Robustness in bacterial chemotaxis https://doi.org/10.1038/16483 Abstract Networks of interacting proteins orchestrate the responses of living cells to a variety of external stimuli 1 , but how sensitive is the functioning of these protein networks to variations in theirbiochemical parameters? One possibility is that to achieve appropriate function, the reaction rate constants and enzyme concentrations need to be adjusted in a precise manner, and any deviation from these ‘fine-tuned’ values ruins the network's performance. An alternative possibility is that key properties of biochemical networks are robust 2 ; that is, they are insensitive to the precise values of the biochemical parameters. Here we address this issue in experiments using chemotaxis of Escherichia coli , one of the best-characterized sensory systems 3 , 4 . We focus on how response and adaptation to attractant signals vary with systematic changes in the intracellular concentration of the components of the chemotaxis network. We find that some properties, such as steady-state behaviour and adaptation time, show strong variations in response to varying protein concentrations. In contrast, the precision of adaptation is robust and does not vary with the protein concentrations. This is consistent with a recently proposed molecular mechanism for exact adaptation, where robustness is a direct consequence of the network's architecture 2 . This is a preview of subscription content, access via your institution Access options Access through your institution Subscribe to this journal Receive 52 print issues and online access ￥56,000 per year only ￥1,077 per issue Learn more Buy this article Purchase on SpringerLink Instant access to the full article PDF. ￥ 4,980 Prices may be subject to local taxes which are calculated during checkout Figure 1: Tumbling frequency as a function of time for wild-type (RP437) cells. Figure 2: Chemotaxis behaviour of cells with varying intracellular concentration of the protein CheR. References Bray, D. Protein molecules as computational elements in living cells. Nature 376 , 307–312 (1995). Article ADS CAS PubMed Google Scholar Barkai, N. & Leibler, S. Robustness in simple biochemical networks. Nature 387 , 913–917 (1997). Article ADS CAS PubMed Google Scholar Stock, J. B. & Surette, M. G. in Escherichia coli and Salmonella, Cellular and Molecular Biology (ed. Neidhardt, F. C.) 1103–1129 (ASM Press, Washington, (1996)). Google Scholar Falke, J. J., Bass, R. B., Butler, S. L., Chervitz, S. A. & Danielson, M. A. The two-component signaling pathway of bacterial chemotaxis: a molecular view of signal transduction by receptors, kinases, and adaptation enzymes. Annu. Rev. Cell Dev. Biol. 13 , 457–512 (1997). Article CAS PubMed PubMed Central Google Scholar Bray, D., Bourret, R. B. & Simon, M. I. Computer simulation of the phosphorylation cascade controlling bacterial chemotaxis. Mol. Biol. Cell 5 , 469–482 (1993). Article Google Scholar Bray, D., Levin, M. D. & Morton-Firth, C. J. Receptor clustering as a cellular mechanism to control sensitivity. Nature 393 , 85–88 (1998). Article ADS CAS PubMed Google Scholar Macnab, R. M. & Koshland, D. E. The gradient sensing mechanism in bacterial chemotaxis. Proc. Natl Acad. Sci. USA 69 , 2509–2512 (1972). Article ADS CAS PubMed PubMed Central Google Scholar Berg, H. C. & Tedesco, P. Transient response to chemotaxis stimuli in Escherichia coli . Proc. Natl Acad. Sci. USA 72 , 3235–3239 (1975). Article ADS CAS PubMed PubMed Central Google Scholar Segel, L. A., Goldbeter, A., Devrotes, P. N. & Knox, B. E. Amechanism for exact sensory adaptation based on receptor modification. J. Theor. Biol. 120 , 151–179 (1986). Article CAS PubMed Google Scholar Hauri, D. C. & Ross, J. A. Amodel of excitation and adaption in bacterial chemotaxis. Biophys. J. 68 , 708–722 (1995). Article ADS CAS PubMed PubMed Central Google Scholar Spiro, P. A., Parkinson, J. S. & Othmer, H. G. Amodel of excitation and adaptation in bacterial chemotaxis. Proc. Natl Acad. Sci. USA 94 , 7263–7268 (1997). Article ADS CAS PubMed PubMed Central Google Scholar Asakura, S. & Honda, H. Two-state model for bacterial chemoreceptor proteins. J. Mol. Biol. 176 , 349–367 (1984). Article CAS PubMed Google Scholar Fell, D. Understanding the Control of Metabolism (Portland Press, London, (1997)). Google Scholar Alon, U. et al. Response regulator output in bacterial chemotaxis. EMBO J. 17 , 4238–4248 (1998). Article PubMed PubMed Central Google Scholar Berg, H. C. & Brown, D. A. Chemotaxis in Escherichia coli analysed by three-dimensional tracking. Nature 239 , 500–504 (1972). Article ADS CAS PubMed Google Scholar Parkinson, J. S. & Houts, S. Isolation and behavior of Escherichia coli deletion mutants lacking chemotaxis function. J. Bacteriol. 151 , 106–113 (1982). CAS PubMed PubMed Central Google Scholar Wolfe, A. J., Conley, P. M., Kramer, T. J. & Berg, H. C. Reconstitution of signaling in bacterial chemotaxis. J. Bacteriol. 169 , 1878–1885 (1987). Article CAS PubMed PubMed Central Google Scholar Russel, C. B., Stewart, R. C. & Dahlquist, F. W. Control of transducer methylation levels in Escherichia coli : investigation of components essential for modulation of methylation and demethylation reactions. J. Bacteriol. 171 , 3609–3618 (1989). Article Google Scholar Levin, M., Morton-Firth, C., Abouhamad, W., Bourret, R. & Bray, D. Origins of individual swimming behavior in bacteria. Biophys. J. 74 , 175–181 (1998). Article ADS CAS PubMed PubMed Central Google Scholar Stewart, R. C., Russel, C. B., Roth, A. F. & Dahlquist, F. W. Interaction of CheB with chemotaxis signal transduction components in Escherichia coli : modulation of the methylesterase activity and effects on cell swimming behavior. Cold Spring Harb. Symp. Quant. Biol. LIII , 27–40 (1988). Article Google Scholar Lupas, A. & Stock, J. B. Phosphorylation of an N-terminus regulatory domain activates the CheB methylesterase in bacterial chemotaxis. J. Biol. Chem. 264 , 17337–17342 (1989). CAS PubMed Google Scholar Segall, J. E., Block, S. M. & Berg, H. C. Temporal comparisons in bacterial chemotaxis. Proc. Natl Acad. Sci. USA 83 , 8987–8991 (1986). Article ADS CAS PubMed PubMed Central Google Scholar Stock, J., Kersulis, G. & Koshland, D. E. Neither methylating nor demethylating enzymes are required for bacterial chemotaxis. Cell 42 , 683–690 (1985). Article CAS PubMed Google Scholar Weis, R. M. & Koshland, D. E. Reversible methylation is essential for normal chemotaxis in Escherichia coli in gradients of aspartic acid. Proc. Natl Acad. Sci. USA 86 , 83–87 (1988). Article ADS Google Scholar Berg, H. & Turner, L. Chemotaxis of bacteria in glass capillary arrays. Biophys. J. 58 , 919–930 (1990). Article ADS CAS PubMed PubMed Central Google Scholar Weis, R. M. & Koshland, D. E. Chemotaxis in Escherichia coli proceeds efficiently from different initial tumble frequencies. J. Bacteriol. 172 , 1099–1105 (1990). Article CAS PubMed PubMed Central Google Scholar Kirsch, M. L. et al. Chemotactic methyltransferase promotes adaptation to repellents in Bacillus subtilis . J. Biol. Chem. 268 , 25350–25356 (1993). CAS PubMed Google Scholar Grishanin, R. N., Gauden, D. E. & Armitage, J. P. Photoresponses in Rhodobacter sphaeroides : role of photosynthetic electron transport. J. Bacteriol. 179 , 24–30 (1997). Article CAS PubMed PubMed Central Google Scholar Simms, A. S., Keane, M. G. & Stock, J. B. Multiple forms of the CheB methyltransferase in bacterial chemosensing. J. Biol. Chem. 260 , 10161–10168 (1985). CAS PubMed Google Scholar Surette, M. G. & Stock, J. B. Role of α-helical coiled-coil interactions in receptor dimerization, signaling and adaptation during bacterial chemotaxis. J. Biol. Chem. 271 , 17966–17973 (1996). Article CAS PubMed Google Scholar Download references Author information Authors and Affiliations Departments of Molecular Biology, Princeton University, Princeton, 08544, New Jersey, USA U. Alon & S. Leibler Departments of Physics, Princeton University, Princeton, 08544, New Jersey, USA U. Alon, N. Barkai & S. Leibler Department of Microbiology and Infectious Diseases, Calgary, T2N 4N1, Alberta, Canada M. G. Surette Authors U. Alon View author publications Search author on: PubMed Google Scholar M. G. Surette View author publications Search author on: PubMed Google Scholar N. Barkai View author publications Search author on: PubMed Google Scholar S. Leibler View author publications Search author on: PubMed Google Scholar Corresponding author Correspondence to S. Leibler . Rights and permissions Reprints and permissions About this article Cite this article Alon, U., Surette, M., Barkai, N. et al. Robustness in bacterial chemotaxis. Nature 397 , 168–171 (1999). https://doi.org/10.1038/16483 Download citation Received : 13 October 1998 Accepted : 27 November 1998 Issue date : 14 January 1999 DOI : https://doi.org/10.1038/16483 Share this article Anyone you share the following link with will be able to read this content: Get shareable link Sorry, a shareable link is not currently available for this article. Copy shareable link to clipboard Provided by the Springer Nature SharedIt content-sharing initiative