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Analysis of chemotactic bacterial distributions in population migration assays using a mathematical model applicable to steep or shallow attractant gradients

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Abstract

The mathematical model developed by Riveroet al. (1989,Chem. Engng Sci. 44, 2881–2897) is applied to literature data measuring chemotactic bacterial population distributions in response to steep as well as shallow attractant gradients. This model is based on a fundamental picture of the sensing and response mechanisms of individual bacterial cells, and thus relates individual cell properties such as swimming speed and tumbling frequency to population parameters such as the random motility coefficient and the chemotactic sensitivity coefficient. Numerical solution of the model equations generates predicted bacterial density and attractant concentration profiles for any given experimental assay. We have previously validated the mathematical model from experimental work involving a step-change in the attractant gradient (Fordet al., 1991Biotechnol. Bioengng.37, 647–660; For and Lauffenburger, 1991,Biotechnol. Bioengng,37, 661–672). Within the context of this experimental assay, effects of attractant diffusion and consumption, random motility, and chemotactic sensitivity on the shape of the profiles are explored to enhance our understanding of this complex phenomenon. We have applied this model to various other types of gradients with successful intepretation of data reported by Dalquistet al. (1972,Nature New Biol. 236, 120–123) forSalmonella typhimurum validating the mathematical model and supportin the involvement of high and low affinity receptors for serine chemotaxis by these cells.

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Literature

  • Adler, J. 1966. Chemotaxis in bacteria.Science 153, 708–716.

    Google Scholar 

  • Adler, J. 1973. A method for measuring chemotaxis and use of the method to determine optimum conditions for chemotaxis byEscherichia coli.J. gen. Microbiol. 74, 77–91.

    Google Scholar 

  • Adler, J. and B. Templeton. 1967. The effect of environmental conditions on the motility ofE. coli.J. gen. Microbiol. 46, 175–184.

    Google Scholar 

  • Alt, W. 1980. Biased random walk models for chemotaxis and related diffusion approximations.J. math. Biol. 9, 147–177.

    Article  MATH  MathSciNet  Google Scholar 

  • Armitage, J. P., A. Gallagher and A. W. B. Johnston. 1988. Comparison of the chemotactic behaviour ofRhizobium leguminosarium with and without the nodulation plasmid.Molec. Microbiol. 2, 743–748.

    Google Scholar 

  • Baracchini, O. and J. C. Sherris, 1959. The chemotactic effect of oxygen on bacteria.J. Pathol. Bacteriol. 77, 565–574.

    Article  Google Scholar 

  • Berg, H. C. 1983.Random Walks in Biology. Princeton: Princeton University Press.

    Google Scholar 

  • Berg, H. C. and D. A. Brown. 1972. Chemotaxis inEscherichia coli analyzed by three-dimensional tracking.Nature 239, 500–504.

    Article  Google Scholar 

  • Beyerinck, M. W. 1893. Ueber atmungsfiguren beweglicher bakterien.Zentr. Bakteriol. Parasitenk. 14, 827–845.

    Google Scholar 

  • Bird, R. B. W. E. Stewart and E. N. Lightfoot. 1960.Transport Phenomenon. New York: John Wiley.

    Google Scholar 

  • Boon, J.-P. and B. Herpigny. 1986. Model for chemotactic bacterial bands.Bull. math. Biol. 48, 1–19.

    Article  MATH  Google Scholar 

  • Chet, I. and R. Mitchell. 1976. Ecological aspects of microbial chemotactic behavior.Ann. Rev. Microbiol. 30, 221–239.

    Article  Google Scholar 

  • Chet, I., P. Asketh and R. Mitchell. 1975. Repulsion of bacteria from marine surfaces.Appl. Microbiol. 30, 1043–1045.

    Google Scholar 

  • Clarke, S. and D. E. Koshland, Jr. 1979. Membrane receptors for aspartate and serine in bacterial chemotaxis.J. biol. Chem. 254, 9695–9702.

    Google Scholar 

  • Dalquist, F. W., P. Lovely and D. E. Koshland, Jr. 1972. Quantitative analysis of bacterial migration in chemotaxis.Nature New Biol. 236, 120–123.

    Article  Google Scholar 

  • Dalquist, F. W., R. A. Elwell and P. S. Lovely. 1976. Studies of bacterial chemotaxis in defined concentration gradients.J. supramolec. Struct. 4, 329–342.

    Article  Google Scholar 

  • Douglas, J., Jr. and B. F. Jones, Jr. 1963. On predictor-corrector methods for nonlinear parabolic differential equations.J. Soc. indust. appl. Math. 11, 195–204.

    Article  MATH  MathSciNet  Google Scholar 

  • Englemann, T. W. 1881. Neue Methode zur Untersuchung der Sauerstoffaussheidung pflanzlicher und thierischer Organismen.Pfluegers Arch. ges. Physiol. Menschen Tiere 25, 285–292.

    Article  Google Scholar 

  • Ford, R. M. 1989. Quantitative studies of bacterial motility and chemotaxis using a stopped-flow diffusion chamber assay and an individual cell-based mathematical model. Ph.D. Dissertation, University of Pennsylvania.

  • 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. Bioengng 37, 661–672.

    Article  Google Scholar 

  • Ford, R. M., J. A. Quinn, B. R. Phillips and D. A. Lauffenburger. 1991. Measurement of bacterial random motility and chemotaxis coefficients: I. Stopped-flow diffusion chamber assay.Biotechnol. Bioengng 37 647–660.

    Article  Google Scholar 

  • Freter, R., P. C. M. O’Brien and M. S. Macsai. 1979. Effect of chemotaxis on the interaction ofCholera vibrios with intestinal mucosa.Am. J. clin. Nutrition 32, 128–132.

    Google Scholar 

  • Gristina, A. G. 1987. Biomaterial-centered infection: microbial adhesion versus tissue integration.Science 237, 1588–1595.

    Google Scholar 

  • Gulash, M., P. Ames, R. C. Larosiliere and K. Bergman. 1984.Rhizobia are attracted to localized site on legume roots.Appl. environ. Microbiol. 48, 149–152.b

    Google Scholar 

  • Holz, M. and S.-H. Chen. 1979 Spatio-temporal structure of migrating chemotactic band ofEscherichia coli. I. Traveling band profile.Biophys. J. 26, 243–262.

    Google Scholar 

  • Keller, E. F. and L. A. Segel 1971a. Model for chemotaxis.J. theor. Biol. 30, 225–234.

    Article  Google Scholar 

  • Keller, E. F. and L. A. Segel. 1971b. Traveling bands of chemotactic bacteria: a theoretical analysis.J. theor. Biol. 30 235–248.

    Article  Google Scholar 

  • Kelly, F. X., K. Dapsis and D. Lauffenburger. 1988. Effect of bacterial chemotaxis on dynamics of microbial competition.Microbial Ecol. 16, 115–131.

    Article  Google Scholar 

  • Kennedy, M. J. and J. G. Lawless. 1985. Role of chemotaxis in the ecology of denitrifiers.Appl. environ. Microbiol. 49, 109–114.

    Google Scholar 

  • Koshland, D. E., Jr. 1988. Chemotaxis as a model second-messenger system.Biochemistry 27, 5829–5834.

    Article  Google Scholar 

  • Lapidus, I. R. and R. Schiller. 1976. A model for the chemotactic response of a bacterial population.Biophys. J. 16, 779–789.

    Google Scholar 

  • Lapidus, I. R. and R. Schiller. 1978. A model for traveling bands of chemotactic bacteria.Biophys. J. 22, 1–13.

    Google Scholar 

  • Lauffenburger, D. A. 1988. Laboratory and theoretical models for the effects of bacterial motility and chemotaxis on microbial population growth. In:CRC Handbook of Laboratory Model Systems for Microbial Ecosystems, J. W. T. Wimpenny (Ed.), Vol. 2, pp. 141–176. Boca Raton, FL: CRC Press.

    Google Scholar 

  • Lauffenburger, D. A. and B. Calcagno P. 1983. Competition between two microbial populations in a nonmixed environment: effect of cell random motility.Biotechnol. Bioengng. 25, 2103–2115.

    Article  Google Scholar 

  • Lauffenburger, D. A., R. Aris and K. Keller. 1982. Effects of cell motility and chemotaxis on microbial population growth.Biophys. J. 40, 209–219.

    Article  Google Scholar 

  • Macnab, R. M. 1980. Sensing the environment: bacterial chemotaxis. In:Biological Regulation and Development, R. Goldberger (Ed.), pp. 377–412. New York: Plenum Press.

    Google Scholar 

  • Macnab, R. M. and D. E. Koshland Jr. 1972. The gradient-sensing mechanism in bacterial chemotaxis.Proc. natn. Acad. Sci. U.S.A. 69, 2509–2512.

    Article  Google Scholar 

  • Mesibov, R., G. W. Ordall and J. Adler. 1973. The range of attractant concentrations for bacterial chemotaxis and the threshold and size of response over this range.J. gen. Physiol. 62, 203–223.

    Article  Google Scholar 

  • Nossal, R. and S. H. Chen. 1973. Effects of chemoattractant on the motility ofEscherichia coli.Nature New Biol. 244, 253–254.

    Google Scholar 

  • Othmer, H., S. Dunbar and Alt. 1988. Models of dispersal in biological systems.J. math. Biol. 26, 263–298.

    Article  MATH  MathSciNet  Google Scholar 

  • Parkinson, J. S. 1988. Protein phosphorylation in bacterial chemotaxis.Cell 53, 1–2.

    Article  Google Scholar 

  • Purcell, E. M. 1977. Life at low Reynolds number.Am. J. Phys. 45, 3–11.

    Article  Google Scholar 

  • 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. Engng Sci. 44, 2881–2897.

    Article  Google Scholar 

  • Rubinow, S. I. 1975.Introduction to Mathematical Biology. New York: John Wiley.

    MATH  Google Scholar 

  • Scribner, T. L., L. A. Segel and E. H. Rogers. 1974. A numerical study of the formation and propagation of traveling bands of chemotactic bacteria.J. Theor. Biol. 46, 189–219.

    Article  Google Scholar 

  • Segel, L. A. 1977. A theoretical study of receptor mechanisms in bacterial chemotaxis.SIAM J. appl. Math.,37, 653–665.

    Article  Google Scholar 

  • Segel, L. A. 1979. On deducing the nature and effect of attractant-receptor binding from population movements of chemotactic bacteria. In:Physical Chemical Aspects of Cell Surface Events in Cellular Regulation, C. DeLisi and R. Blumenthal (Eds), pp. 293–302. New York: Elsevier.

    Google Scholar 

  • Segel, L. A. and J. L. Jackson. 1973. Theoretical analysis of chemotactic movement in bacteria.J. mechanochem. Cell Motil. 2, 25–34.

    Google Scholar 

  • Sherris, J. C., N. W. Preston and J. G. Shoesmith. 1957. The influence of oxygen and arginine on the motility of a strain ofPseudomonas sp.J. gen. Microbiol. 16, 86–96.

    Google Scholar 

  • Spudich, J. L. and D. E. Koshland, Jr. 1975. Quantitation of the sensory response in bacterial chemotaxis.Proc. natn. Acad. Sci. U.S.A. 72, 710–713.

    Article  Google Scholar 

  • Staffeld, P. O., D. A. Lauffenburger and J. A. Quinn. 1987. Mathematical analysis of cell transport phenomena: bacterial chemotaxis in the capillary assay.Chem. Engng Commun. 58, 339–351.

    Google Scholar 

  • Stewart, R. C. and F. W. Dalquist. 1987. Molecular components of bacterial chemotaxis.Chem. Rev. 87, 997–1025.

    Article  Google Scholar 

  • Stock, J. and A. M. Stock. 1987. What is the role of receptor methylation in bacterial chemotaxis?Trends biochem. Sci. 12, 371–375.

    Article  Google Scholar 

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Ford, R.M., Lauffenburger, D.A. Analysis of chemotactic bacterial distributions in population migration assays using a mathematical model applicable to steep or shallow attractant gradients. Bltn Mathcal Biology 53, 721–749 (1991). https://doi.org/10.1007/BF02461551

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