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Escherichia coli chemotaxis is information limited

Abstract

Organisms acquire and use information from their environment to guide their behaviour. However, it is unclear whether this information quantitatively limits their performance at behavioural tasks. Here we relate information to the ability of Escherichia coli to navigate up chemical gradients, the behaviour known as chemotaxis. First, we derive a theoretical limit on the speed with which cells climb gradients, given the rate at which they acquire information. Next, we measure cells’ gradient-climbing speeds and the rate of information acquisition by their chemotaxis signalling pathway. We find that E. coli cells make behavioural decisions with much less than the one bit required to determine whether they are swimming up the gradient. Some of this information is irrelevant to gradient climbing, and some is lost in communication to behaviour. Despite these limitations, E. coli cells climb gradients at speeds within a factor of two of the theoretical bound. Thus, information can limit the performance of an organism, and sensory–motor pathways may have evolved to efficiently use information acquired from the environment.

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Fig. 1: Information sets an upper limit on chemotaxis performance.
Fig. 2: Measuring the rate of information transfer from signal to intracellular kinase.
Fig. 3: E. coli cells efficiently use information to navigate.

Data availability

Source data are provided with this paper. Source data for the Supplementary figures are contained in a Supplementary Data file. Source data for figures in the main text are provided online with the manuscript.

Code availability

Code to reproduce the main text figures are available with the source data. All the algorithms used are described in detail in the Supplementary Information.

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Acknowledgements

We thank J. Moore and X. Zhang for their help in setting up the experimental assays. We also thank K. Taute and M. Grognot for helpful discussions about the gradient experiments. We thank P. R. ten Wolde for providing detailed feedback on an earlier version of this manuscript; I. Nemenman and S. Ito for helpful discussions; and A. Wachtel, I. Graf, and D. Clark for commenting on the text. We acknowledge T. Shimizu and V. Sourjik for bacteria strains and R. Gomez-Sjoberg, Microfluidics Lab, for providing information and software to control the solenoid valves in the microfluidic setup. This work was supported by NIH awards R01GM106189 (H.H.M., K.K. and T.E.), R01GM138533 (H.H.M., K.K. and T.E.), F32GM131583 (H.H.M.) and R35GM138341 (B.B.M.); by a Yale PEB Seed Grant (T.E. and B.B.M.); and by Simons Investigator Award 624156 (B.B.M.).

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H.H.M. and K.K. contributed equally to this work. H.H.M., K.K., B.B.M. and T.E. designed the research. H.H.M. and B.B.M. derived the theoretical bound with inputs from T.E. and K.K. H.H.M. performed the bacteria-tracking experiments. K.K. performed the single-cell FRET experiments. H.H.M., K.K. and T.E. validated the data. H.H.M., K.K., B.B.M. and T.E. discussed the data analysis. H.H.M. and K.K. performed the data analysis. H.H.M., K.K., B.B.M. and T.E. wrote the initial draft and all the revisions.

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Correspondence to B. B. Machta or T. Emonet.

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Peer review information Nature Physics thanks Lev Tsimring and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Supplementary Figs. 1–10, Table 1 and text.

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Supplementary Data

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Source data and code for generating the figure, as well as a README file.

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Source data and code for generating the figure, as well as a README file.

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Source data and code for generating the figure, as well as a README file.

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Mattingly, H.H., Kamino, K., Machta, B.B. et al. Escherichia coli chemotaxis is information limited. Nat. Phys. 17, 1426–1431 (2021). https://doi.org/10.1038/s41567-021-01380-3

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