Chemotactic Signal Transduction in Escherichia coli and Salmonella typhimurium

Charles D. Amsler; Philip Matsumura

doi:10.1128/9781555818319.ch6

Chapter 6 : Chemotactic Signal Transduction in Escherichia coli and Salmonella typhimurium

Authors: Charles D. Amsler¹, Philip Matsumura²

VIEW AFFILIATIONS HIDE AFFILIATIONS

Affiliations: 1: Department of Biology, University of Alabama at Birmingham, Birmingham, Alabama 35294-1170; 2: Department of Microbiology and Immunology (M/C 790), University of Illinois at Chicago, Chicago, Illinois 60612-7344

Content Type: Monograph

Publication Year: 1995

Category: Microbial Genetics and Molecular Biology

Book DOI: 10.1128/9781555818319

Chapter DOI: 10.1128/9781555818319.ch6

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Preview this chapter:

Chemotactic Signal Transduction in Escherichia coli and Salmonella typhimurium, Page 1 of 2

< Previous page | Next page > /docserver/preview/fulltext/10.1128/9781555818319/9781555810894_Chap06-1.gif /docserver/preview/fulltext/10.1128/9781555818319/9781555810894_Chap06-2.gif

Abstract:

Bacterial chemotaxis is an important model for two-component regulatory systems. The flow of information through the chemotactic signal transduction pathway and the proteins responsible for it have been characterized in great detail. The most detailed knowledge of the chemotactic signal transduction pathway comes from studies of the closely related enteric bacteria Escherichia coli and Salmonella typhimurium. The information pathway in these species serves as the model to which all other species are usually compared. Consequently, the chapter focuses exclusively on chemotaxis in E. coli and S. typhimurium. The components of the signal pathway in these two species are virtually interchangeable. The transmembrane receptors discussed in the chapter detect compounds in the periplasm and transmit this information to the cytoplasm, but separate transport proteins are required for uptake. The chapter provides an overview of the function of components and the pathway as a whole while calling attention to some recent advances. Although chemotaxis is probably the most thoroughly understood of all signal transduction pathways, significant gaps remain in our understanding of it. Computer-based quantitative assays of chemotactic behavior are becoming available and will facilitate quantitative analysis of chemotaxis in whole free-swimming cells.

Citation: Amsler C, Matsumura P. 1995. Chemotactic Signal Transduction in Escherichia coli and Salmonella typhimurium, p 89-103. In Hoch J, Silhavy T (ed), Two-Component Signal Transduction. ASM Press, Washington, DC. doi: 10.1128/9781555818319.ch6

Key Concept Ranking

Cell Division: 0.48265022
Phosphoenolpyruvate Sugar Phosphotransferase System: 0.481134

0.48265022

Highlighted Text: Show | Hide

Full text loading...

Figures

Chemotactic Signal Transduction in Escherichia coli and Salmonella typhimurium

[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/10.1128/9781555818319.chap6-1,webId=/content/author/10.1128/9781555818319.chap6-1,properties={foaf_givenname=Charles D., foaf_name=Charles D. Amsler, foaf_surname=Amsler, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/10.1128/9781555818319.chap6-aff1]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/10.1128/9781555818319.chap6-2,webId=/content/author/10.1128/9781555818319.chap6-2,properties={foaf_givenname=Philip, foaf_name=Philip Matsumura, foaf_surname=Matsumura, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/10.1128/9781555818319.chap6-aff2]]}]]

/content/10.1128/9781555818319.chap6.fig6-1

FIGURE 1

Overall model of chemotactic signal transduction. Abbreviations: AL, CheAL; As, CheAs; B, CheB; BB, flagellar basal body; CCW, counterclockwise flagellar rotation; CW, clockwise flagellar rotation; FF, flagellar filament; FM, flagellar motor;MCP, methyl-accepting chemotaxis protein; P, phosphate; R, CheR; W, CheW; Y, CheY; Z, CheZ.

10.1128/9781555818319/fig6-1_thmb.gif

10.1128/9781555818319/fig6-1.gif

FIGURE 1

/content/10.1128/9781555818319.chap6.fig6-2

FIGURE 2

Flagellar patterns during smooth swimming and tumble behaviors.

10.1128/9781555818319/fig6-2_thmb.gif

10.1128/9781555818319/fig6-2.gif

FIGURE 2

Flagellar patterns during smooth swimming and tumble behaviors.

/content/10.1128/9781555818319.chap6.fig6-3

FIGURE 3

Swimming behavior in homogeneous versus heterogeneous environments. Smooth swimming and tumbles as in Fig. 2 , with length of arrows indicating the duration of smooth swimming. Bacteria swim smoothly longer when their environment is getting better than when it is unchanging. There is no difference in smooth swimming duration between homogeneous environments and gradients when the environment is getting worse.

10.1128/9781555818319/fig6-3_thmb.gif

10.1128/9781555818319/fig6-3.gif

FIGURE 3

References

/content/book/10.1128/9781555818319.chap6

1. Adler, J. 1973. A method for measuring chemotaxis and use of the method to determine optimal conditions for chemotaxis by Escherichia coli. J. Gen. Microbiol. 74: 77– 91.

2. Adler, J.,, and M. M. Dahl. 1967. A method for measuring the motility of bacteria and for comparing random and non-random motility. J. Gen. Microbiol. 46: 161– 173.

3. Adler, J.,, and B. Templeton. 1967. The effect of environmental conditions on the motility of Escherichia coli. J. Gen. Microbiol. 46: 175– 184.

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

5. Amsler, C. D.,, M. Cho,, and P. Matsumura. 1993. Multiple factors underlying the maximum motility of Escherichia coli as cultures enter post-exponential growth. J. Bacteriol. 175: 6238– 6244.

6. Armitage, J. P. 1992. Behavioral responses in bacteria. Annu. Rev. Physiol. 54: 683– 714.

Barak, R.,, and M. Eisenbach. 1992a.. Correlation between phosphorylation of the chemotaxis protein- CheY and its activity at the flagellar motor. Biochemistry 31: 1821– 1826.

8. Barak, R.,, and M. Eisenbach. 1992b. Fumarate or a fumarate metabolite restores switching ability to rotating flagella of bacterial envelopes. J. Bacteriol. 174: 643– 645.

9. Bartlett, D. H.,, and P. Matsumura. 1986. Behavorial responses to chemical cues by bacteria. J. Chem. Ecol. 12: 1071– 1089.

10. Berg, H. C.,, and D. A. Brown. 1972. Chemotaxis in Escherichia coli analysed by three-dimensional tracking. Nature (London) 239: 500– 504.

11. Berg, H. C.,, and D. A. Brown. 1974. Chemotaxis in Escherichia coli analysed by three-dimensional tracking. Antibiot. Chemother. 19: 55– 78.

12. Berg, H. C.,, M. D. Manson,, and M. P. Conley. 1982. Dynamics and energetics of flagellar rotation in bacteria. Symp. Soc. Exp. Biol. 35: 1– 31.

13. Berg, H. C.,, and E. M. Purcell. 1977. Physics of chemoreception. Biophys.J. 20: 193– 219.

14. Berg, H. C.,, and P. M. Tedesco. 1975. Transient response to chemotactic stimuli in Escherichia coli. Proc. Natl. Acad. Sci. USA 72: 3235– 3239.

15. Bischoff, D. S.,, and G. W. Ordal. 1992. Bacillis subtilis chemotaxis—a deviation from the paradigm. Mol. Microbiol. 6: 23– 28.

16. Blat, Y.,, and M. Eisenbach. 1994. Phosphorylationdependent binding of the chemotaxis signal molecule CheY to its phosphatase, CheZ. Biochemistry 33: 902– 906.

17. Borkovich, K. A.,, N. Kaplan,, J. F. Hess,, and M. I. Simon. 1989. Transmembrane signal transduction in bacterial chemotaxis involves ligand-dependent activation of phosphate group transfer. Proc. Natl. Acad. Sci. USA 86: 1208– 1212.

18. Borkovich, K. A.,, and M. I. Simon. 1990. The dynamics of signal transduction in bacterial chemotaxis. Cell 63: 1339– 1348.

19. Botsford, J. L.,, and J. G. Harman. 1992. Cyclic AMP in prokaryotes. Microbiol. Rev. 56: 100– 122.

20. Bourret, R. B.,, K. A. Borkovich,, and M. I. Simon. 1991. Signal transduction pathways involving protein phosphorylation in prokaryotes. Annu. Rev. Biochem. 60: 401– 441.

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

22. Bourret, R. B.,, S. K. Drake,, S. A. Chervitz,, M. I. Simon,, and J. J. Falke. 1993b. Activation of the phosphosignaling protein CheY. 2. Analysis of activated mutants by F19 NMR and protein engineering. J. Biol. Chem. 268: 13089– 13096.

23. Bourret, R. B., J. F. Hess,, and M. I. Simon. 1990. Conserved aspartate residues and phosphorylation in signal transduction by the chemotaxis protein CheY. Proc. Natl. Acad. Sci. USA 87: 41– 45.

24. Conley, M. P.,, A. J. Wolfe,, D. F. Blair,, and H. C. Berg. 1989. Both CheA and CheW are required for reconstitution of signaling in bacterial chemotaxis. J. Bacteriol. 171: 5190– 5193.

25. Dahlquist, F. W.,, R. A. Elwell,, and P. S. Lovely. 1976. Studies of bacterial chemotaxis in defined concentration gradients. A model for chemotaxis toward L-serine. J. Supramol. Struct. 4: 329– 342.

26. Dailey, F. E.,, and H. C. Berg. 1993. Change in direction of flagellar rotation in Escherichia coli mediated by acetate kinase. J. Bacteriol. 175: 3236– 3239.

27. Drake, S. K.,, R. B. Bourret,, L. A. Luck,, M. I. Simon,, and J. J. Falke. 1993. Activation of the phosphosignaling protein CheY. 1. Analysis of the phosphorylated conformation by F19 NMR and protein engineering. J. Biol. Chem. 268: 13081– 13088.

28. Fuhrer, D. K.,, and G. W. Ordal. 1991. Bacillis subtilis CheN, a homolog of a, the central regulator of chemotaxis in Escherichia coli. J. Bacteriol. 173: 7443– 7448.

29. Gegner, J. A.,, and F. W. Dahlquist. 1991. Signal transduction in bacteria: CheW forms a reversible complex with the protein kinase CheA. Proc. Natl. Acad. Sci. USA 88: 750– 754.

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

31. Goy, M. F.,, M. S. Springer,, and J. Adler. 1977. Sensory transduction in Escherichia coli: role of a protein methylation reaction in sensory adaptation. Proc. Natl. Acad. Sci. USA 74: 4964– 4968.

32. Hazelbauer, G. L.,, H. C. Berg,, and P. Matsumura. 1993. Bacterial motility and signal transduction. Cell 73: 15– 22.

33. Hazelbauer, G. L.,, R. Yaghmai,, G. G. Burrows,, J. W. Baumgartner,, D. P. Dutton,, and D. G. Morgan. 1990. Transducers: transmembrane receptor proteins involved in bacterial chemotaxis. Soc. Gen. Microbiol. Symp. 46: 107– 134.

34. Helmann, J. D. 1991. Alternative sigma factors and the regulation of flagellar gene expression. Mol. Microbiol. 12: 2875– 2882.

35. Hess, J. E.,, R. B. Bourret,, K. Oosawa,, P. Matsumura,, and M. I. Simon. 1988a. Protein phosphorylation and bacterial chemotaxis. Cold Spring Harbor Symp. Quant. Biol. 53: 41– 48.

36. Hess, J. E.,, R. B. Bourret,, and M. I. Simon. 1988b. Histidine phosphorylation and phosphoryl group transfer in bacterial chemotaxis. Nature (London) 336: 139– 143.

37. Hess, J. E.,, K. Oosawa,, N. Kaplan,, and M. I. Simon. 1988c. Phosphorylation of three proteins in the signaling pathway of bacterial chemotaxis. Cell 53: 79– 87.

38. Huang, C.,, and R. C. Stewart. 1993. CheZ mutants with enhanced ability to dephosphorylate CheY, the response regulator in bacterial chemotaxis. Biochim. Biophys. Acta 1202: 297– 304.

39. Ichihara, A.,, J. E. Segal,, S. M. Block,, and H. C. Berg. 1983. Coordination of flagella on filamentous cells of Escherichia coli. J. Bacteriol. 155: 228– 237.

40. Kar, L.,, P. Z. Decroos,, S. J. Roman,, P. Matsumura,, and M. E. Johnson. 1992a Specificity and affinity of binding of phosphate-containing compounds to CheY protein. Biochem. J. 287: 533– 543.

41. Kar, L.,, P. Matsumura,, and M. E. Johnson. 1992b Bivalent-metal binding to CheY protein—effect on protein conformation. Biochem. J. 287: 521– 531.

42. Kehry, M. R.,, T. G. Doak,, and E. W. Dahlquist. 1984. Stimulus-induced changes in methylesterase activity during chemotaxis in Escherichia coli. J. Biol. Chem. 259: 11828– 11835.

43. Kehry, M. R.,, T. G. Doak,, and E. W. Dahlquist. 1985. Sensory adaptation in bacterial chemotaxis: regulation of methylesterase activity. J. Bacteriol. 163: 983– 990.

44. Khan, S.,, E. Castellano,, J. L. Spudich,, J. A. McCray,, R. S. Goody,, G. P. Reid,, and D. R. Trentham. 1993. Excitatory signaling in bacteria probed by chaged chemoeffectors. Biophys. J. 65: 2368– 2382.

45. Kim, S.-H.,, G. G. Prive,, J. Yeh,, W. G. Scott,, and M. V Milburn. 1992. A model for transmembrane signalling in a bacterial chemotaxis model receptor. Cold Spring Harbor Symp. Quant. Biol. 57: 17– 24.

46. Komeda, Y. 1982. Fusions of flagellar operons to lactose genes on a Mu lac bacteriophage. J. Bacteriol. 150: 16– 26.

47. Komeda, Y.,, and T. lino. 1979. Regulation of the flagellin gene (hag) in Escherichia coli K-12: analysis of hag-lac gene fusions. J. Bacteriol. 139: 721– 729.

48. Kort, E. N.,, M. E Goy,, S. H. Larden,, and J. Adler. 1975. Methylation of a membrane protein involved in bacterial chemotaxis. Proc. Natl. Acad. Sci. USA 72: 3939– 3943.

49. Koshland, D. E. 1980. Bacterial Chemotaxis as a Model Behavioral System. Distinguished Lecture Series of the Society of General Physiologists. Vol. 2. Raven Press, New York.

50. Kuo, S. C.,, and D. E. Koshland, Jr. 1987. Roles of cheY and cheZ gene products in controlling flagellar rotation in bacterial chemotaxis of Escherichia coli. J. Bacteriol. 169: 1307– 1314.

51. Liu, J.,, and J. S. Parkinson. 1989. Role of CheW protein in coupling membrane receptors to the intracellular signalling system of bacterial chemotaxis. Proc. Natl. Acad. Sci. USA 86: 8703– 8707.

52. Liu, J.,, and J. S. Parkinson. 1991. Genetic evidence for the interaction between CheW and Tsr proteins during chemoreceptor signaling by Escherichia coli. J. Bacteriol. 173: 4941– 4951.

53. Liu, X. Y.,, and P. Matsumura. 1994. The FlhD/ FlhC complex, a transcriptional activator of the Escherichia coli flagellar class II operons. J. Bacteriol. 176: 7345– 7351.

54. Lowry, D. E.,, A. Roth,, P. Rupert,, F. W. Dahlquist,, F. Moy,, P. Domaile,, and P. Matsumura. 1994. Signal transduction in chemotaxis; a propagating conformation change upon phosphorylation of CheY. J. Biol. Chem. 269: 26358– 26362.

55. Lupas, A.,, and J. Stock. 1989. Phosphorylation of an N-terminal regulatory domain activates CheB methylesterase in bacterial chemotaxis. J. Biol. Chem. 264: 17337– 17342.

56. Lynch, B. A.,, and D. E. Koshland, Jr. 1991. Disulfide cross-linking studies of the transmembrane regions of the aspartate sensory receptor of Escherichia coli. Proc. Natl. Acad. Sci. USA 88: 10402– 10406.

57. Macnab, R. M. 1977. Bacterial flagella rotating in bundles: a study in helical geometry. Proc. Natl. Acad. Sci. USA 74: 221– 225.

58. Macnab, R. M., 1987a. Flagella, p. 70– 83. In F. C. Neidhardt,, J. L. Ingraham,, K. B. Low,, B. Magasanik,, M. Schaechter,, and H. E. Umbarger (ed.), Escherichia coli and Salmonella typhimurium: Cellular and Molecular Biology. American Society for Microbiology, Washington, D C.

59. Macnab, R. M., 1987b. Motility and chemotaxis, p. 732– 759. In F. C. Neidhardt,, J. L. Ingraham,, K. B. Low,, B. Magasanik,, M. Schaechter,, and H. E. Umbarger (ed.), Escherichia coli and Salmonella typhimurium: Cellular and Molecular Biology. American Society for Microbiology, Washington, DC.

60. Macnab, R. M. 1990. Genetics, structure, and assembly of the bacterial flagellum. Symp. Soc. Gen. Microbiol. 46: 77– 106.

61. Macnab, R. M. 1992. Genetics and biogenesis of bacterial flagella. Annu. Rev. Genet. 26: 131– 158.

62. Macnab, R. M.,, and S.-I. Aizawa. 1984. Bacterial motility and the bacterial flagellar motor. Annu.Rev. Biophys. Bioeng. 13: 51– 83.

63. Macnab, R. M.,, and D. R Han. 1983. Asynchronous switching of flagellar motors on a single bacterial cell. Cell 32: 109– 117.

64. Maddock, J. R.,, and L. Shapiro. 1993. Polar localization of the chemoreceptor complex in the Escherichia coli cell. Science 259: 1717– 1723.

65. Marwan, W.,, and D. Osterhelt. 1990. Quantitation of photochromism of sensory rhodopsin-I by computerized tracking of Halobacterium halobium cells. J. Biol. Chem. 215: 277– 285.

66. Matsumura, P.,, S. Roman,, K. Volz,, and D. Mc-Nally. 1990. Signalling complexes in bacterial chemotaxis. Soc. Gen. Microbiol. Symp. 46: 135– 154.

67. Matsumura, P.,, M. Silverman,, and M. Simon. 1977. Synthesis of mot and che gene products of Escherichia coli programmed by hybrid Col El plasmids in minicells. Bacteriology 132: 996– 1002.

68. McBride, M. J.,, T. Kohler,, and D. R. Zusman. 1992. Methylation of FrzCD, a methyl-accepting taxis protein of Myxococcus xanthus, is correlated with factors affecting cell behavior. J. Bacteriol. 174: 4246– 4257.

69. McNally, D. R.,, and P. Matsumura. 1991. Bacterial chemotaxis signaling complexes: formation of a CheA/CheW complex enhances autophosphorylation and affinity for CheY. Proc. Natl. Acad. Sci. USA 88: 6229– 6273.

70. Milburn, M. V.,, G. G. Prive,, D. L. Milligan,, W. G. Scott,, J. Yeh,, J. Jancarik,, D. E. Koshland, Jr.,, and S.-H. Kim. 1991. Three-dimensional structures of the ligand-binding domain of the bacterial aspart receptor with and without a ligand. Science 254: 1342– 1347.

71. Milligan, D. L.,, and D. E. Koshland, J r. 1988. Site-directed cross-linking establishing the dimeric structure of the aspartate receptor of bacterial chemotaxis. J. Biol. Chem. 263: 6268– 6275.

72. Milligan, D. L.,, and D. E. Koshland, J r. 1991. Intrasubunit signal transduction by the aspartate chemoreceptor. Science 254: 1651– 1654.

73. Ninfa, E. G.,, A. Stock,, S. Mowbray,, and J. Stock. 1991. Reconstitution of the bacterial chemotaxis signal transduction system from purified components. J. Biol. Chem. 266: 9764– 9770.

74. Oosawa, K.,, J. E Hess,, and M. I. Simon. 1988. Mutants defective in bacterial chemotaxis show modified protein phosphorylation. Cell 53: 89– 96.

75. Ordal, G. W. 1985. Bacterial chemotaxis: biochemistry of behavior in a single cell. Crit. Rev. Microbiol. 12: 95– 130.

76. Oxender, D. L. 1972. Membrane transport. Annu. Rev. Biochem. 41: 777– 814.

77. Pakula, A. A.,, and M. I. Simon. 1992a Determination of transmembrane protein structure by disulfide cross-linking: the Escherichia coli Tar receptor. Proc. Natl. Acad. Sci. USA 89: 4144– 4148.

78. Pakula, A. A.,, and M. I. Simon. 1992b Pivits or pistons? Nature (London) 355: 496– 497.

79. Parkinson, J. S. 1993. Signal transduction schemes of bacteria. Cell 73: 857– 871.

80. Parkinson, J. S.,, and D.E. Blair. 1993. Does E. coli have a nose? Science 259: 1701– 1702.

81. Parkinson, J. S.,, and E. C. Kofoid. 1992. Communication modules in bacterial signaling proteins. Annu. Rev. Genet. 26: 71– 112.

82. Parkinson, J. S.,, and S. R. Parker. 1979. Identification of the cheC and cheZ gene products is required for chemotactic behavior in Escherichia coli. Proc. Natl. Acad. Sci. USA 76: 2390– 2394.

83. Parkinson, J. S.,, S. R. Parker,, P. B. Talbert,, and S. E. Houts. 1983. Interactions between chemotaxis genes and flagellar genes in Escherichia coli. J. Bacteriol. 155: 265– 274.

84. Poole, P. S.,, D. R. Sinclair,, and J. P. Armitage. 1988. Real-time computer tracking of free-swimming and tethered rotating cells. Anal. Biochem. 175: 52– 58.

85. Pruss, B.,, and A. J. Wolfe. 1994. Regulation of acetyl phosphate synthesis and degradation and the control of flagellar expression in Escherichia coli. Mol. Microbiol. 12: 973– 984.

86. Roman, S. J.,, M. Meyers,, K. Volz,, and P. Matsumura. 1992. A chemotactic signaling surface on CheY defined by suppressors of flagellar switch mutations. J. Bacteriol. 174: 6247– 6255.

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

88. Sanders, D. A.,, B. L. Gillece-Castro,, and A. M. Stock. 1989. Identification of the site of phosphorylation of the chemotaxis response regulator protein, CheY. J. Biol. Chem. 264: 21770– 21778.

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

90. Shaw, C. H. 1991. Swimming against the tide: chemotaxis in Agrobacterium. Bioessays 13: 25– 29.

91. Shi, W.,, Y. Zhou,, J. Wild,, J. Adler,, and C. A. Gross. 1992. DnaK, DnaJ, and GrpE are required for flagellum synthesis in Escherichia coli. J. Bacteriol. 174: 6256– 6263.

92. Shioi, J.,, C. V. Dang,, and B. L. Taylor. 1987. Oxygen as attractant and repellant in bacterial chemotaxis. J. Bacteriol. 169: 3118– 3123.

93. Shioi, J.,, R. C. Tribhuwan,, S. T. Berg,, and B. L. Taylor. 1988. Signal transduction in chemotaxis to oxygen in Escherichia coli and Salmonella typhimurium. J. Bacteriol. 170: 5507– 5511.

94. Shukla, D.,, and P. Matsumura. Unpublished data.

95. Silverman, M.,, and M. Simon. 1974. Characterization of Escherichia coli mutants that are insensitive to catabolite repression. J. Bacteriol. 120: 1196– 1203.

96. Silverman, M.,, and M. Simon. 1977. Chemotaxis in Escherichia coli: methylation of che gene products. Proc. Natl. Acad. Sci. USA 74: 3317– 3321.

97. Simms, S. A.,, M. G. Keane,, and J. Stock. 1985. Multiple forms of the CheB methyl transferase in bacterial chemosensing. J. Biol. Chem. 260: 10161– 10168.

98. Smith, R. A.,, and J. S. Parkinson. 1980. Overlapping genes at the cheA locus of Escherichia coli. Proc. Natl. Acad. Sci. USA 77: 5370– 5374.

99. Sockett, H.,, S. Yamaguchi,, M. Kihara,, V. M. Irikura,, and R. M. Macnab. 1992. Molecular analysis of the flagellar switch protein FliM of Salmonella typhimurium. J. Bacteriol. 174: 793– 806.

100. Springer, M. S.,, M. F. Goy,, and J. Adler. 1977. Sensory transduction in Escherichia coli: two complementary pathways of information processing that involve methylated proteins. Proc. Natl. Acad. Sci. USA 74: 3312– 3316.

101. Springer, M. S.,, and B. Zanolari. 1984. Sensory transduction in Escherichia coli: regulation of the demethylation rate by CheA protein. Proc. Natl. Acad. Sci. USA 81: 5061– 5065.

102. Springer, M. S.,, B. Zanolari,, and P. A. Pierzchala. 1982. Ordered methylation of the methyl-accepting chemotaxis proteins of Escherichia coli. J. Biol. Chem. 257: 6861– 6866.

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

104. Stewart, R. C. 1993. Activating and inhibitory mutations in the regulatory domain of CheB, the methylesterase in bacterial chemotaxis. J. Biol. Chem. 268: 1921– 1930.

105. Stewart, R. C.,, and F. W. Dahlquist. 1987. Molecular components of bacterial chemotaxis. Chem. Rev. 87: 997– 1025.

106. Stewart, R. C.,, and E. W. Dahlquist. 1988. N-terminal half of CheB is involved in methylesterase response to negative chemotactic stimuli in Escherichia coli. J. Bacteriol. 170: 5728– 5737.

107. Stock, A. M.,, J. M. Mottonen,, J. B. Stock,, and C. E. Schutt. 1989. Three-dimensional structure of CheY, the response regulator of bacterial chemotaxis. Nature (London) 337: 745– 749.

108. Stock, J. B.,, and D. E. Koshland, Jr. 1978. A protein methylesterase involved in bacterial sensing. Proc. Natl. Acad. Sci. USA 75: 3659– 3663.

109. Stock, J. B.,, and D. E. Koshland, Jr. 1981. Changing reactivity of receptor carboxyl groups during bacterial sensing. J. Biol. Chem. 256: 10826– 10833.

110. Stock, J. B.,, and G. S. Lukat. 1991. Bacterial chemotaxis and the molecular logic of intracellular signal transduction networks. Annu. Rev. Biophys. Biophys. Chem. 20: 109– 136.

111. Stock, J. B.,, A. J. Ninfa,, and A. M. Stock. 1989. Protein phosphorylation and regulation of adaptive responses in bacteria. Microbiol. Rev. 53: 450– 490.

112. Swanson, R. V.,, R. B. Bourret,, and M. I. Simon. 1993a. Intramolecular compartmentalization of the kinase activity of CheA. Mol. Microbiol. 8: 435– 441.

113. Swanson, R. V.,, S. C. Schyster,, and M. I. Simon. 1993b. Expression of CheA fragments which define domains encoding kinase, phosphotransfer, and CheY binding activities. Biochemistry 32: 7623– 7629.

114. Taylor, B. L. 1983a How do bacteria find the optimal concentration of oxygen? Trends Biochem. Sci. 8: 438– 441.

115. Taylor, B. L. 1983b. Role of proton motive force in sensory transduction in bacteria. Annu. Rev. Microbiol. 37: 551– 573.

116. Tisa, L. S.,, and J. Adler. 1992. Calcium ions are involved in Escherichia coli chemotaxis. Proc. Natl. Acad. Sci. USA. 89: 11804– 11808.

117. Titgemeyer, F. 1993. Signal transduction in chemotaxis mediated by the bacterial phosphotransferase system. J. Cell. Biochem. 51: 69– 74.

118. Toews, M. L.,, and J. Adler. 1979. Methanol formation in vivo from methylated chemotaxis proteins in Escherichia coli. J. Biol. Chem. 254: 1761– 1764.

119. Toews, M. L.,, M. F. Goy,, M. S. Springer,, and J. Adler. 1979. Attractants and repellents control demethylation of methylated chemotaxis proteins in Escherichia coli. Proc. Natl. Acad. Sci. USA 76: 5544– 5548.

120. Volz, K. 1993. Structural conservation in the CheY superfamily. Biochemistry 32: 11741– 11753.

121. Volz, K.,, and P. Matsumura. 1991. Crystal structure of Escherichia coli CheY refined at 1.7 Å. J. Biol. Chem. 266: 15511– 15519.

122. Wang, H.,, D. F. McNally,, and P. Matsumura. Unpublished data.

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

124. Wolfe, A. J.,, P. Conley,, and H. C. Berg. 1988. Acetyladenylate plays a role in controlling the direction of flagellar rotation. Proc. Natl. Acad. Sci. USA 85: 6711– 6715.

125. Wolfe, A. J.,, P. Conley,, T. J. Cramer,, and H. C. Berg. 1987. Reconstitution of signaling in bacterial chemotaxis J. Bacteriol. 169: 1878– 1885.

126. Wolfe, A. J.,, and R. C. Stewart. 1993. The short form of CheA protein restores kinase activity and chemotactic ability to kinase-deficient mutants. Proc. Natl. Acad. Sci. USA 90: 1518– 1522.

127. Yamaguchi, S.,, S.-I. Aizawa,, M. Kihara,, M. Isomura,, C. J. Jones., and R. M. Macnab. 1986a. Genetic evidence for a switching and energy-transducing complex in the flagellar motor of Salmonella typhimurium. J. Bacteriol. 168: 1172– 1179.

128. Yamaguchi, S.,, H. Fujita,, A. Ishihara,, S.-I. Aizawa,, and R. M. Macnab. 1986b. Subdivision of flagellar genes of Salmonella typhimurium into regions responsible for assembly, rotation, and switching. J. Bacteriol. 166: 187– 193.

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

130. Zhulin, I. B.,, and J. P. Armitage. 1993. Motility, chemotaxis, and methylation-independent chemotaxis in Azospirillum brasilense. J. Bacteriol. 175: 952– 958.