Skip to main content
Log in

A Mathematical Description of Bacterial Chemotaxis in Response to Two Stimuli

  • Original Article
  • Published:
Bulletin of Mathematical Biology Aims and scope Submit manuscript

Abstract

Bacteria are often exposed to multiple stimuli in complex environments, and their efficient chemotactic decisions are critical to survive and grow in their native environments. Bacterial responses to the environmental stimuli depend on the ratio of their corresponding chemoreceptors. By incorporating the signaling machinery of individual cells, we analyze the collective motion of a population of Escherichia coli bacteria in response to two stimuli, mainly serine and methyl-aspartate (MeAsp), in a one-dimensional and a two-dimensional environment, which is inspired by experimental results in Y. Kalinin et al., J. Bacteriol. 192(7):1796–1800, 2010. Under suitable conditions, we show that if the ratio of the main chemoreceptors of individual cells, namely Tar/Tsr, is less than a specific threshold, the bacteria move to the gradient of serine, and if the ratio is greater than the threshold, the group of bacteria moves toward the gradient of MeAsp. Finally, we examine the theory with Monte Carlo agent-based simulations and verify that our results qualitatively agree well with the experimental results in Y. Kalinin et al. (2010).

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10

Similar content being viewed by others

References

  • Alt W (1980) Biased random walk models for chemotaxis and related diffusion approximations. J Math Biol 9(2):147–177

    Article  MathSciNet  MATH  Google Scholar 

  • Aminzare, Z, Sontag ED (2013) Remarks on a population-level model of chemotaxis: advection-diffusion approximation and simulations. arXiv preprintarXiv:1302.2605

  • Barkai N, Leibler S Robustness in simple biochemical networks. Nature, 387(6636):913–917

  • Berg HC, Brown DA (1972) Chemotaxis in Escherichia coli analysed by three-dimensional tracking. Nature 239(5374):500–504

    Article  Google Scholar 

  • Berg HC, Tedesco PM (1975) Transient response to chemotactic stimuli in Escherichia coli. Proc Natl Acad Sci 72(8):3235–3239

    Article  Google Scholar 

  • Berg HC, Turner L (1990) Chemotaxis of bacteria in glass capillary arrays. Escherichia coli, motility, microchannel plate, and light scattering. Biophys J 58(4):919–930

    Article  Google Scholar 

  • Bray D, Bourret RB (1995) Computer analysis of the binding reactions leading to a transmembrane receptor-linked multiprotein complex involved in bacterial chemotaxis. Mol Biol Cell 6(10):1367–1380

    Article  Google Scholar 

  • Bren A, Welch M, Blat Y, Eisenbach M (1996) Signal termination in bacterial chemotaxis: CheZ mediates dephosphorylation of free rather than switch-bound CheY. Proc Natl Acad Sci 93(19):10090–10093

    Article  Google Scholar 

  • Clausznitzer D, Oleksiuk O, Løvdok L, Sourjik V, Endres RG (2010) Chemotactic response and adaptation dynamics in Escherichia coli. PLoS Comput Biol 6(5):e1000784

    Article  MathSciNet  Google Scholar 

  • Demir M, Douarche C, Yoney A, Libchaber A, Salman H (2011) Effects of population density and chemical environment on the behavior of Escherichia coli in shallow temperature gradients. Phys Biol 8(6):63001

    Article  Google Scholar 

  • Edgington MP, Tindall MJ (2018) Mathematical analysis of the Escherichia coli chemotaxis Signalling pathway. Bull Math Biol 80(4):758–787

    Article  MathSciNet  MATH  Google Scholar 

  • Endres RG, Wingreen NS (2006) Precise adaptation in bacterial chemotaxis through assistance neighborhoods. Proc Natl Acad Sci 103(35):13040–13044

    Article  Google Scholar 

  • Endres RG, Oleksiuk O, Hansen CH, Meir Y, Sourjik V, Wingreen NS (2008) Variable sizes of Escherichia coli chemoreceptor signaling teams. Mol Syst Biol 4(1):211

    Article  Google Scholar 

  • Erban R, Othmer HG (2004) From individual to collective behavior in bacterial chemotaxis. SIAM J Appl Math 65(2):361–391

    Article  MathSciNet  MATH  Google Scholar 

  • Erban R, Othmer HG (2005) From signal transduction to spatial pattern formation in E. coli: a paradigm for multiscale modeling in biology. Multiscale Model. Simul., 3(2):362–394

  • Gosztolai A, Barahona M (2020) Cellular memory enhances bacterial chemotactic navigation in rugged environments. Commun Phys 3(1):1–10

    Article  Google Scholar 

  • Hansen CH, Sourjik V, Wingreen NS (2010) A dynamic-signaling-team model for chemotaxis receptors in Escherichia coli. Proc Natl Acad Sci 107(40):17170–17175

    Article  Google Scholar 

  • Hu B, Tu Y (2013) Precision sensing by two opposing gradient sensors: how does Escherichia coli find its preferred pH level? Biophys J 105(1):276–285

    Article  Google Scholar 

  • Hu B, Tu Y (2014) Behaviors and strategies of bacterial navigation in chemical and nonchemical gradients. PLoS Comput Biol 10(6):1003672

    Article  Google Scholar 

  • Jiang L, Ouyang Q, Tu Y (2010) Quantitative modeling of Escherichia coli chemotactic motion in environments varying in space and time. PLoS Comput Biol 6(4):1000735

    Article  MathSciNet  Google Scholar 

  • Kalinin YV, Jiang L, Tu Y, Wu M (2009) Logarithmic sensing in Escherichia coli bacterial chemotaxis. Biophys J 96(6):2439–2448

    Article  Google Scholar 

  • Kalinin Y, Neumann S, Sourjik V, Wu M (2010) Responses of escherichia coli bacteria to two opposing chemoattractant gradients depend on the chemoreceptor ratio. J Bacteriol 192(7):1796–1800

    Article  Google Scholar 

  • Keller EF, Segel LA (1971) Model for chemotaxis. J Theor Biol 30(2):225–234

    Article  MATH  Google Scholar 

  • Keymer JE, Endres RG, Skoge M, Meir Y, Wingreen NS (2006) Chemosensing in Escherichia coli: two regimes of two-state receptors. Proc Natl Acad Sci 103(6):1786–1791

    Article  Google Scholar 

  • Lai R-Z, Gosink KK, Parkinson JS (2017) Signaling consequences of structural lesions that alter the stability of chemoreceptor trimers of dimers. J Mol Biol 429(6):823–835

    Article  Google Scholar 

  • Lan G, Schulmeister S, Sourjik V, Tu Y (2011) Adapt locally and act globally: strategy to maintain high chemoreceptor sensitivity in complex environments. Molecular Syst Biol 7(1):475

    Article  Google Scholar 

  • Lazova MD, Ahmed T, Bellomo D, Stocker R, Shimizu TS (2011) Response rescaling in bacterial chemotaxis. Proc Natl Acad Sci 108(33):13870–13875

    Article  Google Scholar 

  • Lipkow K (2006) Changing cellular location of CheZ predicted by molecular simulations. PLoS Comput. Biol. 2(4):39

    Article  Google Scholar 

  • Lipkow K, Andrews SS, Bray D (2005) Simulated diffusion of phosphorylated CheY through the cytoplasm of Escherichia coli. J Bacteriol 187(1):45–53

    Article  Google Scholar 

  • Long Z, Quaife B, Salman H, Oltvai ZN (2017) Cell-cell communication enhances bacterial chemotaxis toward external attractants. Sci Rep 7(1):1–12

    Article  Google Scholar 

  • Macnab RM, Koshland DE (1972) The gradient-sensing mechanism in bacterial chemotaxis. Proc Natl Acad Sci 69(9):2509–2512

    Article  Google Scholar 

  • Mello BA, Tu Y (2005) An allosteric model for heterogeneous receptor complexes: under-standing bacterial chemotaxis responses to multiple stimuli. Proc Natl Acad Sci 102(48):17354–17359

    Article  Google Scholar 

  • Mello BA, Tu Y (2007) Effects of adaptation in maintaining high sensitivity over a wide range of backgrounds for Escherichia coli chemotaxis. Biophys J 92(7):2329–2337

    Article  Google Scholar 

  • Menolascina F, Rusconi R, Fernandez VI, Smriga S, Aminzare Z, Sontag ED, Stocker R (2017) Logarithmic sensing in Bacillus subtilis aerotaxis. NPJ Syst Biol Appl 3:16036

    Article  Google Scholar 

  • Monod J, Wyman J, Changeux J-P (1965) On the nature of allosteric transitions: a plausible model. J Mol Biol 12(1):88–118

    Article  Google Scholar 

  • Neumann S, Hansen CH, Wingreen NS, Sourjik V (2010) Differences in signalling by directly and indirectly binding ligands in bacterial chemotaxis. The EMBO J 29(20):3484–3495

    Article  Google Scholar 

  • Othmer HG, Stevens A (1997) Aggregation, blowup and collapse: the ABC s of generalized taxis. SIAM J Appl Math 57(4):1044–1081

    Article  MathSciNet  MATH  Google Scholar 

  • Othmer HG, Dunbar SR, Alt W (1988) Models of dispersal in biological systems. J Math Biol 26:263–298

    Article  MathSciNet  MATH  Google Scholar 

  • Painter KJ, Maini PK, Othmer HG (2000) Development and applications of a model for cellular response to multiple chemotactic cues. J Math Biol 41(4):285–314

    Article  MathSciNet  MATH  Google Scholar 

  • Park J, Aminzare Z (2020) A Mathematical Description of Bacterial Chemotaxis in Response to Two Stimuli. arXiv preprint arXiv:2006.00688

  • Rousset M, Samaey G (2013) Individual-based models for bacterial chemotaxis in the diffusion asymptotics. Math Models Methods Appl Sci 23(11):2005–2037

    Article  MathSciNet  MATH  Google Scholar 

  • Salman H, Libchaber A (2007) A concentration-dependent switch in the bacterial response to temperature. Nat Cell Biol 9(9):1098

    Article  Google Scholar 

  • Shimizu TS, Delalez N, Pichler K, Berg HC (2006) Monitoring bacterial chemo-taxis by using bioluminescence resonance energy transfer: absence of feedback from the flagellar motors. Proc Natl Acad Sci 103(7):2093–2097

    Article  Google Scholar 

  • Shoval O, Goentoro L, Hart Y, Mayo A, Sontag E, Alon U (2010) Fold-change detection and scalar symmetry of sensory input fields. Proc Natl Acad Sci 107(36):15995–16000

    Article  Google Scholar 

  • Shoval O, Alon U, Sontag E (2011) Symmetry invariance for adapting biological systems. SIAM J Appl Math 10(3):857–886

    MathSciNet  MATH  Google Scholar 

  • Simms SA, Stock AM, Stock JB (1987) Purification and characterization of the s-adenosylmethionine: glutamyl methyltransferase that modifies membrane chemoreceptor proteins in bacteria. J Biol Chem 262(18):8537–8543

    Article  Google Scholar 

  • Sourjik V, Berg HC (2002) Receptor sensitivity in bacterial chemotaxis. Proc Natl Acad Sci 99(1):123–127

    Article  Google Scholar 

  • Spiro, P. A., Parkinson, J. S., Othmer, H. G.: A model of excitation and adaptation in bacterial chemotaxis. Proc. Natl. Acad. Sci., 94(14):7263–7268

  • Springer WR, Koshland DE (1977) Identification of a protein methyltransferase as the cheR gene product in the bacterial sensing system. Proc Natl Acad Sci 74(2):533–537

    Article  Google Scholar 

  • Stock JB, Koshland DE (1978) A protein methylesterase involved in bacterial sensing. Proc Natl Acad Sci 75(8):3659–3663

    Article  Google Scholar 

  • Stroock DW (1974) Some stochastic processes which arise from a model of the motion of a bacterium. Z Wahrscheinlichkeitstheor verw Geb 28(4):305–315

    Article  MATH  Google Scholar 

  • Terwilliger TC, Wang JY, Koshland DE (1986) Kinetics of receptor modification. The multiply methylated aspartate receptors involved in bacterial chemotaxis. J Biol Chem 261(23):10814–10820

    Article  Google Scholar 

  • Tindall MJ, Maini PK, Porter SL, Armitage JP (2008) Overview of mathematical approaches used to model bacterial chemotaxis II: bacterial populations. Bull Math Biol 70(6):1570

    Article  MathSciNet  MATH  Google Scholar 

  • Tu Y, Shimizu TS, Berg HC (2008) Modeling the chemotactic response of Escherichia coli to time-varying stimuli. Proc Natl Acad Sci 105(39):14855–14860

    Article  Google Scholar 

  • Vladimirov N, Sourjik V (2009) Chemotaxis: how bacteria use memory. Biol Chem 390(11):1097–1104

    Article  Google Scholar 

  • Vladimirov N, Løvdok L, Lebiedz D, Sourjik V (2008) Dependence of bacterial chemotaxis on gradient shape and adaptation rate. PLoS Comput. Biol 4(12):e1000242

    Article  Google Scholar 

  • Wadhams GH, Armitage JP (2004) Making sense of it all: bacterial chemotaxis. Nat Rev Mol Cell Biol 5(12):1024–1037

    Article  Google Scholar 

  • Welch M, Oosawa K, Aizawa S-L, Eisenbach M (1993) Phosphorylation-dependent binding of a signal molecule to the flagellar switch of bacteria. Proc Natl Acad Sci 90(19):8787–8791

    Article  Google Scholar 

  • Xin X, Othmer HG (2012) A trimer of dimer based model for the chemotactic signal transduction network in bacterial chemotaxis. Bull Math Biol 74(10):2339–2382

  • Xue C (2015) Macroscopic equations for bacterial chemotaxis: integration of detailed biochemistry of cell signaling. J Math Biol 70(1):1–44

    Article  MathSciNet  MATH  Google Scholar 

  • Xue C, Othmer HG (2009) Multiscale models of taxis-driven patterning in bacterial populations. SIAM J Appl Math 70(1):133–167

    Article  MathSciNet  MATH  Google Scholar 

  • Xue C, Yang X (2016) Moment-flux models for bacterial chemotaxis in large signal gradients. J Math Biol 73(4):977–1000

    Article  MathSciNet  MATH  Google Scholar 

  • Yang Y, Sourjik V (2012) Opposite responses by different chemoreceptors set a tunable preference point in Escherichia coli pH taxis. Molecular Microbiol 86(6):1482–1489

    Article  Google Scholar 

Download references

Acknowledgements

The authors would like to thank Professor Eduardo Sontag for sharing the Matlab codes for one-dimensional space (used in Aminzare and Sontag (2013)) and Professor Hans Othmer for helpful discussions. This work is partially supported by the University of Iowa Old Gold Fellowship and Simons Foundation (712522) to ZA. The authors would also like to thank the anonymous referee who provided valuable suggestions and comments to improve this work.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Zahra Aminzare.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Appendix

Appendix

Table 1 Parameters used in intracellular signaling pathway of E. coli

A brief description of Monte Carlo simulation: In a one-dimensional (respectively, two-dimensional) channel, we locate an ensemble of 100,000 agents in the center of the channel \(x=200\) (respectively, \((x,y) = (200, 800)\)) at time \(t=0\). At each time step, the individuals choose a direction +1 or -1 (respectively, \((\cos (\theta ), \sin (\theta ))\), \(\theta \in [0, 2\pi )\)) at random, and move in that direction with a constant speed \(\nu >0\). At each time step, the internal dynamics of each individual are computed by Euler method. At the end of each time step, we choose a number between 0 and 1 randomly and compare the number with the probability of change from run to tumble in interval of length dt, namely \(\lambda (a) dt\). If the turn occurs, the cell moves in the opposite direction with a probability of 0.5 (respectively, rotates by \(\theta \in [0, 2\pi )\), where \(\theta \) is chosen at random). If a cell is located outside the spatial domain, we relocate the cell by imposing reflecting boundary conditions.

See Tables 1 and 2.

Table 2 Input data used in numerical simulation

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Park, J., Aminzare, Z. A Mathematical Description of Bacterial Chemotaxis in Response to Two Stimuli. Bull Math Biol 84, 9 (2022). https://doi.org/10.1007/s11538-021-00965-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11538-021-00965-6

Keywords

Navigation