 4345–4350 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Malfatti, F. & Azam, F. Atomic force microscopy reveals microscale networks and possible symbioses among pelagic marine bacteria. Aquat. Microb. Ecol. 58, 1–14 (2009).

    Article  Google Scholar 

  81. Kiviet, D. J. et al. Stochasticity of metabolism and growth at the single-cell level. Nature 514, 376–379 (2014).

    Article  CAS  PubMed  Google Scholar 

  82. Rojas, E., Theriot, J. A. & Huang, K. C. Response of Escherichia coli growth rate to osmotic shock. Proc. Natl Acad. Sci. USA 111, 7807–7812 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Brumley, D. R., Wan, K. Y., Polin, M. & Goldstein, R. E. Flagellar synchronization through direct hydrodynamic interactions. eLife 3, e02750 (2014).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  84. Berg, H. C. & Brown, D. A. Chemotaxis in Escherichia coli analyzed by three-dimensional tracking. Nature 239, 500–504 (1972).

    Article  CAS  PubMed  Google Scholar 

  85. Liu, B. et al. Helical motion of the cell body enhances Caulobacter crescentus motility. Proc. Natl Acad. Sci. USA 111, 11252–11256 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Wu, M. M., Roberts, J. W., Kim, S., Koch, D. L. & DeLisa, M. P. Collective bacterial dynamics revealed using a three-dimensional population-scale defocused particle tracking technique. Appl. Environ. Microb. 72, 4987–4994 (2006).

    Article  CAS  Google Scholar 

  87. Taute, K. M., Gude, S., Tans, S. J. & Shimizu, T. S. High-throughput 3D tracking of bacteria on a standard phase contrast microscope. Nat. Commun. 6, 8776 (2015).

    Article  CAS  PubMed  Google Scholar 

  88. Brumley, D. R., Polin, M., Pedley, T. J. & Goldstein, R. E. Metachronal waves in the flagellar beating of Volvox and their hydrodynamic origin. J. R. Soc. Interface. 12, 20141358 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  89. Weibel, D. B., DiLuzio, W. R. & Whitesides, G. M. Microfabrication meets microbiology. Nat. Rev. Microbiol. 5, 209–218 (2007).

    Article  CAS  PubMed  Google Scholar 

  90. Xia, Y. N. & Whitesides, G. M. Soft lithography. Annu. Rev. Mater. Sci. 28, 153–184 (1998).

    Article  CAS  Google Scholar 

  91. Tabeling, P. Introduction to Microfluidics (Oxford Univ. Press, 2005).

    Google Scholar 

  92. Kantsler, V., Dunkel, J., Blayney, M., Goldstein, R. E. & Hyman, A. A. Rheotaxis facilitates upstream navigation of mammalian sperm cells. eLife 3, e02403 (2014).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  93. Kim, S., Kim, H. J. & Jeon, N. L. Biological applications of microfluidic gradient devices. Integr. Biol. 2, 584–603 (2010).

    Article  CAS  Google Scholar 

  94. Adler, M., Erickstad, M., Gutierrez, E. & Groisman, A. Studies of bacterial aerotaxis in a microfluidic device. Lab. Chip 12, 4835–4847 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Wong, I. & Ho, C. M. Surface molecular property modifications for poly(dimethylsiloxane) (PDMS) based microfluidic devices. Microfluid Nanofluid 7, 291–306 (2009).

    Article  CAS  PubMed  Google Scholar 

  96. Cheng, S. Y. et al. A hydrogel-based microfluidic device for the studies of directed cell migration. Lab. Chip 7, 763–769 (2007).

    Article  CAS  PubMed  Google Scholar 

  97. Weibel, D. B. et al. Bacterial printing press that regenerates its ink: Contact-printing bacteria using hydrogel stamps. Langmuir 21, 6436–6442 (2005).

    Article  CAS  PubMed  Google Scholar 

  98. Lauga, E. & Powers, T. R. The hydrodynamics of swimming microorganisms. Rep. Prog. Phys. 72, 096601 (2009).

    Article  Google Scholar 

Download references

Acknowledgements

The authors gratefully acknowledge support through a Samsung Scholarship (to K.S.), a Human Frontier Science Program (HFSP) Cross-Disciplinary Fellowship (to D.R.B.) and a Marine Microbiology Initiative Investigator Award from the Gordon and Betty Moore Foundation (GBMF3783, to R.S.). The authors also thank G. Gorick for help with some of the figures.

Author information

Authors and Affiliations

  1. Department of Mechanical Engineering, Massachusetts Institute of Technology, Cambridge, 02139, Massachusetts, USA

    Kwangmin Son

  2. Department of Civil and Environmental Engineering, Ralph M. Parsons Laboratory, Massachusetts Institute of Technology, Cambridge, 02139, Massachusetts, USA

    Kwangmin Son, Douglas R. Brumley & Roman Stocker

  3. Department of Civil, Environmental and Geomatic Engineering, ETH Zurich, Zurich, 8093, Switzerland

    Douglas R. Brumley & Roman Stocker

Authors
  1. Kwangmin Son
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Douglas R. Brumley
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Roman Stocker
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Roman Stocker.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary information S1 (movie)

Motility mechanics. Many marine bacteria reorient by a 'flick', an off-axis deformation of the flagellum that enables bacteria with a single flagellum to change their direction of swimming. This video shows the flick process of Vibrio alginolyticus (see also Fig. 1c–f), recorded using high-speed, high-intensity dark-field microscopy (40X objective lens, 420 frames s−1). On the left is the raw video, on the right a processed version showing the (single, polar) flagellum in magenta. Note the buckling of the flagellum (see also Fig. 1e, 50–70 ms) shortly after the reversal in swimming direction ( Fig. 1e, 20 ms). This movie is reproduced from Ref. 2, Nature Publishing Group. (MOV 8234 kb)

Supplementary information S2 (movie)

Chemotaxis. Using chemotaxis, natural marine bacteria can cluster around photosynthetic diatoms, here Chaetoceros affinis, in response to the gradients in dissolved organic matter originating from the diatom (see also Fig. 2a). Courtesy of Steven Smriga and Vicente Fernandez, Department of Civil, Environmental and Geomatic Engineering, ETH Zurich, 8093 Zurich, Switzerland. (MOV 1950 kb)

Supplementary information S3 (movie)

Surface motility. Two-point tracking of a single Pseudomonas aeruginosa bacterium as it crawls along a surface (see also Fig. 3d). Markers 1 and 2 represent the leading and trailing poles, respectively. The video corresponds to 700 s in real time, with playback sped up by a factor of 40. This movie is reproduced with permission from Ref. 6, National Academy of Sciences. (AVI 6123 kb)

Supplementary information S4 (movie)

Motility in flow. Trajectory of a smooth-swimming Bacillus subtilis bacterium in a microfluidic channel (see also Fig. 4b). The raw video of the motile cell is shown first, followed by a replay in which the tracked cell trajectory (green) and position and orientation (red) are included. The flow in the channel is from left to right, and the video is recorded in the reference frame comoving with the mean speed of the flow (mean speed = 500 μm s−1, mean absolute shear rate = 2.5 s−1). The looped trajectory results from the velocity gradient generating a hydrodynamic torque that continually reorients the cell while it swims. The video was captured at 70.6 frames s−1 using dark-field microscopy, and is replayed 1.7 times slower than real time. This movie is reproduced from Ref. 63, Nature Publishing Group. (AVI 452 kb)

PowerPoint slides

Glossary

Soft lithography

A technique used for fabricating, at the micrometre to nanometre scale, features in elastomeric materials such as polydimethylsiloxane (PDMS).

Defocused microscopy

A microscopic imaging technique whereby the distance of a microorganism ('into the plane') from the imaging plane is determined by matching its defocused ring size with a reference stack.

Particle image velocimetry

(PIV). A method to measure the velocity field of a fluid based on the motion of many small passive tracer particles.

Thermal fluctuations

A source of random noise in a system at equilibrium that induces diffusion of small particles.

Rotational diffusion

For a swimming microorganism, this describes the continuous, random changes in swimming direction owing to thermal fluctuations (passive rotational diffusion) or to intrinsic imperfections (for example, wobbling) in the locomotion system (termed active rotational diffusion).

Buckling

A sudden sideways failure of a structure subjected to compressive load.

Logarithmic sensing

A sensing property in which cells respond to the relative gradient in a stimulus, ∇C/C, in which C is the magnitude and ∇C is the gradient magnitude of the stimulus.

Förster resonance energy transfer

(FRET). A mechanism quantifying energy transfer between two light-sensitive molecules in which excitation is transferred from a donor molecule to an acceptor molecule without emission of a photon. In chemotactic transduction studies of Escherichia coli, FRET is used to measure the level of the chemotaxis signalling molecule phospho-CheY (CheYP) that controls flagellar reversals.

Chemokinesis

The modulation of swimming speed in response to changes in the concentration of a chemical.

Twitching

Crawling motion of bacteria on surfaces by means of pili.

Digital holographic microscopy

A microscopic imaging technique where the position of an object 'into the plane' is encoded by the interference fringes it creates by diffracting light and can be reconstructed in post-processing to yield 3D information.

Torque

The moment of the forces that act on an object, which quantifies their tendency to rotate the object.

Mannose-sensitive haemagglutinin pili

(MSHA pili). One of three type IV pili, which play an important part in biofilm formation.

Type IV pili

Thin, hair-like appendages present on the surface of many bacteria, involved in adherence to and motility on substrates.

Jeffery orbit

Periodic rotational trajectory of an elongated particle (in this case, a microorganism) in a fluid velocity gradient, in which the angular speed varies with orientation relative to the flow.

Laminar flow

Fluid motion devoid of turbulence and typically occurring as a smooth, orderly flow.

Biofilm streamers

Conglomerates of cells and cell-secreted polymeric substances (exopolysaccharide) that are attached by one end to a surface and otherwise suspended in the flow. These biofilm structures exist in topographically complex environments exposed to fluid flow.

Rights and permissions

Reprints and Permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Son, K., Brumley, D. & Stocker, R. Live from under the lens: exploring microbial motility with dynamic imaging and microfluidics. Nat Rev Microbiol 13, 761–775 (2015). https://doi.org/10.1038/nrmicro3567

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nrmicro3567

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing