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Dependence of Bacterial Chemotaxis on Gradient Shape and Adaptation Rate

Author

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  • Nikita Vladimirov
  • Linda Løvdok
  • Dirk Lebiedz
  • Victor Sourjik

Abstract

Simulation of cellular behavior on multiple scales requires models that are sufficiently detailed to capture central intracellular processes but at the same time enable the simulation of entire cell populations in a computationally cheap way. In this paper we present RapidCell, a hybrid model of chemotactic Escherichia coli that combines the Monod-Wyman-Changeux signal processing by mixed chemoreceptor clusters, the adaptation dynamics described by ordinary differential equations, and a detailed model of cell tumbling. Our model dramatically reduces computational costs and allows the highly efficient simulation of E. coli chemotaxis. We use the model to investigate chemotaxis in different gradients, and suggest a new, constant-activity type of gradient to systematically study chemotactic behavior of virtual bacteria. Using the unique properties of this gradient, we show that optimal chemotaxis is observed in a narrow range of CheA kinase activity, where concentration of the response regulator CheY-P falls into the operating range of flagellar motors. Our simulations also confirm that the CheB phosphorylation feedback improves chemotactic efficiency by shifting the average CheY-P concentration to fit the motor operating range. Our results suggest that in liquid media the variability in adaptation times among cells may be evolutionary favorable to ensure coexistence of subpopulations that will be optimally tactic in different gradients. However, in a porous medium (agar) such variability appears to be less important, because agar structure poses mainly negative selection against subpopulations with low levels of adaptation enzymes. RapidCell is available from the authors upon request.Author Summary: Chemotaxis plays an important role in bacterial lifestyle, providing bacteria with the ability to actively search for an optimal growth environment. The chemotaxis system is likely to be highly optimized, because on the evolutionary time scale even a modest enhancement of its efficiency can give cells a large competitive advantage. In this study, we use up-to-date experimental and modeling information to construct a new computational model of chemotactic E. coli and implement it in a computationally efficient way to simulate large bacterial populations. Our simulations are performed in a new type of attractant gradient that ensures a constant level of chemotactic excitation at any position. We show that optimal chemotactic movement in a gradient results from a fine balance between excitation and adaptation. As a consequence, steeper gradients require higher optimal rates of adaptation. Simulations demonstrate that the observed intercellular variability of adaptation times, which is caused by gene expression noise, may play a positive role for the bacterial population as a whole, by allowing its subpopulations to be optimally tactic in gradients of different strengths. We further show that optimal chemotactic properties in a porous medium (agar) are different from those in a liquid.

Suggested Citation

  • Nikita Vladimirov & Linda Løvdok & Dirk Lebiedz & Victor Sourjik, 2008. "Dependence of Bacterial Chemotaxis on Gradient Shape and Adaptation Rate," PLOS Computational Biology, Public Library of Science, vol. 4(12), pages 1-17, December.
  • Handle: RePEc:plo:pcbi00:1000242
    DOI: 10.1371/journal.pcbi.1000242
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    References listed on IDEAS

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    2. Clinton H Hansen & Robert G Endres & Ned S Wingreen, 2008. "Chemotaxis in Escherichia coli: A Molecular Model for Robust Precise Adaptation," PLOS Computational Biology, Public Library of Science, vol. 4(1), pages 1-1, January.
    3. Burton W Andrews & Tau-Mu Yi & Pablo A Iglesias, 2006. "Optimal Noise Filtering in the Chemotactic Response of Escherichia coli," PLOS Computational Biology, Public Library of Science, vol. 2(11), pages 1-12, November.
    4. N. Barkai & S. Leibler, 1997. "Robustness in simple biochemical networks," Nature, Nature, vol. 387(6636), pages 913-917, June.
    5. Markus Kollmann & Linda Løvdok & Kilian Bartholomé & Jens Timmer & Victor Sourjik, 2005. "Design principles of a bacterial signalling network," Nature, Nature, vol. 438(7067), pages 504-507, November.
    6. Ekaterina Korobkova & Thierry Emonet & Jose M. G. Vilar & Thomas S. Shimizu & Philippe Cluzel, 2004. "From molecular noise to behavioural variability in a single bacterium," Nature, Nature, vol. 428(6982), pages 574-578, April.
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