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Making sense of it all: bacterial chemotaxis

Key Points

  • Bacterial chemotaxis is the biasing of movement towards environments that contain higher concentrations of beneficial, or lower concentrations of toxic, chemicals. The signalling pathway that is involved has long been viewed as a paradigm of histidine–aspartate-phosphorelay signalling, and is one of the most well-understood physiological processes in biology.

  • The pathway is composed of chemoreceptors, the histidine protein kinase chemotaxis protein (Che)A and two diffusable response regulators (CheY and CheB). CheY controls flagellar motor switching, whereas CheB controls chemoreceptor adaptation.

  • The chemoreceptors and other proteins of the chemotaxis signalling pathway localize to specific regions of the cell as large higher-order arrays. This is thought to allow sensitivity and gain — cells can respond to a change of just a few molecules over background concentrations that can vary over five orders of magnitude.

  • Biochemical, cellular-concentration and molecular-structure data for the various components of this pathway are available. These data have allowed various mathematical and computational models to be generated and tested.

  • Many bacterial species have several chemosensory pathways, as well as further components that might be expressed under particular environmental conditions to allow bacteria to tune their responses to a specific environment.

  • Chemotaxis is thought to be involved in pathogenicity, symbiosis, biofilm formation and stability, and in maintaining bacteria in their optimal environmental niche. The correct interplay between chemotaxis and other sensing systems is essential for bacterial survival in a changing environment.

Abstract

Bacteria must be able to respond to a changing environment, and one way to respond is to move. The transduction of sensory signals alters the concentration of small phosphorylated response regulators that bind to the rotary flagellar motor and cause switching. This simple pathway has provided a paradigm for sensory systems in general. However, the increasing number of sequenced bacterial genomes shows that although the central sensory mechanism seems to be common to all bacteria, there is added complexity in a wide range of species.

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Figure 1: The domain organization of selected histidine–aspartate-phosphorelay systems.
Figure 2: Schematic diagram of the chemosensory system of Escherichia coli.
Figure 3: The structures of components of the chemosensory system of Escherichia coli.
Figure 4: Chemotaxis-protein localization.

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References

  1. West, A. H. & Stock, A. M. Histidine kinases and response regulator proteins in two-component signaling systems. Trends Biochem. Sci. 26, 369–376 (2001). A good review of the biochemical and structural aspects of chemotaxis and other two-component signalling systems.

    CAS  PubMed  Google Scholar 

  2. Maeda, T., Wurglermurphy, S. M. & Saito, H. A two-component system that regulates an osmosensing MAP kinase cascade in yeast. Nature 369, 242–245 (1994).

    CAS  PubMed  Google Scholar 

  3. Nagahashi, S. et al. Isolation of CaSLN1 and CaNIK1, the genes for osmosensing histidine kinase homologues, from the pathogenic fungus Candida albicans. Microbiology 144, 425–432 (1998).

    CAS  PubMed  Google Scholar 

  4. Schuster, S. C., Noegel, A. A., Oehme, F., Gerisch, G. & Simon, M. I. The hybrid histidine kinase DokA is part of the osmotic response system of Dictyostelium. EMBO J. 15, 3880–3889 (1996).

    CAS  PubMed  PubMed Central  Google Scholar 

  5. Wilkinson, J. Q., Lanahan, M. B., Yen, H. C., Giovannoni, J. J. & Klee, H. J. An ethylene-inducible component of signal transduction encoded by never-ripe. Science 270, 1807–1809 (1995).

    CAS  PubMed  Google Scholar 

  6. Ashby, M. K. Survey of the number of two-component response regulator genes in the complete and annotated genome sequences of prokaryotes. FEMS Microbiol. Lett. 231, 277–281 (2004).

    CAS  PubMed  Google Scholar 

  7. Stock, A. M., Robinson, V. L. & Goudreau, P. N. Two-component signal transduction. Annu. Rev. Biochem. 69, 183–215 (2000).

    CAS  PubMed  Google Scholar 

  8. Inouye, M. & Dutta, R. Histidine Kinases in Signal Transduction (Academic Press, London, UK, 2003).

    Google Scholar 

  9. Potter, C. A. et al. Expression, purification and characterisation of full-length histidine protein kinase RegB from Rhodobacter sphaeroides. J. Mol. Biol. 320, 201–213 (2002).

    CAS  PubMed  Google Scholar 

  10. Armitage, J. P. Bacterial tactic responses. Adv. Microb. Physiol. 41, 229–289 (1999).

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  12. Faguy, D. M. & Jarrell, K. F. A twisted tale: the origin and evolution of motility and chemotaxis in prokaryotes. Microbiology 145, 279–281 (1999).

    PubMed  Google Scholar 

  13. Schnitzer, M. J., Block, S. M., Berg, H. C. & Purcell, E. M. Biology of the Chemotactic Response (Armitage, J. P. & Lackie, J. M. eds) 15–34 (Cambridge Univ. Press, UK, 1990).

    Google Scholar 

  14. Thar, R. & Kühl, M. Bacteria are not too small for spatial sensing of chemical gradients: an experimental evidence. Proc. Natl Acad. Sci. USA 100, 5748–5753 (2003).

    CAS  PubMed  PubMed Central  Google Scholar 

  15. Turner, L., Ryu, W. S. & Berg, H. C. Real-time imaging of fluorescent flagellar filaments. J. Bacteriol. 182, 2793–2801 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  16. Armitage, J. P. & Schmitt, R. Bacterial chemotaxis: Rhodobacter sphaeroides and Sinorhizobium meliloti — variations on a theme? Microbiology 143, 3671–3682 (1997).

    CAS  PubMed  Google Scholar 

  17. Adler, J. Chemoreceptors in bacteria. Science 166, 1588–1597 (1969).

    CAS  PubMed  Google Scholar 

  18. Levin, M. D., Morton, F. C., Abouhamad, W. N., Bourret, R. B. & Bray, D. Origins of individual swimming behavior in bacteria. Biophys. J. 74, 175–181 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  19. Alon, U., Surette, M. G., Barkai, N. & Leibler, S. Robustness in bacterial chemotaxis. Nature 397, 168–171 (1999). A mathematical consideration of the processes of adaptation and robustness in the bacterial chemotaxis pathway.

    CAS  PubMed  Google Scholar 

  20. Kim, S. H., Wang, W. R. & Kim, K. K. Dynamic and clustering model of bacterial chemotaxis receptors: structural basis for signaling and high sensitivity. Proc. Natl Acad. Sci. USA 99, 11611–11615 (2002).

    CAS  PubMed  PubMed Central  Google Scholar 

  21. Sourjik, V. & Berg, H. C. Functional interactions between receptors in bacterial chemotaxis. Nature 428, 437–441 (2004).

    CAS  PubMed  Google Scholar 

  22. Sourjik, V. & Berg, H. C. Receptor sensitivity in bacterial chemotaxis. Proc. Natl Acad. Sci. USA 99, 123–127 (2002). References 21 and 22 use fluorescence resonance energy transfer to assay the interactions between chemoreceptors in E. coli and between CheY–P and CheZ to explain sensitivity and gain in the chemotaxis pathway.

    CAS  PubMed  Google Scholar 

  23. Kim, C., Jackson, M., Lux, R. & Khan, S. Determinants of chemotactic signal amplification in Escherichia coli. J. Mol. Biol. 307, 119–135 (2001).

    CAS  PubMed  Google Scholar 

  24. Hess, J. F., Oosawa, K., Kaplan, N. & Simon, M. I. Phosphorylation of three proteins in the signalling pathway of bacterial chemotaxis. Cell 53, 79–87 (1988). An early report showing that the phosphorylation of chemotaxis proteins is a mechanism for signal transduction.

    CAS  PubMed  Google Scholar 

  25. Anand, G. S., Goudreau, P. N. & Stock, A. M. Activation of methylesterase CheB: evidence of a dual role for the regulatory domain. Biochemistry 37, 14038–14047 (1998).

    CAS  PubMed  Google Scholar 

  26. Welch, M., Oosawa, K., Aizawa, S. -I. & Eisenbach, M. Phosphorylation-dependent binding of a signal molecule to the flagellar switch of bacteria. Proc. Natl Acad. Sci. USA 90, 8787–8791 (1993).

    CAS  PubMed  PubMed Central  Google Scholar 

  27. Toker, A. S. & Macnab, R. M. Distinct regions of bacterial flagellar switch protein FliM interact with FliG, FliN and CheY. J. Mol. Biol. 273, 623–634 (1997).

    CAS  PubMed  Google Scholar 

  28. McEvoy, M. M., Bren, A., Eisenbach, M. & Dahlquist, F. W. Identification of the binding interfaces on CheY for two of its targets, the phosphatase CheZ and the flagellar switch protein FliM. J. Mol. Biol. 289, 1423–1433 (1999).

    CAS  PubMed  Google Scholar 

  29. Sourjik, V. & Berg, H. C. Binding of the Escherichia coli response regulator CheY to its target measured in vivo by fluorescence resonance energy transfer. Proc. Natl Acad. Sci. USA 99, 12669–12674 (2002).

    CAS  PubMed  PubMed Central  Google Scholar 

  30. Morgan, D. G., Baumgartner, J. B. & Hazelbauer, G. L. Proteins antigenically related to methyl-accepting chemotaxis proteins of Escherichia coli detected in a wide range of bacterial species. J. Bacteriol. 175, 133–140 (1993).

    CAS  PubMed  PubMed Central  Google Scholar 

  31. Falke, J. J. & Hazelbauer, G. L. Transmembrane signaling in bacterial chemoreceptors. Trends Biochem. Sci. 26, 257–265 (2001).

    CAS  PubMed  PubMed Central  Google Scholar 

  32. Yeh, J. I. et al. High resolution structures of the ligand binding domain of the wild type aspartate receptor. J. Mol. Biol. 262, 186–201 (1996).

    CAS  PubMed  Google Scholar 

  33. Kim, K. K., Yokota, H. & Kim, S. H. Four-helical-bundle structure of the cytoplasmic domain of a serine chemotaxis receptor. Nature 400, 787–792 (1999).

    CAS  PubMed  Google Scholar 

  34. Milburn, M. V. et al. Structural changes in a transmembrane receptor — crystal structures of the ligand domain of aspartate chemotaxis receptor with and without aspartate. Biochemistry 31, 2192 (1992).

    Google Scholar 

  35. Mowbray, S. L. & Koshland, D. E. Jr. Additive and independent responses to a single receptor: aspartate and maltose stimuli on the Tar protein. Cell 50, 171–180 (1987).

    CAS  PubMed  Google Scholar 

  36. Beel, B. D. & Hazelbauer, G. L. Substitutions in the periplasmic domain of low-abundance chemoreceptor Trg that induce or reduce transmembrane signaling: kinase activation and context effects. J. Bacteriol. 183, 671–679 (2001).

    CAS  PubMed  PubMed Central  Google Scholar 

  37. Isaac, B., Gallagher, G. J., Balazs, Y. S. & Thompson, L. K. Site-directed rotational resonance solid-state NMR distance measurements probe structure and mechanism in the transmembrane domain of the serine bacterial chemoreceptor. Biochemistry 41, 3025–3036 (2002).

    CAS  PubMed  Google Scholar 

  38. Murphy, O. J., Kovacs, F. A., Sicard, E. L. & Thompson, L. K. Site-directed solid-state NMR measurement of a ligand-induced conformational change in the serine bacterial chemoreceptor. Biochemistry 40, 1358–1366 (2001).

    CAS  PubMed  Google Scholar 

  39. 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  PubMed  Google Scholar 

  40. Ames, P. & Parkinson, J. S. Transmembrane signaling by bacterial chemoreceptors: E. coli transducers with locked signal output. Cell 55, 817–826 (1988).

    CAS  PubMed  Google Scholar 

  41. 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).

    CAS  PubMed  Google Scholar 

  42. Storch, K. F., Rudolph, J. & Oesterhelt, D. Car: a cytoplasmic sensor responsible for arginine chemotaxis in the archaeon Halobacterium salinarum. EMBO J. 18, 1146–1158 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  43. Wadhams, G. H. et al. TlpC, a novel chemotaxis protein in Rhodobacter sphaeroides, localizes to a discrete region in the cytoplasm. Mol. Microbiol. 46, 1211–1221 (2002).

    CAS  PubMed  Google Scholar 

  44. Nishiyama, S., Maruyama, I. N., Homma, M. & Kawagishi, I. Inversion of thermosensing property of the bacterial receptor Tar by mutations in the second transmembrane region. J. Mol. Biol. 286, 1275–1284 (1999).

    CAS  PubMed  Google Scholar 

  45. Appleman, J. A., Chen, L. L. & Stewart, V. Probing conservation of HAMP linker structure and signal transduction mechanism through analysis of hybrid sensor kinases. J. Bacteriol. 185, 4872–4882 (2003).

    CAS  PubMed  PubMed Central  Google Scholar 

  46. Aravind, L. & Ponting, C. P. The cytoplasmic helical linker domain of receptor histidine kinase and methyl-accepting proteins is common to many prokaryotic signalling proteins. FEMS Microbiol. Lett. 176, 111–116 (1999).

    CAS  PubMed  Google Scholar 

  47. Weis, R. M. & Koshland, D. E. Jr. Reversible receptor methylation is essential for normal chemotaxis of Escherichia coli in gradients of aspartic acid. Proc. Natl Acad. Sci. USA 85, 83–87 (1988).

    CAS  PubMed  PubMed Central  Google Scholar 

  48. Kehry, M. R., Bond, M. W., Hunkapiller, M. W. & Dahlquist, F. W. Enzymatic deamidation of methyl-accepting chemotaxis proteins in Escherichia coli catalyzed by the cheB gene product. Proc. Natl Acad. Sci. USA 80, 3599–3603 (1983).

    CAS  PubMed  PubMed Central  Google Scholar 

  49. Wu, J. G., Li, J. Y., Li, G. Y., Long, D. G. & Weis, R. M. The receptor binding site for the methyltransferase of bacterial chemotaxis is distinct from the sites of methylation. Biochemistry 35, 4984–4993 (1996).

    CAS  PubMed  Google Scholar 

  50. Barnakov, A. N., Barnakova, 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 

  51. Le Moual, H., Quang, T. & Koshland, D. E. Jr. Methylation of the Escherichia coli chemotaxis receptors: intra- and interdimer mechanisms. Biochemistry 36, 13441–13448 (1997).

    CAS  PubMed  Google Scholar 

  52. Maddock, J. R. & Shapiro, L. Polar location of the chemoreceptor complex in the Escherichia coli cell. Science 259, 1717–1723 (1993). The use of immunogold electron microscopy to show for the first time that chemoreceptors cluster at the poles of bacterial cells.

    CAS  PubMed  Google Scholar 

  53. Wadhams, G. H., Martin, A. C. & Armitage, J. P. Identification and localization of a methyl-accepting chemotaxis protein in Rhodobacter sphaeroides. Mol. Microbiol. 36, 1222–1233 (2000).

    CAS  PubMed  Google Scholar 

  54. Thomason, P. A., Wolanin, P. M. & Stock, J. B. Signal transduction: receptor clusters as information processing arrays. Curr. Biol. 12, R399–R401 (2002).

    CAS  PubMed  Google Scholar 

  55. Sourjik, V. & Berg, H. C. Localization of components of the chemotaxis machinery of Escherichia coli using fluorescent protein fusions. Mol. Microbiol. 37, 740–751 (2000).

    CAS  PubMed  Google Scholar 

  56. Martin, A. C., Wadhams, G. H. & Armitage, J. P. The roles of the multiple CheW and CheA homologues in chemotaxis and in chemoreceptor localization in Rhodobacter sphaeroides. Mol. Microbiol. 40, 1261–1272 (2001).

    CAS  PubMed  Google Scholar 

  57. Homma, M., Shiomi, D., Homma, M. & Kawagishi, I. Attractant binding alters arrangement of chemoreceptor dimers within its cluster at a cell pole. Proc. Natl Acad. Sci. USA 101, 3462–3467 (2004).

    CAS  PubMed  PubMed Central  Google Scholar 

  58. Studdert, C. A. & Parkinson, J. S. Crosslinking snapshots of bacterial chemoreceptor squads. Proc. Natl Acad. Sci. USA 101, 2117–2122 (2004).

    CAS  PubMed  PubMed Central  Google Scholar 

  59. Wolanin, P. M. & Stock, J. B. Bacterial chemosensing: cooperative molecular logic. Curr. Biol. 14, R486–R487 (2004).

    CAS  PubMed  Google Scholar 

  60. Bray, D., Levin, M. D. & Morton, F. C. Receptor clustering as a cellular mechanism to control sensitivity. Nature 393, 85–88 (1998). One of the first papers to propose that chemoreceptor clustering could explain the sensitivity and gain in the chemotaxis pathway.

    CAS  PubMed  Google Scholar 

  61. Levit, M. N., Grebe, T. W. & Stock, J. B. Organization of the receptor-kinase signaling array that regulates Escherichia coli chemotaxis. J. Biol. Chem. 277, 36748–36754 (2002).

    CAS  PubMed  Google Scholar 

  62. Lamanna, A. C. et al. Conserved amplification of chemotactic responses through chemoreceptor interactions. J. Bacteriol. 184, 4981–4987 (2002).

    CAS  PubMed  PubMed Central  Google Scholar 

  63. Ames, P., Studdert, C. A., Reiser, R. H. & Parkinson, J. S. Collaborative signaling by mixed chemoreceptor teams in Escherichia coli. Proc. Natl Acad. Sci. USA 99, 7060–7065 (2002).

    CAS  PubMed  PubMed Central  Google Scholar 

  64. Li, M. & Hazelbauer, G. L. Cellular stoichiometries of the components of the chemotaxis signaling complex. J. Bacteriol 186, 3687–3694 (2004). A quantitative western-blot analysis of chemotaxis proteins in cells that were grown under different growth conditions, which showed that although the absolute numbers of the signalling components vary, the stoichiometry between them remains relatively constant.

    CAS  PubMed  PubMed Central  Google Scholar 

  65. Shimizu, T. S. et al. Molecular model of a lattice of signalling proteins involved in bacterial chemotaxis. Nature Cell Biol. 2, 792–796 (2000).

    CAS  PubMed  Google Scholar 

  66. Rebbapragada, A. et al. The Aer protein and the serine chemoreceptor Tsr independently sense intracellular energy levels and transduce oxygen, redox, and energy signals for Escherichia coli behavior. Proc. Natl Acad. Sci. USA 94, 10541–10546 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  67. Bibikov, S. I., Barnes, L. A., Gitin, Y. & Parkinson, J. S. Domain organization and flavin adenine dinucleotide-binding determinants in the aerotaxis signal transducer Aer of Escherichia coli. Proc. Natl Acad. Sci. USA 97, 5830–5835 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  68. Fu, R., Wall, J. D. & Voordouw, G. DcrA, a c-type heme-containing methyl-accepting chemotaxis protein from Desulfovibrio vulgaris Hildenborough, senses the oxygen concentration or redox potential of the environment. J. Bacteriol. 176, 344–350 (1994).

    CAS  PubMed  PubMed Central  Google Scholar 

  69. Hou, S. et al. Myoglobin-like aerotaxis transducers in Archaea and bacteria. Nature 403, 540–544 (2000).

    CAS  PubMed  Google Scholar 

  70. Lux, R. et al. Elucidation of a PTS-carbohydrate chemotactic signal pathway in Escherichia coli using a time-resolved behavioral assay. Mol. Biol. Cell 10, 1133–1146 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  71. Boukhvalova, M., VanBruggen, R. & Stewart, R. C. CheA kinase and chemoreceptor interaction surfaces on CheW. J. Biol. Chem. 277, 23596–23603 (2002).

    CAS  PubMed  Google Scholar 

  72. Griswold, I. J. et al. The solution structure and interactions of CheW from Thermotoga maritima. Nature Struct. Biol. 9, 121–125 (2002).

    CAS  PubMed  Google Scholar 

  73. Shah, D. S. et al. Identification of a fourth cheY gene in Rhodobacter sphaeroides and interspecies interaction within the bacterial chemotaxis signal transduction pathway. Mol. Microbiol. 35, 101–112 (2000).

    CAS  PubMed  Google Scholar 

  74. Hamblin, P. A., Bourne, N. A. & Armitage, J. P. Characterization of the chemotaxis protein CheW from Rhodobacter sphaeroides and its effect on the behaviour of Escherichia coli. Mol. Microbiol. 24, 41–51 (1997).

    CAS  PubMed  Google Scholar 

  75. Morrison, T. B. & Parkinson, J. S. A fragment liberated from the Escherichia coli CheA kinase that blocks stimulatory, but not inhibitory, chemoreceptor signaling. J. Bacteriol. 179, 5543–5550 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  76. Mourey, L. et al. Crystal structure of the CheA histidine phosphotransfer domain that mediates response regulator phosphorylation in bacterial chemotaxis. J. Biol. Chem. 276, 31074–31082 (2001).

    CAS  PubMed  Google Scholar 

  77. Bilwes, A. M., Alex, L. A., Crane, B. R. & Simon, M. I. Structure of CheA, a signal-transducing histidine kinase. Cell 96, 131–141 (1999).

    CAS  PubMed  Google Scholar 

  78. Bourret, R. B., Davagnino, J. & Simon, M. I. The carboxy-terminal portion of the CheA kinase mediates regulation of autophosphorylation by transducer and CheW. J. Bacteriol. 175, 2097–2101 (1993).

    CAS  PubMed  PubMed Central  Google Scholar 

  79. Levit, M. N., Liu, Y. & Stock, J. B. Mechanism of CheA protein kinase activation in receptor signaling complexes. Biochemistry 38, 6651–6658 (1999).

    CAS  PubMed  Google Scholar 

  80. Li, J. Y., Swanson, R. V., Simon, M. I. & Weis, R. M. The response regulators CheB and CheY exhibit competitive binding to the kinase CheA. Biochemistry 34, 14626–14636 (1995).

    CAS  PubMed  Google Scholar 

  81. Welch, M., Chinardet, N., Mourey, L., Birck, C. & Samama, J. P. Structure of the CheY-binding domain of histidine kinase CheA in complex with CheY. Nature Struct. Biol. 5, 25–29 (1998).

    CAS  PubMed  Google Scholar 

  82. Stewart, R. C., Jahreis, K. & Parkinson, J. S. Rapid phosphotransfer to CheY from a CheA protein lacking the CheY-binding domain. Biochemistry 39, 13157–13165 (2000).

    CAS  PubMed  Google Scholar 

  83. Hess, J. F., Bourret, R. B. & Simon, M. I. Histidine phosphorylation and phosphoryl group transfer in bacterial chemotaxis. Nature 336, 139–143 (1988).

    CAS  PubMed  Google Scholar 

  84. Halkides, C. J. et al. The 1.9 Å resolution crystal structure of phosphono-CheY, an analogue of the active form of the response regulator, CheY. Biochemistry 39, 5280–5286 (2000).

    CAS  PubMed  Google Scholar 

  85. Lee, S. Y. et al. Crystal structure of activated CheY — comparison with other activated receiver domains. J. Biol. Chem. 276, 16425–16431 (2001).

    CAS  PubMed  Google Scholar 

  86. Cho, H. S. et al. NMR structure of activated CheY. J. Mol. Biol. 297, 543–551 (2000).

    CAS  PubMed  Google Scholar 

  87. Bren, A. & Eisenbach, M. The N terminus of the flagellar switch protein, FliM, is the binding domain for the chemotactic response regulator, CheY. J. Mol. Biol. 278, 507–514 (1998).

    CAS  PubMed  Google Scholar 

  88. Sagi, Y., Khan, S. & Eisenbach, M. Binding of the chemotaxis response regulator CheY to the isolated, intact switch complex of the bacterial flagellar motor — lack of cooperativity. J. Biol. Chem. 278, 25867–25871 (2003). Showed that CheY–P binds to the switch component of the bacterial flagellar motor in a non-cooperative manner, which indicates that any amplification that occurs at the motor occurs after CheY–P binding.

    CAS  PubMed  Google Scholar 

  89. Lee, S. Y. et al. Crystal structure of an activated response regulator bound to its target. Nature Struct. Biol. 8, 52–56 (2001).

    CAS  PubMed  Google Scholar 

  90. Da Re, S. S., Deville-Bonne, D., Tolstykh, T., Veron, M. & Stock, J. B. Kinetics of CheY phosphorylation by small molecule phosphodonors. FEBS Lett. 457, 323–326 (1999).

    CAS  PubMed  Google Scholar 

  91. Barak, R. & Eisenbach, M. Acetylation of the response regulator, CheY, is involved in bacterial chemotaxis. Mol. Microbiol. 40, 731–743 (2001).

    CAS  PubMed  Google Scholar 

  92. Blat, Y. & Eisenbach, M. Oligomerization of the phosphatase CheZ upon interaction with the phosphorylated form of CheY — the signal protein of bacterial chemotaxis. J. Biol. Chem. 271, 1226–1231 (1996).

    CAS  PubMed  Google Scholar 

  93. Blat, Y. & Eisenbach, M. Mutants with defective phosphatase activity show no phosphorylation-dependent oligomerization of CheZ. The phosphatase of bacterial chemotaxis. J. Biol. Chem. 271, 1232–1236 (1996).

    CAS  PubMed  Google Scholar 

  94. Zhao, R., Collins, E. J., Bourret, R. B. & Silversmith, R. E. Structure and catalytic mechanism of the E. coli chemotaxis phosphatase CheZ. Nature Struct. Biol. 9, 570–575 (2002).

    CAS  PubMed  Google Scholar 

  95. Sourjik, V. & Schmitt, R. Phosphotransfer between CheA, CheY1, and CheY2 in the chemotaxis signal transduction chain of Rhizobium meliloti. Biochemistry 37, 2327–2335 (1998). Identified an alternative signal-termination mechanism, which uses a phosphate sink in a bacterial species that lacks CheZ.

    CAS  PubMed  Google Scholar 

  96. Karatan, E., Saulmon, M. M., Bunn, M. W. & Ordal, G. W. Phosphorylation of the response regulator CheV is required for adaptation to attractants during Bacillus subtilis chemotaxis. J. Biol. Chem. 276, 43618–43626 (2001).

    CAS  PubMed  Google Scholar 

  97. Pittman, M. S., Goodwin, M. & Kelly, D. J. Chemotaxis in the human gastric pathogen Helicobacter pylori: different roles for CheW and the three CheV paralogues, and evidence for CheV2 phosphorylation. Microbiology 147, 2493–2504 (2001).

    CAS  PubMed  Google Scholar 

  98. Jiang, Z. Y. & Bauer, C. E. Analysis of a chemotaxis operon from Rhodospirillum centenum. J. Bacteriol. 179, 5712–5719 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  99. Porter, S. L. & Armitage, J. P. Phosphotransfer in Rhodobacter sphaeroides chemotaxis. J. Mol. Biol. 324, 35–45 (2002). Showed that different CheA proteins from R. sphaeroides differentially phosphorylate specific RRs.

    CAS  PubMed  Google Scholar 

  100. Springer, W. R. & Koshland, D. E. Jr. Identification of a protein methyltransferase as the cheR gene product in the bacterial sensing system. Proc. Natl Acad. Sci. USA 74, 533–537 (1977).

    CAS  PubMed  PubMed Central  Google Scholar 

  101. Kehry, M. R. & Dahlquist, F. W. Adaptation in bacterial chemotaxis: CheB-dependent modification permits additional methylations of sensory transducing proteins. Cell 29, 761–772 (1982).

    CAS  PubMed  Google Scholar 

  102. Kehry, M. R., Doak, T. G. & Dahlquist, F. W. Sensory adaptation in bacterial chemotaxis — regulation of demethylation. J. Bacteriol. 163, 983–990 (1985).

    CAS  PubMed  PubMed Central  Google Scholar 

  103. Djordjevic, S. & Stock, A. M. Chemotaxis receptor recognition by protein methyltransferase CheR. Nature Struct. Biol. 5, 446–450 (1998).

    CAS  PubMed  Google Scholar 

  104. Djordjevic, S. & Stock, A. M. Crystal structure of the chemotaxis receptor methyltransferase CheR suggests a conserved structural motif for binding S-adenosylmethionine. Structure 5, 545–558 (1997).

    CAS  PubMed  Google Scholar 

  105. Shiomi, D., Zhulin, I. B., Homma, M. & Kawagishi, I. Dual recognition of the bacterial chemoreceptor by chemotaxis-specific domains of the CheR methyltransferase. J. Biol. Chem. 277, 42325–42333 (2002).

    CAS  PubMed  Google Scholar 

  106. Djordjevic, S., Goudreau, P. N., Xu, Q., Stock, A. M. & West, A. H. Structural basis for methylesterase CheB regulation by a phosphorylation-activated domain. Proc. Natl Acad. Sci. USA 95, 1381–1386 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  107. Anand, G. S. & Stock, A. M. Kinetic basis for the stimulatory effect of phosphorylation on the methylesterase activity of CheB. Biochemistry 41, 6752–6760 (2002).

    CAS  PubMed  Google Scholar 

  108. Levit, M. N., Liu, Y. & Stock, J. B. Stimulus response coupling in bacterial chemotaxis: receptor dimers in signalling arrays. Mol. Microbiol. 30, 459–466 (1998).

    CAS  PubMed  Google Scholar 

  109. Szurmant, H. & Ordal, G. W. Diversity in chemotaxis mechanisms among the bacteria and Archaea. Microbiol. Mol. Biol. Rev. 68, 301–319 (2004).

    CAS  PubMed  PubMed Central  Google Scholar 

  110. Bischoff, D. S., Bourret, R. B., Kirsch, M. L. & Ordal, G. W. Purification and characterization of Bacillus subtilis CheY. Biochemistry 32, 9256–9261 (1993).

    CAS  PubMed  Google Scholar 

  111. Zimmer, M. A., Tiu, J., Collins, M. A. & Ordal, G. W. Selective methylation changes on the Bacillus subtilis chemotaxis receptor McpB promote adaptation. J. Biol. Chemistry 275, 24264–24272 (2000).

    CAS  Google Scholar 

  112. Nordmann, B. et al. Identification of volatile forms of methyl groups released by Halobacterium salinarium. J. Biol. Chem. 269, 16449–16454 (1994).

    CAS  PubMed  Google Scholar 

  113. Thoelke, M. S., Kirby, J. R. & Ordal, G. W. Novel methyl transfer during chemotaxis in Bacillus subtilis. Biochemistry 28, 5585–5589 (1989).

    CAS  PubMed  Google Scholar 

  114. Kirby, J. R., Kristich, C. J., Feinberg, S. L. & Ordal, G. W. Methanol production during chemotaxis to amino acids in Bacillus subtilis. Mol. Microbiol. 24, 869–878 (1997).

    CAS  PubMed  Google Scholar 

  115. Kirsch, M. L., Peters, P. D., Hanlon, D. W., Kirby, J. R. & Ordal, G. W. Chemotactic methylesterase promotes adaptation to high concentrations of attractant in Bacillus subtilis. J. Biol. Chem. 268, 18610–18616 (1993).

    CAS  PubMed  Google Scholar 

  116. Rosario, M. M. & Ordal, G. W. CheC and CheD interact to regulate methylation of Bacillus subtilis methyl-accepting chemotaxis proteins. Mol. Microbiol. 21, 511–518 (1996).

    CAS  PubMed  Google Scholar 

  117. Szurmant, H., Muff, T. J. & Ordal, G. W. Bacillus subtilis CheC and FliY are members of a novel class of CheY–P-hydrolyzing proteins in the chemotactic signal transduction cascade. J. Biol. Chem. 279, 21787–21792 (2004). Identified roles for extra chemotaxis proteins in B. subtilis.

    CAS  PubMed  Google Scholar 

  118. Porter, S. L., Warren, A. V., Martin, A. C. & Armitage, J. P. The third chemotaxis locus of Rhodobacter sphaeroides is essential for chemotaxis. Mol. Microbiol. 46, 1081–1094 (2002).

    CAS  PubMed  Google Scholar 

  119. Wadhams, G. H., Warren, A. V., Martin, A. C. & Armitage, J. P. Targeting of two signal transduction pathways to different regions of the bacterial cell. Mol. Microbiol. 50, 763–770 (2003). Showed for the first time that the components of two chemotaxis pathways are physically separated within a bacterial cell.

    CAS  PubMed  Google Scholar 

  120. Porter, S. L. & Armitage, J. P. Chemotaxis in Rhodobacter sphaeroides requires an atypical histidine protein kinase. J. Biol. Chem. 12 Oct 2004 (doi:10.1074/jbc.M408855200).

  121. O'Toole, R. et al. The chemotactic response of Vibrio anguillarum to fish intestinal mucus is mediated by a combination of multiple mucus components. J. Bacteriol. 181, 4308–4317 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  122. Kim, H. & Farrand, S. K. Opine catabolic loci from Agrobacterium plasmids confer chemotaxis to their cognate substrates. Mol. Plant Microbe Interact. 11, 131–143 (1998).

    CAS  PubMed  Google Scholar 

  123. Zhu, J. & Mekalanos, J. J. Quorum sensing-dependent biofilms enhance colonization in Vibrio cholerae. Dev. Cell 5, 647–656 (2003).

    CAS  PubMed  Google Scholar 

  124. Butler, S. M. & Camilli, A. Both chemotaxis and net motility greatly influence the infectivity of Vibrio cholerae. Proc. Natl Acad. Sci. USA 101, 5018–5023 (2004).

    CAS  PubMed  PubMed Central  Google Scholar 

  125. Pandya, S., Iyer, P., Gaitonde, V., Parekh, T. & Desai, A. Chemotaxis of Rhizobium SP.S2 towards Cajanus cajan root exudate and its major components. Curr. Microbiol. 38, 205–209 (1999).

    CAS  PubMed  Google Scholar 

  126. Millikan, D. S. & Ruby, E. G. FlrA, a σ54-dependent transcriptional activator in Vibrio fischeri, is required for motility and symbiotic light-organ colonization. J. Bacteriol. 185, 3547–3557 (2003).

    CAS  PubMed  PubMed Central  Google Scholar 

  127. Stoodley, P., Sauer, K., Davies, D. G. & Costerton, J. W. Biofilms as complex differentiated communities. Annu. Rev. Microbiol. 56, 187–209 (2002).

    CAS  PubMed  Google Scholar 

  128. Costerton, J. W. Anaerobic biofilm infections in cystic fibrosis. Mol. Cell 10, 699–700 (2002).

    CAS  PubMed  Google Scholar 

  129. Taga, M. E. & Bassler, B. L. Chemical communication among bacteria. Proc. Natl Acad. Sci. USA 100, 14549–14554 (2003).

    CAS  PubMed  PubMed Central  Google Scholar 

  130. Berg, H. C. The rotary motor of bacterial flagella. Annu. Rev. Biochem. 72, 19–54 (2003). A comprehensive review of the mechanism of rotation of the bacterial flagellar motor.

    CAS  PubMed  Google Scholar 

  131. Atsumi, T., McCarter, L. & Imae, Y. Polar and lateral flagellar motors of marine Vibrio are driven by different ion-motive forces. Nature 355, 182–184 (1992).

    CAS  PubMed  Google Scholar 

  132. Mattick, J. S. Type IV pili and twitching motility. Annu. Rev. Microbiol. 56, 289–314 (2002).

    CAS  PubMed  Google Scholar 

  133. Kaiser, D. Coupling cell movement to multicellular development in Myxobacteria. Nature Rev. Microbiol. 1, 45–54 (2003).

    CAS  Google Scholar 

  134. McBride, M. J. Bacterial gliding motility: multiple mechanisms for cell movement over surfaces. Annu. Rev. Microbiol. 55, 49–75 (2001).

    CAS  PubMed  Google Scholar 

  135. Wolgemuth, C. W., Igoshin, O. & Oster, G. The motility of mollicutes. Biophys. J. 85, 828–842 (2003).

    CAS  PubMed  PubMed Central  Google Scholar 

  136. Armitage, J. P., Pitta, T. P., Vigeant, M. A., Packer, H. L. & Ford, R. M. Transformations in flagellar structure of Rhodobacter sphaeroides and possible relationship to changes in swimming speed. J. Bacteriol. 181, 4825–4833 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  137. Macnab, R. M. How bacteria assemble flagella. Annu. Rev. Microbiol. 57, 77–100 (2003). A review of the process of bacterial flagella assembly.

    CAS  PubMed  Google Scholar 

  138. Hueck, C. J. Type III protein secretion systems in bacterial pathogens of animals and plants. Microbiol. Mol. Biol. Rev. 62, 379–433 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  139. Oster, G. & Wang, H. Rotary protein motors. Trends Cell Biol. 13, 114–121 (2003).

    CAS  PubMed  Google Scholar 

  140. Shi, W., Kohler, T. & Zusman, D. R. Chemotaxis plays a role in the social behaviour of Myxococcus xanthus. Mol. Microbiol. 9, 601–611 (1993).

    CAS  PubMed  Google Scholar 

  141. Shi, W. Y., Yang, Z. M., Sun, H., Lancero, H. & Tong, L. M. Phenotypic analyses of frz and dif double mutants of Myxococcus xanthus. FEMS Microbiol. Lett. 192, 211–215 (2000).

    CAS  PubMed  Google Scholar 

  142. Kirby, J. R. & Zusman, D. R. Chemosensory regulation of developmental gene expression in Myxococcus xanthus. Proc. Natl Acad. Sci. USA 100, 2008–2013 (2003). Provides an example of an operon that encodes chemotaxis-protein homologues that are not involved in the regulation of bacterial motility.

    CAS  PubMed  PubMed Central  Google Scholar 

  143. Koradi, R., Billeter, M. & Wuthrich, K. MOLMOL: a program for display and analysis of macromolecular structures. J. Mol. Graph. 14, 51–61 (1996).

    CAS  PubMed  Google Scholar 

  144. Bray, D. Genomics: molecular prodigality. Science 299, 1189–1190 (2003).

    CAS  PubMed  Google Scholar 

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Acknowledgements

We would like to thank the Biotechnology and Biological Sciences Research Council for funding the research on R. sphaeroides behaviour that has been carried out in our laboratory, and we apologise to the many authors whose work we have not been able to include because of space restraints.

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Correspondence to Judith P. Armitage.

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The authors declare no competing financial interests.

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DATABASES

Entrez Gene

ArcB

CheA

CheB

CheC

CheD

CheR

CheV

CheW

CheY

CheZ

FliM

KinB

McpB

NtrB

PrrB

Tap

Tar

Trg

Tsr

Interpro

FAD-binding domain

HAMP domain

HPt domain

PAS domain

SH3

Protein Data Bank

1A2O

1ANF

1B3Q

1BC5

1EAY

1EHC

1I5N

1KMI

1KOS

1QU7

1WAT

FURTHER INFORMATION

Department of Energy Joint Genome Institute

The Institute for Genomic Research

Glossary

HAMP DOMAIN

('Histidine kinases, adenylyl cyclases, methyl-binding proteins and phosphatases' domain). A domain that is broadly conserved in histidine protein kinases, chemoreceptors and phosphatases. It contains two amphipathic helices, and is presumed to have a role in signal transduction.

NODULE

A swelling on the roots of nitrogen-fixing plants that contains symbiotic nitrogen-fixing bacteria.

QUORUM SENSING

The ability of bacteria to sense their own cell density by detecting the concentration of signalling molecules that have been released in their environment.

PILI

Short, polymerized-protein projections that protrude from the bacterial cell and are used for surface attachment and twitching motility.

PAS DOMAIN

(PER, ARNT, SIM domain). A domain that is involved in recognizing stimuli such as light, oxygen, redox potential, energy status and small ligands.

HPt DOMAIN

(Histidine-containing phosphotransfer domain). These domains are 120 amino acids long and contain a histidine residue that can participate in phosphoryl-transfer reactions. They function as phosphoreceivers and phosphodonors, and can therefore be used to create multistep phosphorelay systems.

HYPERFLAGELLATE

An increased number of flagella.

GAIN

A parameter of chemotactic behaviour that describes the relationship between the stimulus and the response. It is defined as the fractional increase in anticlockwise motor bias divided by the fractional change in receptor occupancy.

CHEMORECEPTOR

A sensory receptor that responds to chemical stimuli. The term covers transmembrane receptors (such as the methyl-accepting chemotaxis proteins) and cytoplasmic receptors (such as transducer-like proteins).

METHYL-ACCEPTING CHEMOTAXIS PROTEIN

(MCP). A transmembrane chemoreceptor that shows methylation-dependent adaptation.

FLAVIN ADENINE DINUCLEOTIDE

(FAD). FAD functions as a redox centre in many proteins.

SRC-HOMOLOGY-3 DOMAIN

(SH3 domain). A 60-amino-acid domain that mediates the assembly of specific protein complexes through binding to proline-rich peptides. It is found in many proteins that are involved in signal transduction and membrane–cytoskeleton interactions.

TRANSDUCER-LIKE PROTEIN

(Tlp). Tlp proteins are cytoplasmic chemoreceptors that have the cytoplasmic domain of methyl-accepting chemotaxis proteins and lack transmembrane domains.

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Wadhams, G., Armitage, J. Making sense of it all: bacterial chemotaxis. Nat Rev Mol Cell Biol 5, 1024–1037 (2004). https://doi.org/10.1038/nrm1524

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