1887

Abstract

has a more complex mechanism of chemotaxis than does the paradigm organism, . In order to understand better the role of the novel chemotaxis proteins – CheC, CheD and CheV – mutants in which increasing numbers of the corresponding genes had been deleted were studied as tethered cells and their biases and sometimes durations of counterclockwise (CCW) and clockwise (CW) flagellar rotations in response to addition and removal of the attractant asparagine were observed. The mutant was found to have considerably reduced switching frequency (that is, prolonged CCW and CW rotations) without a significantly different prestimulus CCW bias, compared with wild-type. This result may indicate that in absence of CheC the switch might be in a conformation less resembling the transition state than in presence of CheC. Conversely, the (methylesterase) mutant showed considerably increased switching frequency without affecting CCW bias, compared with wild-type. Removal of all known adaptation systems – the methylation, CheC and CheV systems – resulted in a mutant () that still retained some adaptation following the addition of attractant.

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2004-03-01
2024-04-18
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References

  1. Aizawa S.-I., Zhulin I. B., Márquez-Magaña L., Ordal G. W. 2001; Chemotaxis and motility. In Bacillus subtilis and its Relatives: from Genes to Cells pp 437–452 Edited by Sonenshein A., Losick R., Hoch J. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  2. Alon U., Camarena L., Surette M. G., Liu Y., Leibler S., Stock J. B., Aguera y Arcas B. 1998; Response regulator output in bacterial chemotaxis. EMBO J 17:4238–4248 [CrossRef]
    [Google Scholar]
  3. Alon U., Surette M. G., Barkai N., Leibler S. 1999; Robustness in bacterial chemotaxis. Nature 397:168–171 [CrossRef]
    [Google Scholar]
  4. Barkai N., Leibler S. 1997; Robustness in simple biochemical networks. Nature 387:913–917 [CrossRef]
    [Google Scholar]
  5. Berg H. C., Brown D. A. 1972; Chemotaxis in Escherichia coli analysed by three-dimensional tracking. Nature 239:500–504 [CrossRef]
    [Google Scholar]
  6. Bischoff D. S., Ordal G. W. 1991; Sequence and characterization of Bacillus subtilis CheB, a homolog of Escherichia coli CheY, and its role in a different mechanism of chemotaxis. J Biol Chem 266:12301–12305
    [Google Scholar]
  7. Bischoff D. S., Bourret R. B., Kirsch M. L., Ordal G. W. 1993; Purification and characterization of Bacillus subtilis CheY. Biochemistry 32:9256–9261 [CrossRef]
    [Google Scholar]
  8. Blat Y., Eisenbach M. 1994; Phosphorylation-dependent binding of the chemotaxis signal molecule CheY to its phosphatase, CheZ. Biochemistry 33:902–906 [CrossRef]
    [Google Scholar]
  9. Bourret R. B., Stock A. M. 2002; Molecular information processing: lessons from bacterial chemotaxis. J Biol Chem 277:9625–9628 [CrossRef]
    [Google Scholar]
  10. Bren A., Eisenbach M. 1998; 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 [CrossRef]
    [Google Scholar]
  11. Bren A., Eisenbach M. 2000; How signals are heard during bacterial chemotaxis: protein-protein interactions in sensory signal propagation. J Bacteriol 182:6865–6873 [CrossRef]
    [Google Scholar]
  12. Bren A., Eisenbach M. 2001; Changing the direction of flagellar rotation in bacteria by modulating the ratio between the rotational states of the switch protein FliM. J Mol Biol 312:699–709 [CrossRef]
    [Google Scholar]
  13. Burgess-Cassler A., Ordal G. W. 1982; Functional homology of Bacillus subtilis methyltransferase II and Escherichia coli CheR protein. J Biol Chem 257:12835–12838
    [Google Scholar]
  14. Burgess-Cassler A., Ullah A. H., Ordal G. W. 1982; Purification and characterization of Bacillus subtilis methyl-accepting chemotaxis protein methyltransferase II. J Biol Chem 257:8412–8417
    [Google Scholar]
  15. Cercignani G., Lucia S., Petracchi D. 1998; Photoresponses of Halobacterium salinarum to repetitive pulse stimuli. Biophys J 75:1466–1472 [CrossRef]
    [Google Scholar]
  16. Falke J. J., Hazelbauer G. L. 2001; Transmembrane signaling in bacterial chemoreceptors. Trends Biochem Sci 26:257–265 [CrossRef]
    [Google Scholar]
  17. Falke J. J., Kim S. H. 2000; Structure of a conserved receptor domain that regulates kinase activity: the cytoplasmic domain of bacterial taxis receptors. Curr Opin Struct Biol 10:462–469 [CrossRef]
    [Google Scholar]
  18. Fosnaugh K., Greenberg E. P. 1988; Motility and chemotaxis of Spirochaeta aurantia: computer-assisted motion analysis. J Bacteriol 170:1768–1774
    [Google Scholar]
  19. Fredrick K. L., Helmann J. D. 1994; Dual chemotaxis signaling pathways in Bacillus subtilis: a sigma D-dependent gene encodes a novel protein with both CheW and CheY homologous domains. J Bacteriol 176:2727–2735
    [Google Scholar]
  20. Fuhrer D. K., Ordal G. W. 1991; Bacillus subtilis CheN, a homolog of CheA, the central regulator of chemotaxis inEscherichia coli. J Bacteriol 173:7443–7448
    [Google Scholar]
  21. Garrity L. F., Ordal G. W. 1997; Activation of the CheA kinase by asparagine in Bacillus subtilis chemotaxis. Microbiology 143:2945–2951 [CrossRef]
    [Google Scholar]
  22. Goldman D. J., Nettleton D. O., Ordal G. W. 1984; Purification and characterization of chemotactic methylesterase from Bacillus subtilis. Biochemistry 23:675–680 [CrossRef]
    [Google Scholar]
  23. Hanlon D. W., Ordal G. W. 1994; Cloning and characterization of genes encoding methyl-accepting chemotaxis proteins in Bacillus subtilis. J Biol Chem 269:14038–14046
    [Google Scholar]
  24. Hanlon D. W., Marquez-Magana L. M., Carpenter P. B., Chamberlin M. J., Ordal G. W. 1992; Sequence and characterization of Bacillus subtilis CheW. J Biol Chem 267:12055–12060
    [Google Scholar]
  25. Hanlon D. W., Ying C., Ordal G. W. 1993; Purification and reconstitution of the methyl-accepting chemotaxis proteins from Bacillus subtilis. Biochim Biophys Acta 1158:345–351 [CrossRef]
    [Google Scholar]
  26. Hess J. F., Bourret R. B., Simon M. I. 1988a; Histidine phosphorylation and phosphoryl group transfer in bacterial chemotaxis. Nature 336:139–143 [CrossRef]
    [Google Scholar]
  27. Hess J. F., Oosawa K., Kaplan N., Simon M. I. 1988b; Phosphorylation of three proteins in the signaling pathway of bacterial chemotaxis. Cell 53:79–87 [CrossRef]
    [Google Scholar]
  28. Karatan E., Saulmon M. M., Bunn M. W., Ordal G. W. 2001; Phosphorylation of the response regulator CheV is required for adaptation to attractants during Bacillus subtilis chemotaxis. J Biol Chem 276:43618–43626 [CrossRef]
    [Google Scholar]
  29. Kirby J. R., Kristich C. J., Feinberg S. L., Ordal G. W. 1997; Methanol production during chemotaxis to amino acids in Bacillus subtilis. Mol Microbiol 24:869–878 [CrossRef]
    [Google Scholar]
  30. Kirby J. R., Saulmon M. M., Kristich C. J., Ordal G. W. 1999; CheY-dependent methylation of the asparagine receptor, McpB, during chemotaxis in Bacillus subtilis. J Biol Chem 274:11092–11100 [CrossRef]
    [Google Scholar]
  31. Kirby J. R., Niewold T. B., Maloy S., Ordal G. W. 2000; CheB is required for behavioural responses to negative stimuli during chemotaxis in Bacillus subtilis. Mol Microbiol 35:44–57 [CrossRef]
    [Google Scholar]
  32. Kirby J. R., Kristich C. J., Saulmon M. M., Zimmer M. A., Garrity L. F., Zhulin I. B., Ordal G. W. 2001; CheC is related to the family of flagellar switch proteins and acts independently from CheD to control chemotaxis in Bacillus subtilis. Mol Microbiol 42:573–585
    [Google Scholar]
  33. Kirsch M. L., Peters P. D., Hanlon D. W., Kirby J. R., Ordal G. W. 1993a; Chemotactic methylesterase promotes adaptation to high concentrations of attractant in Bacillus subtilis. J Biol Chem 268:18610–18616
    [Google Scholar]
  34. Kirsch M. L., Zuberi A. R., Henner D., Peters P. D., Yazdi M. A., Ordal G. W. 1993b; Chemotactic methyltransferase promotes adaptation to repellents in Bacillus subtilis. J Biol Chem 268:25350–25356
    [Google Scholar]
  35. Kristich C. J., Ordal G. W. 2002; Bacillus subtilis CheD is a chemoreceptor modification enzyme required for chemotaxis. J Biol Chem 277:25356–25362 [CrossRef]
    [Google Scholar]
  36. Lukat G. S., Stock J. B. 1993; Response regulation in bacterial chemotaxis. J Cell Biochem 51:41–46 [CrossRef]
    [Google Scholar]
  37. Macnab R. M., Koshland D. E., Jr. 1972; The gradient-sensing mechanism in bacterial chemotaxis. Proc Natl Acad Sci U S A 69:2509–2512 [CrossRef]
    [Google Scholar]
  38. Morrison T. B., Parkinson J. S. 1997; A fragment liberated from the Escherichia coli CheA kinase that blocks stimulatory, but not inhibitory, chemoreceptor signaling. J Bacteriol 179:5543–5550
    [Google Scholar]
  39. Nordmann B., Lebert M. R., Alam M., Nitz S., Kollmannsberger H., Oesterhelt D., Hazelbauer G. L. 1994; Identification of volatile forms of methyl groups released by Halobacterium salinarium. J Biol Chem 269:16449–16454
    [Google Scholar]
  40. Ordal G. W., Villani D. P., Gibson K. J. 1977; Amino acid chemoreceptors of Bacillus subtilis. J Bacteriol 129:156–165
    [Google Scholar]
  41. Ordal G. W., Nettleton D. O., Hoch J. A. 1983; Genetics of Bacillus subtilis chemotaxis: isolation and mapping of mutations and cloning of chemotaxis genes. J Bacteriol 154:1088–1097
    [Google Scholar]
  42. Rosario M. M., Ordal G. W. 1996; CheC and CheD interact to regulate methylation of Bacillus subtilis methyl-accepting chemotaxis proteins. Mol Microbiol 21:511–518 [CrossRef]
    [Google Scholar]
  43. Rosario M. M., Fredrick K. L., Ordal G. W., Helmann J. D. 1994; Chemotaxis in Bacillus subtilis requires either of two functionally redundant CheW homologs. J Bacteriol 176:2736–2739
    [Google Scholar]
  44. Rosario M. M., Kirby J. R., Bochar D. A., Ordal G. W. 1995; Chemotactic methylation and behavior in Bacillus subtilis: role of two unique proteins, CheC and CheD. Biochemistry 34:3823–3831 [CrossRef]
    [Google Scholar]
  45. Rudolph J., Oesterhelt D. 1996; Deletion analysis of the che operon in the archaeon Halobacterium salinarium. J Mol Biol 258:548–554 [CrossRef]
    [Google Scholar]
  46. Scharf B. E., Fahrner K. A., Turner L., Berg H. C. 1998; Control of direction of flagellar rotation in bacterial chemotaxis. Proc Natl Acad Sci U S A 95:201–206 [CrossRef]
    [Google Scholar]
  47. Slack F. J., Serror P., Joyce E., Sonenshein A. L. 1995; A gene required for nutritional repression of the Bacillus subtilis dipeptide permease operon. Mol Microbiol 15:689–702
    [Google Scholar]
  48. Sourjik V., Berg H. C. 2002; Binding of the Escherichia coli response regulator CheY to its target measured in vivo by fluorescence resonance energy transfer. Proc Natl Acad Sci U S A 99:12669–12774 [CrossRef]
    [Google Scholar]
  49. Springer W. R., Koshland D. E., Jr. 1977; Identification of a protein methyltransferase as the cheR gene product in the bacterial sensing system. Proc Natl Acad Sci U S A 74:533–537 [CrossRef]
    [Google Scholar]
  50. Spudich E. N., Takahashi T., Spudich J. L. 1989; Sensory rhodopsins I and II modulate a methylation/demethylation system in Halobacterium halobium phototaxis. Proc Natl Acad Sci U S A 86:7746–7750 [CrossRef]
    [Google Scholar]
  51. Stock J., Levit M. 2000; Signal transduction: hair brains in bacterial chemotaxis. Curr Biol 10:R11–14 [CrossRef]
    [Google Scholar]
  52. Stock J. B., Koshland D. E., Jr. 1978; A protein methylesterase involved in bacterial sensing. Proc Natl Acad Sci U S A 75:3659–3663 [CrossRef]
    [Google Scholar]
  53. Szurmant H., Bunn M. W., Cannistraro V. J., Ordal G. W. 2003; Bacillus subtilis hydrolyzes CheY-P at the location of its action, the flagellar switch. J Biol Chem 278:48611–48616 [CrossRef]
    [Google Scholar]
  54. Taylor B. L., Zhulin I. B., Johnson M. S. 1999; Aerotaxis and other energy-sensing behavior in bacteria. Annu Rev Microbiol 53:103–128 [CrossRef]
    [Google Scholar]
  55. Terwilliger T. C., Wang J. Y., Koshland D. E., Jr. 1986; Kinetics of receptor modification. The multiply methylated aspartate receptors involved in bacterial chemotaxis. J Biol Chem 261:10814–10820
    [Google Scholar]
  56. Toker A. S., Macnab R. M. 1997; Distinct regions of bacterial flagellar switch protein FliM interact with FliG, FliN and CheY. J Mol Biol 273:623–634 [CrossRef]
    [Google Scholar]
  57. Toker A. S., Kihara M., Macnab R. M. 1996; Deletion analysis of the FliM flagellar switch protein of Salmonella typhimurium. J Bacteriol 178:7069–7079
    [Google Scholar]
  58. Ullah A. H., Ordal G. W. 1981; Purification and characterization of methyl-accepting chemotaxis protein methyltransferase I in Bacillus subtilis. Biochem J 199:795–805
    [Google Scholar]
  59. Zhao R., Collins E. J., Bourret R. B., Silversmith R. E. 2002; Structure and catalytic mechanism of the E. coli chemotaxis phosphatase CheZ. Nat Struct Biol 9:570–575
    [Google Scholar]
  60. Zimmer M. A., Tiu J., Collins M. A., Ordal G. W. 2000; Selective methylation changes on the Bacillus subtilis chemotaxis receptor McpB promote adaptation. J Biol Chem 275:24264–24272 [CrossRef]
    [Google Scholar]
  61. Zimmer M. A., Szurmant H., Saulmon M. M., Collins M. A., Bant J. S., Ordal G. W. 2002; The role of heterologous receptors in McpB-mediated signalling in Bacillus subtilis chemotaxis. Mol Microbiol 45:555–568 [CrossRef]
    [Google Scholar]
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