Skip to main content

Advertisement

Log in

Coexistence in the chemostat as a result of metabolic by-products

  • Published:
Journal of Mathematical Biology Aims and scope Submit manuscript

Abstract

Classical chemostat models assume that competition is purely exploitative and mediated via a common, limiting and single resource. However, in laboratory experiments with pathogens related to the genetic disease Cystic Fibrosis, species specific properties of production, inhibition and consumption of a metabolic by-product, acetate, were found. These assumptions were implemented into a mathematical chemostat model which consists of four nonlinear ordinary differential equations describing two species competing for one limiting nutrient in an open system. We derive classical chemostat results and find that our basic model supports the competitive exclusion principle, the bistability of the system as well as stable coexistence. The analytical results are illustrated by numerical simulations performed with experimentally measured parameter values. As a variant of our basic model, mimicking testing of antibiotics for therapeutic treatments in mixed cultures instead of pure ones, we consider the introduction of a lethal inhibitor, which cannot be eliminated by one of the species and is selective for the stronger competitor. We discuss our theoretical results in relation to our experimental model system and find that simulations coincide with the qualitative behavior of the experimental result in the case where the metabolic by-product serves as a second carbon source for one of the species, but not the producer.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Armstrong R.A., McGehee R. (1980) Competitive exclusion. Am. Nat. 115(2): 151–170

    Article  MathSciNet  Google Scholar 

  2. Bassler B.L. (1999) How bacteria talk to each other: regulation of gene expression by quorum sensing. Curr. Opin. Microbiol. 2, 582

    Article  Google Scholar 

  3. Braselton J.P., Waltman P. (2001) A competition model with dynamically allocated inhibitor production. Math. Biosci. 173, 55–84

    Article  MATH  MathSciNet  Google Scholar 

  4. Butler G.J., Wolkowicz G.S.K. (1985) A mathematical model of the chemostat with a general class of functions describing nutrient uptake. SIAM J. Appl. Math. 45, 138–151

    Article  MATH  MathSciNet  Google Scholar 

  5. Chao L., Levin B.R. (1981) Structured habitats and the evolution of anticompetitor toxins in bacteria. Proc. Nat. Acad. Sci. USA 78, 6324–6328

    Article  Google Scholar 

  6. Coppel W.A. (1965) Stability and Asymptotic Behavior of Differential Equations. D.C. Heath and Co., Boston

    MATH  Google Scholar 

  7. Diekmann O., Gyllenberg M., Metz J.A.J. (2003) Steady-state analysis of structured population models. Theor. Popul. Biol. 63, 309–338

    Article  MATH  Google Scholar 

  8. Dockery J.D., Keener J.P. (2000) A mathematical model for quorum sensing in Pseudomonas aeruginosa. Bull. Math. Biol. 00, 1–22

    Google Scholar 

  9. Doebeli M. (2002) A model for the evolutionary dynamics of cross-feeding polymorphisms in microorganisms. Popul. Ecol. 44, 59–70

    Article  Google Scholar 

  10. Ermentrout, B.: Simulating, Analyzing, and Animating Dynamical Systems: A Guide to XPPAUT for Researchers and Students. Society for Industrial and Applied Mathematics, (2002)

  11. Freedman H.I., Xu. Y. (1993) Models of competition in the chemostat with instantaneous and delayed nutrient recycling. J. Math. Biol. 31, 513–527

    Article  MATH  MathSciNet  Google Scholar 

  12. Ghani M., Soothill J.S. (1997) Ceftazidime, gentamicin, and rifampicin, in combination, kill biofilm of mucoid Pseudomonas aeruginosa. Can. J. Microbiol. 43, 999–1004

    Article  Google Scholar 

  13. Gopalsamy K. (1992) Stability and Oscillations in Delay Differential Equations of Population Dynamics. Kluwer, Dordrecht

    MATH  Google Scholar 

  14. S.R. Hansen, S.R., Hubbell, S.P.: Single-nutrient microbial competition: Qualitative agreement between experimental and theoretically forecast outcomes. Science 207(4438), 1491–1493 (1980)

  15. Hardin G. (1960) The competitive exclusion principle. Science 131, 1292–1298

    Article  Google Scholar 

  16. Hirsch M.W., Hanisch H., Gabriel J.-P. (1985) Differential equation models of some parasitic infections: methods for the study of asymptotic behavior. Comm. Pure Appl. Math. 38, 733–753

    Article  MATH  MathSciNet  Google Scholar 

  17. Hsu S.B. (1978) Limiting behavior for competing species. SIAM J. Appl. Math. 34, 760–763

    Article  MATH  MathSciNet  Google Scholar 

  18. Hsu S.B., Hubbell S.P., Waltman P. (1977) A mathematical theory for single-nutrient competition in continuous cultures of micro-organisms. SIAM J. Appl. Math. 32(2): 366–383

    Article  MATH  MathSciNet  Google Scholar 

  19. Hsu S.B., Li Y.-S., Waltman P. (2000) Competition in the presence of a lethal external inhibitor. Math. Biosci. 167(2): 177–199

    Article  MATH  MathSciNet  Google Scholar 

  20. Hsu S.B., Luo T.-K., Waltman P. (1995) Competition between plasmid-bearing and plasmid-free organisms in a chemostat with an inhibitor. J. Math. Biol. 34, 225–238

    Article  MATH  MathSciNet  Google Scholar 

  21. Hsu S.B., Waltman P. (1991) Analysis of a model of two competitors in a chemostat with an external inhibitor. SIAM J. Appl. Math. 52(2): 528–541

    Article  MathSciNet  Google Scholar 

  22. Hsu S.B., Waltman P. (1997) Competition between plasmid-bearing and plasmid-free organisms in selective media. Chem. Eng. Sci. 52(1): 23–35

    Article  Google Scholar 

  23. Hsu S.B., Waltman P. (1998) Competition in the chemostat when one competitor produces a toxin. Jpn J. Indust. Appl. Math. 15, 471–490

    Article  MATH  MathSciNet  Google Scholar 

  24. Hsu S.B., Waltman P. (2002) A model of the effect of anti-competitor toxins on plasmid-bearing, plasmid-free competition. Taiwanese J. Mathematics 6, 135–155

    MATH  MathSciNet  Google Scholar 

  25. S.B., Hsu, Waltman, P.: A survey of mathematical models of competition with an inhibitor. Math. Biosci. 187, 53–91 (2004)

    Google Scholar 

  26. Hutchinson G.E. (1961) The paradox of the plankton. Am. Nat. 95, 137–145

    Article  Google Scholar 

  27. Lenski R.E., Hattingh S.E. (1986) Coexistence of two competitors on one resource and one inhibitor: A chemostat model based on bacteria and antibiotics. J. Theor. Biol. 122, 83–96

    Article  MathSciNet  Google Scholar 

  28. Li B. (1998) Global asymptotic behavior of the chemostat: General response functions and different removal rate. SIAM J. Appl. Math. 59(2): 411–422

    Article  Google Scholar 

  29. Lu Z., Hadeler K.P. (1998) Model of plasmid-bearing, plasmid-free competition in the chemostat with nutrient recycling and an inhibitor. Math. Biosci. 148, 147–159

    Article  MATH  MathSciNet  Google Scholar 

  30. Luo T.K., Hsu S.B. (1995) Global analysis of a model of plasmid-bearing, plasmid-free competition in a chemostat with inhibitons. J. Math. Biol. 34, 41–76

    Article  MATH  MathSciNet  Google Scholar 

  31. Madigan, M.T. Martinko, J.M., Parker, J.: Brock Biology of Microorganisms. Prentice Hall Englewood Cliffs, (2003)

  32. Marsh P.D., Bowden G.H.W. (2000) Microbial community interactions in biofilms. In: Allison D.G., Gilbert P., Lappin-Scott H.M., Wilson M. (eds) Community Structure and Co-operation in Biofilms. Press Syndicate of the University of Cambridge, Cambridge, pp. 167–198

    Google Scholar 

  33. Passarge J., Huisman J.(2002) Competition in well-mixed habitats: From competitive exclusion to competitive chaos. In: Sommer U., Worm B. ed, Competition and Coexistence Ecological Studies., vol 161, Springer, Berlin Heidelberg New York, pp. 7–42

  34. Reeves G.T., Narang A., Pilyugin S.S. (2004) Growth of mixed cultures on mixtures of substitutable substrates: the operating diagram for a structured model. J. Theor. Biol. 226, 143–157

    Article  MathSciNet  Google Scholar 

  35. Riedel K., et al. (2001) N-acylhomoserine-lactone-mediated communication between Pseudomonas aeruginosa and Burkholderia cepacia in mixed biofilms. Microbiology 147, 3249–3262

    Google Scholar 

  36. Ruan S., He X.-Z. Global stability in chemostat-type competition models with nutrient recycling. SIAM J. Appl. Math. 58(1): 170–198 (1998) A correction can be found online at http://www.math.miami.edu/∼ruan/publications.html

    Google Scholar 

  37. Sardonini C.A., DiBiasio D. (1987) A model for growth of Saccharomyces cerevisiae containing a recombinant plasmid in selective media. Biotechnol. Bioeng. 29, 469–475

    Article  Google Scholar 

  38. Schmidt, J.K., König, B., Reichl, U.: Characterization of a three bacteria mixed culture in a chemostat: Evaluation and application of a quantitative Terminal-Restriction Fragment Polymorphism (T-RFLP) analysis for absolute and species specific cell enumeration. Biotechnol. Bioeng. (2006) (submitted)

  39. Smith H.L., Waltman P. (1995) The Theory of the Chemostat. Cambridge University Press, Cambridge

    MATH  Google Scholar 

  40. Turner P.E., Souza V., Lenski R.E. (1996) Test of ecological mechanisms promoting the stable coexistence of two bacterial genotypes. Ecology 77(7): 2119–2129

    Article  Google Scholar 

  41. Wolkowicz G.S.K., Lu Z. (1992) Global dynamics of a mathematical model of competition in the chemostat: General response functions and differential death rates. SIAM J. Appl. Math. 52(1): 222–233

    Article  MATH  MathSciNet  Google Scholar 

  42. Wolkowicz G.S.K., Zhiqi L. (1998) Direct interference on competition in a chemostat. J. Biomath. 13(3): 282–291

    MATH  MathSciNet  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Julia Heßeler.

Additional information

Julia Heßeler and Julia K. Schmidt contributed equally to this work

Rights and permissions

Reprints and permissions

About this article

Cite this article

Heßeler, J., Schmidt, J.K., Reichl, U. et al. Coexistence in the chemostat as a result of metabolic by-products. J. Math. Biol. 53, 556–584 (2006). https://doi.org/10.1007/s00285-006-0012-3

Download citation

  • Received:

  • Revised:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00285-006-0012-3

Keywords

Navigation