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Optimal methylation noise for best chemotactic performance of E. coli
Phys. Rev. E 97, 032420 – Published 29 March, 2018
DOI: https://doi.org/10.1103/PhysRevE.97.032420
Abstract
In response to a concentration gradient of chemoattractant, E. coli bacterium modulates the rotational bias of flagellar motors which control its run-and-tumble motion, to migrate towards regions of high chemoattractant concentration. Presence of stochastic noise in the biochemical pathway of the cell has important consequences on the switching mechanism of motor bias, which in turn affects the runs and tumbles of the cell in a significant way. We model the intracellular reaction network in terms of coupled time evolution of three stochastic variables—kinase activity, methylation level, and CheY-P protein level—and study the effect of methylation noise on the chemotactic performance of the cell. In presence of a spatially varying nutrient concentration profile, a good chemotactic performance allows the cell to climb up the concentration gradient quickly and localize in the nutrient-rich regions in the long time limit. Our simulations show that the best performance is obtained at an optimal noise strength. While it is expected that chemotaxis will be weaker for very large noise, it is counterintuitive that the performance worsens even when noise level falls below a certain value. We explain this striking result by detailed analysis of CheY-P protein level statistics for different noise strengths. We show that when the CheY-P level falls below a certain (noise-dependent) threshold the cell tends to move down the concentration gradient of the nutrient, which has a detrimental effect on its chemotactic response. This threshold value decreases as noise is increased, and this effect is responsible for noise-induced enhancement of chemotactic performance. In a harsh chemical environment, when the nutrient degrades with time, the amount of nutrient intercepted by the cell trajectory is an effective performance criterion. In this case also, depending on the nutrient lifetime, we find an optimum noise strength when the performance is at its best.
Physics Subject Headings (PhySH)
Corrections
9 April, 2018
Correction: A minor typographical error in Eq. (6) has been corrected, and a missing definition afterward in text has been inserted.
Article Text
References (60)
- M. Jeschke, S. Baumgartner, and S. Legewie, Determinants of cell-to-cell variability in protein kinase signaling, PLoS Comput. Biol. 9, e1003357 (2013).
- M. B. Elowitz, A. J. Levine, E. D. Siggia, and P. S. Swain, Stochastic Gene Expression in a Single Cell, Science 297, 1183 (2002).
- A. Eldar and M. B. Elowitz, Functional roles for noise in genetic circuits, Nature (London) 467, 167 (2010).
- R. Milo, P. Jorgensen, U. Moran, G. Weber, and M. Springer, BioNumbers: The database of key numbers in molecular and cell biology, Nucl. Acid. Res. 38, D750 (2010).
- C. V. Rao, D. M. Wolf, and A. P. Arkin, Control, exploitation and tolerance of intracellular noise, Nature (London) 420, 231 (2002).
- L. S. Tsimring, BioNumbers: The database of key numbers in molecular and cell biology, Rep. Prog. Phys. 77, 026601 (2014).
- G. Lan and Y. Tu, Information processing in bacteria: Memory, computation, and statistical physics: A key issues review, Rep. Prog. Phys. 79, 052601 (2016).
- P. C. Bressloff, Stochastic Processes in Cell Biology (Springer, Heidelberg, 2014).
- H. C. Berg, E. Coli in Motion (Springer, New York, 2003).
- J. Adler, A method for measuring chemotaxis and use of the method to determine optimum conditions for chemotaxis by Escherichia coli, J. Gen. Microbiol. 74, 77 (1973).
- H. C. Berg and D. A. Brown, Chemotaxis in Eschericia coli analysed by three-dimensional tracking, Nature (London) 239, 500 (1972).
- S. M. Block, J. E. Segall, and H. C. Berg, Adaptation kinetics in bacterial chemotaxis, J. Bacteriol. 154, 312 (1983).
- S. M. Block, J. E. Segall, and H. C. Berg, Impulse responses in bacterial chemotaxis, Cell 31, 215 (1982).
- V. Sourjik, Receptor clustering and signal processing in E. coli chemotaxis, Trends Microbiol. 12, 569 (2004).
- A. Bren and M. Eisenbach, How signals are heard during bacterial chemotaxis: protein-protein interactions in sensory propagation, J. Bacteriol. 182, 6865 (2000).
- M. Eisenbach, Control of bacterial chemotaxis, Mol. Microbiol. 20, 903 (1996).
- E. Korobkova, T. Emonet, J. M. Vilar, T. S. Shimizu, and P. Cluzel, From molecular noise to behavioral variability in a single bacterium, Nature (London) 428, 574 (2004).
- Y. Tu and G. Grinstein, How White Noise Generates Power-Law Switching in Bacterial Flagellar Motors, Phys. Rev. Lett. 94, 208101 (2005).
- F. Matthaus, M. Jagodic, and J. Dobnikar, E. coli superdiffusion and chemotaxis-search strategy, precision, and motility, Biophys. J. 97, 946 (2009).
- F. Matthaus, M. S. Mommer, T. Curk, and J. Dobnikar, On the origin and characteristics of noise-induced lévy walks of e. coli, PLoS ONE 6, e18623 (2011).
- E. A. Korobkova, T. Emonet, H. Park, and P. Cluzel, Hidden Stochastic Nature of A Single Bacterial Motor, Phys. Rev. Lett. 96, 058105 (2006).
- H. Park, P. Oikonomou, C. C. Guet, and P. Cluzel, Noise underlies switching behavior of the bacterial flagellum, Biophys. J. 101, 2336 (2011).
- T. Emonet and P. Cluzel, Relationship between cellular response and behavioral variability in bacterial chemotaxis, Proc. Natl. Acad. Sci. USA 105, 3304 (2008).
- H. Park, W. Pontius, C. C. Guet, J. F. Marko, T. Emonet, and P. Cluzel, Interdependence of behavioural variability and response to small stimuli in bacteria, Nature (London) 468, 819 (2010).
- M. W. Sneddon, W. Pontius, and T. Emonet, Stochastic coordination of multiple actuators reduces latency and improves chemotactic response in bacteria, Proc. Natl. Acad. Sci. USA 109, 805 (2012).
- B. Hu and Y. Tu, Coordinated Switching of Bacterial Flagellar Motors: Evidence for Direct Motor-Motor Coupling, Phys. Rev. Lett. 110, 158703 (2013).
- N. Barkai and S. Leibler, Robustness in simple biochemical networks, Nature (London) 387, 913 (1997).
- U. Alon, M. G. Surette, N. Barkai, and S. Leibler, Robustness in bacterial chemotaxis, Nature (London) 397, 168 (1999).
- Y. S. Dufour, S. Gillet, N. W. Frankel, D. B. Weibel, and T. Emonet, Direct correlation between motile behaviors and protein abundance in single cells, PLoS Comput. Biol. 12, e1005041 (2016).
- U. Roy and M. Gopalakrishnan, Ultrasensitivity and fluctuations in the Barkai-Leibler model of chemotaxis receptors in Escherichia coli, PLoS ONE 12, e0175309 (2017).
- N. W. Frankel, W. Pontius, Y. S. Dufour, J. Long, L. Hernandez-Nunez, and T. Emonet, Adaptability of non-genetic diversity in bacterial chemotaxis, eLife 3, e03526 (2014).
- K. M. Taute, S. Gude, S. J. Tans, and T. S. Shimizu, High-throughput 3D tracking of bacteria on a standard phase contrast microscope, Nat. Commun. 6, 8776 (2015).
- R. He, R. Zhang, and J. Yuan, Noise-Induced Increase of Sensitivity in Bacterial Chemotaxis, Biophys. J. 111, 430 (2016).
- M. Flores, T. S. Shimizu, P. R. ten Wolde, and F. Tostevin, Signaling Noise Enhances Chemotactic Drift of E. coli, Phys. Rev. Lett. 109, 148101 (2012).
- Y. Tu, T. S. Shimizu, and H. C. Berg, Modeling the chemotactic response of Escherichia coli to time-varying stimuli, Proc. Natl. Acad. Sci. USA 105, 14855 (2008).
- L. Jiang, Q. Ouyang, and Y. Tu, Quantitative modelling of Escherichia coli chemotactic motion in environments varying in space and time, PLoS Comp. Biol. 6, e1000735 (2010).
- B. A. Mello and Y. Tu, An allosteric model for heterogeneous receptor complexes: Understanding bacterial chemotaxis responses to multiple stimuli, Proc. Natl. Acad. Sci. USA 102, 17354 (2005).
- J. E. Keymer, R. G. Endres, M. Skoge, Y. Meir, and N. S. Wingreen, Chemosening in Escherichia coli: two regimes of two-state receptors, Proc. Natl. Acad. Sci. USA 103, 1786 (2006).
- M. S. Li and G. L. Hazelbauer, Cellular stoichiometry of the components of the chemotaxis signaling complex, J. Bacteriol. 186, 3687 (2004).
- M. S. Li and G. L. Hazelbauer, Adaptational assistance in clusters of bacterial chemoreceptors, Mol. Mibrobiol. 56, 1617 (2005).
- S. Schulmeister, M. Ruttorf, S. Thiem, D. Kentner, D. Lebiedz, and V. Sourjik, Protein exchange dynamics at chemoreceptor clusters in Escherichia coli, Proc. Natl. Acad. Sci. USA 105, 6403 (2008).
- T. S. Shimizu, Y. Tu, and H. C. Berg, A modular gradient-sensing network for chemotaxis in Escherichia coli revealed by responses to time-varying stimuli, Mol. Syst. Biol. 6, 382 (2010).
- P. Cluzel, M. Surette, and S. Leibler, An ultrasensitive bacterial motor revealed by monitoring signaling proteins in single cells, Science 287, 1652 (2000).
- M. Binz, A. P. Lee, C. Edwards, and D. V. Nicolau, Motility of bacteria in microfluidic structures, Microelectron. Eng. 87, 810 (2010).
- Z. Li, Q. Cai, X. Zhang, G. Si, Q. Ouyang, C. Luo, and Y. Tu, Barrier Crossing in Escherichia coli Chemotaxis, Phys. Rev. Lett. 118, 098101 (2017).
- R. Karmakar, R. V. S. Uday Bhaskar, R. E. Jesudasan, M. S. Tirumkudulu, and K. V. Venkatesh, Enhancement of swimming speed leads to a more-efficient chemotactic response to repellent, Appl. Environ. Microbiol. 82, 1205 (2016).
- Y. S. Dufour, X. Fu, L. Hernandez-Nunez, and T. Emonet, Limits of feedback control in bacterial chemotaxis, PLoS Comput. Biol. 10, e1003694 (2014).
- C. W. Gardiner, Handbook of Stochastic Methods for Physics, Chemistry and the Natural Sciences (Springer, Berlin, 2004).
- M. Abramowitz and I. Stegun, Handbook of Mathematical Functions (Dover, New York, 1965).
- Z. X. Wang and D. R. Guo, Special Functions (World Scientific, Singapore, 1989).
- P. G. de Gennes, Chemotaxis and the role of internal delays, Eur. Biophys. J. 33, 691 (2004).
- S. Chatterjee, R. A. da Silveira, and Y. Kafri, Chemotaxis when bacteria remember: drift versus diffusion, PLoS Comput. Biol. 7, e1002283 (2011).
- Y. Kafri and R. A. da Silveira, Steady-State Chemotactic Response in E. coli, Phys. Rev. Lett. 100, 238101 (2008).
- J. Yuan, R. W. Branch, B. G. Hosu, and H. C. Berg, Adaptation at the output of the chemotaxis signalling pathway, Nature (London) 484, 233 (2012); Y. Tu and H. C. Berg, Tandem adaptation with a common design in Escherichia coli chemotaxis, J. Mol. Biol. 423, 782 (2012).
- W. Pontius, M. W. Sneddon, and T. Emonet, Adaptation dynamics in densely clustered chemoreceptors, PLoS Comput. Biol. 9, e1003230 (2013).
- R. Colin, C. Rosazza, A. Vaknin, and V. Sourjik, Multiple sources of slow activity fluctuations in a bacterial chemosensory network, eLife 6, e26796 (2017).
- S. Dev and S. Chatterjee, Optimal search time in E. coli chemotaxis, Phys. Rev. E 91, 042714 (2015).
- A. Celani and M. Vergassola, Bacterial strategies for chemotaxis response, Proc. Natl. Acad. Sci. USA 107, 1391 (2010).
- S. Redner, A Guide to First Passage Processes (Cambridge University, Cambridge, England, 2001).
- R. Metzler, G. Oshanin, and S. Redner, First-Passage Phenomena and their Applications (World Scientific, Singapore, 2014).