Inter-receptor communication through arrays of bacterial chemoreceptors


The sensing mechanisms of chemotactic bacteria allow them to respond sensitively to stimuli. Escherichia coli, for example, respond to changes in chemoattractant concentration of less than 10% over a range spanning six orders of magnitude1,2. Sensitivity over this range depends on a nonlinear relationship between ligand concentration and output response3. At low ligand concentrations, substantial amplification of the chemotactic signal is required; however, the mechanism responsible for this amplification remains unclear. Here we demonstrate that inter-receptor communication within a lattice4,5 acts to amplify and integrate sensory information. Synthetic multivalent ligands that interact through the low-abundance, galactose-sensing receptor Trg stabilize large clusters of chemoreceptors and markedly enhance signal output from these enforced clusters. On treatment with multivalent ligands, the response to the attractant serine is amplified by at least 100-fold. This amplification requires a full complement of chemoreceptors; deletion of the aspartate (Tar) or dipeptide (Tap) receptors diminishes the amplification of the serine response. These results demonstrate that the entire array is involved in sensing. This mode of information exchange has general implications for the processing of signals by cellular receptors.

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Figure 1: Effects of chemoattractants on the behaviour of E. coli and the localization of MCPs.
Figure 2: Tsr is included in clusters formed on treatment with galactose-bearing ligand 3.
Figure 3: Response of wild-type E. coli (AW405) to chemoattractants after pre-treatment with buffer or ligands 1–3 at a galactose residue concentration of 10 µM.
Figure 4: Response of E. coli to serine.


  1. 1

    Mesibov, R., Ordal, G. W. & Adler, J. The range of attractant concentrations for bacterial chemotaxis and the threshold and size over this range. J. Gen. Physiol. 62, 203–223 (1973).

    CAS  Article  Google Scholar 

  2. 2

    Adler, J., Hazelbauer, G. L. & Dahl, M. M. Chemotaxis towards sugars in Escherichia coli. J. Bacteriol. 115, 824–847 (1973).

    CAS  PubMed  PubMed Central  Google Scholar 

  3. 3

    Jasuja, R., Yu-Lin,, Trentham, D. R. & Khan, S. Response tuning in bacterial chemotaxis. Proc. Natl Acad. Sci. USA 96, 11346–11351 (1999).

    Google Scholar 

  4. 4

    Duke, T. A. J. & Bray, D. Heightened sensitivity of a lattice of membrane receptors. Proc. Natl Acad. Sci. USA 96, 10104–10108 (1999).

    ADS  CAS  Article  Google Scholar 

  5. 5

    Bray, D., Levin, M. D. & Morton-Firth, C. J. Receptor clustering as a cellular mechanism to control sensitivity. Nature 393, 85–88 (1998).

    ADS  CAS  Article  Google Scholar 

  6. 6

    Bren, A. & Eisenbach, M. How signals are heard during bacterial chemotaxis: Protein–protein interactions in sensory signal perception. J. Bacteriol. 182, 6865–6873 (2000).

    CAS  Article  Google Scholar 

  7. 7

    Barkai, N. & Leibler, S. Robustness in simple biochemical networks. Nature 387, 913–917 (1997).

    ADS  CAS  Article  Google Scholar 

  8. 8

    Hazelbauer, G. L. & Engström, P. Multiple forms of methyl-accepting chemotaxis proteins distinguished by a factor in addition to multiple methylation. J. Bacteriol. 145, 35–42 (1981).

    CAS  PubMed  PubMed Central  Google Scholar 

  9. 9

    Slocum, M. K. & Parkinson, J. S. Genetics of methyl-accepting chemotaxis proteins in Escherichia coli: organization of the tar region. J. Bacteriol. 155, 565–577 (1983).

    CAS  PubMed  PubMed Central  Google Scholar 

  10. 10

    Gegner, J. A., Graham, D. R., Roth, A. F. & Dahlquist, F. W. Assembly of an MCP receptor, CheW, and kinase CheA complex in the bacterial chemotaxis signal transduction pathway. Cell 70, 975–982 (1992).

    CAS  Article  Google Scholar 

  11. 11

    Liu, Y., Levit, M., Lurz, R., Surette, M. G. & Stock, J. B. Receptor-mediated protein kinase activation and the mechanism of transmembrane signaling in bacterial chemotaxis. EMBO J. 16, 7231–7240 (1997).

    CAS  Article  Google Scholar 

  12. 12

    Schuster, S. C., Swanson, R. V., Alex, L. A., Bourret, R. B. & Simon, M. I. Assembly and function of a quaternary signal transduction complex by surface plasmon resonance. Nature 365, 343–347 (1993).

    ADS  CAS  Article  Google Scholar 

  13. 13

    Ottemann, K. M., Xiao, W., Shin, Y.-K. & Koshland, D. E. Jr A piston model for transmembrane signaling of the aspartate receptor. Science 285, 1751–1754 (1999).

    CAS  Article  Google Scholar 

  14. 14

    Maddock, J. R. & Shapiro, L. Polar location of the chemoreceptor complex in the Escherichia coli cell. Science 259, 1717–1723 (1993).

    ADS  CAS  Article  Google Scholar 

  15. 15

    Gestwicki, J. E. et al. Evolutionary conservation of methyl-accepting chemotaxis protein location in Bacteria and Archaea. J. Bacteriol. 182, 6499–6502 (2000).

    CAS  Article  Google Scholar 

  16. 16

    Barnakov, A. N., Barnakov, L. A. & Hazelbauer, G. L. Comparison in vitro of a high- and a low-abundance chemoreceptor of Escherichia coli: similar kinase activation but different methyl-accepting activities. J. Bacteriol. 180, 6713–6718 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  17. 17

    Li, J., Li, G. & Weis, R. M. The serine chemoreceptor from Escherichia coli is methylated through an inter-dimer process. Biochemistry 36, 11851–11857 (1997).

    CAS  Article  Google Scholar 

  18. 18

    Gardina, P. J. & Manson, M. D. Attractant signaling by an aspartate chemoreceptor dimer with a single cytoplasmic domain. Science 274, 425–426 (1996).

    ADS  CAS  Article  Google Scholar 

  19. 19

    Tatsuno, I., Homma, M., Oosawa, K. & Kawagishi, I. Signaling by the Escherichia coli aspartate chemoreceptor Tar with a single cytoplasmic domain per dimer. Science 274, 423–425 (1996).

    ADS  CAS  Article  Google Scholar 

  20. 20

    Yeh, J. I., Biemann, H.-P., Pandit, J., Koshland, D. E. & Kim, S.-H. The three-dimensional structure of the ligand-binding domain of a wild-type chemotaxis receptor. J. Biol. Chem. 268, 9787–9792 (1993).

    CAS  PubMed  Google Scholar 

  21. 21

    Trnka, T. M. & Grubbs, R. H. The development of L2X2Ru = CHR olefin metathesis catalysts: an organometallic success story. Acc. Chem. Res. 34, 18–29 (2001).

    CAS  Article  Google Scholar 

  22. 22

    Gestwicki, J. E., Strong, L. E. & Kiessling, L. L. Tuning chemotactic responses using synthetic multivalent ligands. Chem. Biol. 7, 583–591 (2000).

    CAS  Article  Google Scholar 

  23. 23

    Gestwicki, J. E. et al. Designed potent multivalent chemoattractants for Escherichia coli. Bioorg. Med. Chem. 9, 2387–2393 (2001).

    CAS  Article  Google Scholar 

  24. 24

    Sager, B. M., Sekelsky, J. J., Matsumura, P. & Adler, J. Use of a computer to assay motility in bacteria. Anal. Biochem. 173, 271–277 (1988).

    CAS  Article  Google Scholar 

  25. 25

    Parkinson, J. S. & Houts, S. E. Isolation and behavior of Escherichia coli deletion mutants lacking chemotaxis functions. J. Bacteriol. 151, 106–113 (1982).

    CAS  PubMed  PubMed Central  Google Scholar 

  26. 26

    Hazelbauer, G. L., Mesibov, R. E. & Adler, J. Escherichia coli mutants defective in chemotaxis toward specific chemicals. Proc. Natl Acad. Sci. USA 64, 1300–1307 (1969).

    ADS  CAS  Article  Google Scholar 

  27. 27

    Yin, C. C. & Lai, F. A. Intrinsic lattice formation by ryanodine receptor calcium-release channel. Nature Cell Biol. 2, 669–671 (2000).

    CAS  Article  Google Scholar 

  28. 28

    Matsuuchi, L. & Gold, M. R. New views of BCR structure and organization. Curr. Opin. Immunol. 13, 270–277 (2001).

    CAS  Article  Google Scholar 

  29. 29

    Delon, J. & Germain, R. N. Information transfer at the immunological synapse. Curr. Biol. 10, R923–R933 (2000).

    CAS  Article  Google Scholar 

  30. 30

    Chan, C., George, A. J. T. & Stark, J. Cooperative enhancement of specificity in a lattice of T cell receptors. Proc. Natl Acad. Sci. USA 98, 5758–5763 (2001).

    ADS  CAS  Article  Google Scholar 

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We thank J. Adler for supplying E. coli strains AW405, AW550, AW518 and AW701, and for advice. We thank J. S. Parkinson for E. coli strains RP1078, RP5854 and RP2361, and for anti-MCP antibodies. This work was supported by the National Institutes of Health (NIH). J.E.G. acknowledges the NIH Biotechnology Training Grant for support.

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Correspondence to Laura L. Kiessling.

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Gestwicki, J., Kiessling, L. Inter-receptor communication through arrays of bacterial chemoreceptors. Nature 415, 81–84 (2002).

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