Experimental verification of the behavioral foundation of bacterial transport parameters using microfluidics

Biophysical Journal

Volumn 95, Issue 9, 2008, Pages 4481-4493

  Ahmed, Tanvir ^a   Stocker, Roman ^a  

^a Massachusetts Institute of Technology Cambridge   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOTACTIC FACTOR;

ARTICLE; CHEMOTAXIS; CYTOLOGY; DRUG EFFECT; ESCHERICHIA COLI; MICROFLUIDIC ANALYSIS; PHYSIOLOGY; TIME;

CHEMOTACTIC FACTORS; CHEMOTAXIS; ESCHERICHIA COLI; MICROFLUIDIC ANALYTICAL TECHNIQUES; TIME FACTORS;

EID: 55149108941     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1529/biophysj.108.134510     Document Type: Article

References (80)

1. Koyama, S., D. Amarie, H. A. Soini, M. V. Novotny, and S. C. Jacobson. 2006. Chemotaxis assays of mouse sperm on microfluidic devices. Anal. Chem. 78:3354-3359.
2. Fauci, L. J., and R. Dillon. 2006. Biofluidmechanics of reproduction. Annu. Rev. Fluid Mech. 38:371-394.
3. Pratt, L. A., and R. Kolter. 1998. Genetic analysis of Escherichia coli biofilm formation: roles of flagella, motility, chemotaxis and type I pili. Mol. Microbiol. 30:285-293.
4. O'Toole, G., H. B. Kaplan, and R. Kolter. 2000. Biofilm formation as microbial development. Annu. Rev. Microbiol. 54:49-79.
5. Duffy, K. J., R. M. Ford, and P. T. Cummings. 1997. Residence time calculation for chemotactic bacteria within porous media. Biophys. J. 73:2930-2936.
6. Barton, J. W., and R. M. Ford. 1997. Mathematical model for characterization of bacterial migration through sand cores. Biotechnol. Bioeng. 53:487-496.
7. Lanning, L. M., and R. M. Ford. 2002. Glass micromodel study of bacterial dispersion in spatially periodic porous networks. Biotechnol. Bioeng. 78:556-566.
8. Mai, U. E. H., G. I. Perezperez, J. B. Allen, S. M. Wahl, M. J. Blaser, and P. D. Smith. 1992. Surface-proteins from Helicobacter pylori exhibit chemotactic activity for human-leukocytes and are present in gastric-mucosa. J. Exp. Med. 175:517-525.
9. Moens, S., and J. Vanderleyden. 1996. Functions of bacterial flagella. Crit. Rev. Microbiol. 22:67-100.
10. Ottemann, K. M., and A. C. Lowenthal. 2002. Helicobacter pylori uses motility for initial colonization and to attain robust infection. Infect. Immun. 70:1984-1990.
11. Kiorboe, T., and G. A. Jackson. 2001. Marine snow, organic solute plumes, and optimal chemosensory behavior of bacteria. Limnol. Oceanogr. 46:1309-1318.
12. Jackson, G. A. 1989. Simulation of bacterial attraction and adhesion to falling particles in an aquatic environment. Limnol. Oceanogr. 34:514-530.
13. Jackson, G. A. 1987. Simulating chemosensory responses of marine organisms. Limnol. Oceanogr. 32:1253-1266.
14. Azam, F., and F. Malfatti. 2007. Microbial structuring of marine ecosystems. Nat. Rev. Microbiol. 5:782-791.
15. Azam, F., and R. A. Long. 2001. Oceanography - sea snow microcosms. Nature. 414:495-498.
16. Berg, H. C. 1983. Random Walks in Biology. Princeton University Press, Princeton, NJ.
17. Berg, H. C., and D. A. Brown. 1972. Chemotaxis in Escherichia coli analysed by three-dimensional tracking. Nature. 239:500-504.
18. Macnab, R. M., and D. E. Koshland. 1972. Gradient sensing mechanism in bacterial chemotaxis. Proc. Natl. Acad. Sci. USA. 69:2509-2512.
19. Segall, J. E., S. M. Block, and H. C. Berg. 1986. Temporal comparisons in bacterial chemotaxis. Proc. Natl. Acad. Sci. USA. 83:8987-8991.
20. Keller, E. F., and L. A. Segel. 1971. Model for chemotaxis. J. Theor. Biol. 30:225-234.
21. Adler, J. 1973. Method for measuring chemotaxis and use of method to determine optimum conditions for chemotaxis by Escherichia coli. J. Gen. Microbiol. 74:77-91.
22. Marx, R. B., and M. D. Aitken. 1999. Quantification of chemotaxis to naphthalene by Pseudomonas putida G7. Appl. Environ. Microbiol. 65:2847-2852.
23. Lewus, P., and R. M. Ford. 1999. Temperature-sensitive motility of Sulfolobus acidocaldarius influences population distribution in extreme environments. J. Bacteriol. 181:4020-4025.
24. Vicker, M. G. 1981. Ideal and nonideal concentration gradient propagation in chemotaxis studies. Exp. Cell Res. 136:91-100.
25. Ford, R. M., B. R. Phillips, J. A. Quinn, and D. A. Lauffenburger. 1991. Measurement of bacterial random motility and chemotaxis coefficients: I. Stopped flow diffusion chamber assay. Biotechnol. Bioeng. 37:647-660.
26. Holz, M., and S. H. Chen. 1979. Spatio-temporal structure of migrating chemotactic band of Escherichia coli. I. Traveling band profile. Biophys. J. 26:243-261.
27. Zaval'skii, L. Y., A. I. Marchenko, and R. V. Borovik. 2003. The study of bacterial chemotaxis to naphthalene. Microbiology. 72:363-368.
28. Rivero, M. A., R. T. Tranquillo, H. M. Buettner, and D. A. Lauffenburger. 1989. Transport models for chemotactic cell-populations based on individual cell behavior. Chem. Eng. Sci. 44:2881-2897.
29. Othmer, H. G., S. R. Dunbar, and W. Alt. 1988. Models of dispersal in biological systems. J. Math. Biol. 26:263-298.
30. Farrell, B. E., R. P. Daniele, and D. A. Lauffenburger. 1990. Quantitative relationships between single-cell and cell-population model parameters for chemosensory migration responses of alveolar macrophages to C5a. Cell Motil. Cytoskeleton. 16:279-293.
31. Whitesides, G. M., E. Ostuni, S. Takayama, X. Y. Jiang, and D. E. Ingber. 2001. Soft lithography in biology and biochemistry. Annu. Rev. Biomed. Eng. 3:335-373.
32. Weibel, D. B., W. R. DiLuzio, and G. M. Whitesides. 2007. Microfabrication meets microbiology. Nat. Rev. Microbiol. 5:209-218.
33. Saadi, W., S. J. Wang, F. Lin, and N. L. Jeon. 2006. A parallel-gradient microfluidic chamber for quantitative analysis of breast cancer cell chemotaxis. Biomed. Microdevices. 8:109-118.
34. Walker, G. M., J. Q. Sai, A. Richmond, M. Stremler, C. Y. Chung, and J. P. Wikswo. 2005. Effects of flow and diffusion on chemotaxis studies in a microfabricated gradient generator. Lab Chip. 5:611-618.
35. Mao, H. B., P. S. Cremer, and M. D. Manson. 2003. A sensitive, versatile microfluidic assay for bacterial chemotaxis. Proc. Natl. Acad. Sci. USA. 100:5449-5454.
36. Jeon, N. L., H. Baskaran, S. K. W. Dertinger, G. M. Whitesides, L. Van de Water, and M. Toner. 2002. Neutrophil chemotaxis in linear and complex gradients of interleukin-8 formed in a microfabricated device. Nat. Biotechnol. 20:826-830.
37. Chung, B. G., F. Lin, and N. L. Jeon. 2006. A microfluidic multi-injector for gradient generation. Lab Chip. 6:764-768.
38. Irimia, D., and M. Toner. 2006. Cell handling using microstructured membranes. Lab Chip. 6:345-352.
39. Cheng, S. Y., S. Heilman, M. Wasserman, S. Archer, M. L. Shuler, and M. M. Wu. 2007. A hydrogel-based microfluidic device for the studies of directed cell migration. Lab Chip. 7:763-769.
40. Diao, J. P., L. Young, S. Kim, E. A. Fogarty, S. M. Heilman, P. Zhou, M. L. Shuler, M. M. Wu, and M. P. DeLisa. 2006. A three-channel microfluidic device for generating static linear gradients and its application to the quantitative analysis of bacterial chemotaxis. Lab Chip. 6:381-388.
41. Lanning, L. M., R. M. Ford, and T. Long. 2008. Bacterial chemotaxis transverse to axial flow in a microfluidic channel. Biotechnol. Bioeng. 100:653-663.
42. Chen, K. C., R. M. Ford, and P. T. Cummings. 1998. Perturbation expansion of Alt's cell balance equations reduces to Segel's one-dimensional equations for shallow chemoattractant gradients. SIAM J. Appl. Math. 59:35-57.
43. Ford, R. M., and P. T. Cummings. 1992. On the relationship between cell balance-equations for chemotactic cell-populations. SIAM J. Appl. Math. 52:1426-1441.
44. Mesibov, R., G. W. Ordal, and J. Adler. 1973. Range of attractant concentrations for bacterial chemotaxis and threshold and size of response over this range - Weber law and related phenomena. J. Gen. Physiol. 62:203-223.
45. Berg, H. C., and P. M. Tedesco. 1975. Transient response to chemotactic stimuli in Escherichia coli. Proc. Natl. Acad. Sci. USA. 72:3235-3239.
46. Lewus, P., and R. M. Ford. 2001. Quantification of random motility and chemotaxis bacterial transport coefficients using individual-cell and population-scale assays. Biotechnol. Bioeng. 75:292-304.
47. Stocker, R., J. R. Seymour, A. Samadani, D. E. Hunt, and M. F. Polz. 2008. Rapid chemotactic response enables marine bacteria to exploit ephemeral microscale nutrient patches. Proc. Natl. Acad. Sci. USA. 105:4209-4214.
48. Wright, S., B. Walia, J. S. Parkinson, and S. Khan. 2006. Differential activation of Escherichia coli chemoreceptors by blue-light stimuli. J. Bacteriol. 188:3962-3971.
49. Law, A. M. J., and M. D. Aitken. 2005. Continuous-flow capillary assay for measuring bacterial chemotaxis. Appl. Environ. Microbiol. 71:3137-3143.
50. Dahlquist, F. W., R. A. Elwell, and P. S. Lovely. 1976. Studies of bacterial chemotaxis in defined concentration gradients - model for chemotaxis toward L-serine. J. Supramol. Struct. 4:329-342.
51. Dahlquist, F., P. Lovely, and D. Koshland. 1972. Quantitative analysis of bacterial migration in chemotaxis. Nat. New Biol. 236:120-123.
52. Block, S. M., J. E. Segall, and H. C. Berg. 1983. Adaptation kinetics in bacterial chemotaxis. J. Bacteriol. 154:312-323.
53. Block, S. M., J. E. Segall, and H. C. Berg. 1982. Impulse responses in bacterial chemotaxis. Cell. 31:215-226.
54. Ford, R. M., and D. A. Lauffenburger. 1991. Measurement of bacterial random motility and chemotaxis coefficients: II. Application of single-cell-based mathematical model. Biotechnol. Bioeng. 37:661-672.
55. Packer, H. L., and J. P. Armitage. 1994. The chemokinetic and chemotactic behavior of Rhodobacter sphaeroides - 2 independent responses. J. Bacteriol. 176:206-212.
56. Zhulin, I. B., and J. P. Armitage. 1993. Motility, chemokinesis, and methyl ation-independent chemotaxis in Azospirillum brasilense. J. Bacteriol. 175:952-958.
57. Wu, M. M., J. W. Roberts, S. Kim, D. L. Koch, and M. P. DeLisa. 2006. Collective bacterial dynamics revealed using a three-dimensional population-scale defocused particle tracking technique. Appl. Environ. Microbiol. 72:4987-4994.
58. Sheng, J., E. Malkiel, J. Katz, J. Adolf, R. Belas, and A. R. Place. 2007. Digital holographic microscopy reveals prey-induced changes in swimming behavior of predatory dinoflagellates. Proc. Natl. Acad. Sci. USA. 104:17512-17517.
59. Zhao, B., J. S. Moore, and D. J. Beebe. 2001. Surface-directed liquid flow inside microchannels. Science. 291:1023-1026.
60. Armitage, J. P. 1997. Behavioural responses of bacteria to light and oxygen. Arch. Microbiol. 168:249-261.
61. Wellman, A. M., and H. W. Paerl. 1981. Rapid chemotaxis assay using radioactively labeled bacterial cells. Appl. Environ. Microbiol. 42:216-221.
62. Marx, R. B., and M. D. Aitken. 2000. A material-balance approach for modeling bacterial chemotaxis to a consumable substrate in the capillary assay. Biotechnol. Bioeng. 68:308-315.
63. Marcos, and R. Stocker. 2006. Microorganisms in vortices: a microfluidic setup. Limnol. Oceanogr. 4:392-398.
64. Jeffery, G. B. 1922. The motion of ellipsoidal particles immersed in a viscous fluid. Proc. Roy. Soc. Lond. 120:161-179.
65. Wu, L., G. P. Li, W. Xu, and M. Bachman. 2006. Droplet formation in microchannels under static conditions. Appl. Phys. Lett. 89:144106.
66. Liu, Z. W., and K. D. Papadopoulos. 1995. Unidirectional motility of Escherichia coli in restrictive capillaries. Appl. Environ. Microbiol. 61:3567-3572.
67. Berg, H. C., and L. Turner. 1990. Chemotaxis of bacteria in glass-capillary arrays. Biophys. J. 58:919-930.
68. Biondi, S. A., J. A. Quinn, and H. Goldfine. 1998. Random motility of swimming bacteria in restricted geometries. AIChE J. 44:1923-1929.
69. Lauga, E., W. R. DiLuzio, G. M. Whitesides, and H. A. Stone. 2006. Swimming in circles: motion of bacteria near solid boundaries. Biophys. J. 90:400-412.
70. DiLuzio, W. R., L. Turner, M. Mayer, P. Garstecki, D. B. Weibel, H. C. Berg, and G. M. Whitesides. 2005. Escherichia coli swim on the right-hand side. Nature. 435:1271-1274.
71. Frymier, P. D., and R. M. Ford. 1997. Analysis of bacterial swimming speed approaching a solid-liquid interface. AIChE J. 43:1341-1347.
72. Frymier, P. D., R. M. Ford, H. C. Berg, and P. T. Cummings. 1995. 3-Dimensional tracking of motile bacteria near a solid planar surface. Proc. Natl. Acad. Sci. USA. 92:6195-6199.
73. Hill, J., O. Kalkanci, J. L. McMurry, and H. Koser. 2007. Hydrodynamic surface interactions enable Escherichia coli to seek efficient routes to swim upstream. Phys. Rev. Lett. 98:068101.
74. Ramia, M., D. L. Tullock, and N. Phanthien. 1993. The role of hydrodynamic interaction in the locomotion of microorganisms. Biophys. J. 65:755-778.
75. Korobkova, E., T. Emonet, J. M. G. Vilar, T. S. Shimizu, and P. Cluzel. 2004. From molecular noise to behavioural variability in a single bacterium. Nature. 428:574-578.
76. Nilson, J. H. 2001. Editorial - A growing partnership between structural biology and molecular endocrinology. Mol. Endocrinol. 15:351-352.
77. Fenchel, T., and N. Blackburn. 1999. Motile chemosensory behaviour of phagotrophic protists: mechanisms for and efficiency in congregating at food patches. Protist. 150:325-336.
78. Barbara, G. M., and J. G. Mitchell. 2003. Bacterial tracking of motile algae. FEMS Microbiol. Ecol. 44:79-87.
79. Brown, D. A., and H. C. Berg. 1974. Temporal stimulation of chemotaxis in Escherichia coli. Proc. Natl. Acad. Sci. USA. 71:1388-1392.
80. Strauss, I., P. D. Frymier, C. M. Hahn, and R. M. Ford. 1995. Analysis of bacterial migration: II. Studies with multiple attractant gradients. AIChE J. 41:402-414.