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. 1985 Jan;161(1):51–59. doi: 10.1128/jb.161.1.51-59.1985

Chemotactic signaling in filamentous cells of Escherichia coli.

J E Segall, A Ishihara, H C Berg
PMCID: PMC214834  PMID: 3881399

Abstract

Video techniques were used to record chemotactic responses of filamentous cells of Escherichia coli stimulated iontophoretically with aspartate. Long, nonseptate cells were produced from polyhook strains either by introducing a cell division mutation or by growth in the presence of cephalexin. Markers indicating rotation of flagellar motors were attached with anti-hook antibodies. Aspartate was applied by iontophoretic ejection from a micropipette, and the effects on the direction of rotation of the markers were measured. Motors near the pipette responded, whereas those sufficiently far away did not, even when the pipette was near the cell surface. The response of a given motor decreased as the pipette was moved away, but it did so less steeply when the pipette remained near the cell surface than when it was moved out into the external medium. This shows that there is an internal signal, but its range is short, only a few micrometers. These experiments rule out signaling by changes in membrane potential, by simple release or binding of a small molecule, or by diffusion of the receptor-attractant complex. A likely candidate for the signal is a protein or ligand that is activated by the receptor and inactivated as it diffuses through the cytoplasm. The range of the signal was found to be substantially longer in a cheZ mutant, suggesting that the product of the cheZ gene contributes to this inactivation.

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Selected References

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  1. Adler J. A method for measuring chemotaxis and use of the method to determine optimum conditions for chemotaxis by Escherichia coli. J Gen Microbiol. 1973 Jan;74(1):77–91. doi: 10.1099/00221287-74-1-77. [DOI] [PubMed] [Google Scholar]
  2. Adler J. Chemoreceptors in bacteria. Science. 1969 Dec 26;166(3913):1588–1597. doi: 10.1126/science.166.3913.1588. [DOI] [PubMed] [Google Scholar]
  3. Adler J., Tso W. W. "Decision"-making in bacteria: chemotactic response of Escherichia coli to conflicting stimuli. Science. 1974 Jun 21;184(4143):1292–1294. doi: 10.1126/science.184.4143.1292. [DOI] [PubMed] [Google Scholar]
  4. Armstrong J. B., Adler J., Dahl M. M. Nonchemotactic mutants of Escherichia coli. J Bacteriol. 1967 Jan;93(1):390–398. doi: 10.1128/jb.93.1.390-398.1967. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Armstrong J. B. Chemotaxis and methionine metabolism in Escherichia coli. Can J Microbiol. 1972 May;18(5):591–596. doi: 10.1139/m72-093. [DOI] [PubMed] [Google Scholar]
  6. Aswad D. W., Koshland D. E., Jr Evidence for an S-adenosylmethionine requirement in the chemotactic behavior of Salmonella typhimurium. J Mol Biol. 1975 Sep 15;97(2):207–223. doi: 10.1016/s0022-2836(75)80035-0. [DOI] [PubMed] [Google Scholar]
  7. Begg K. J., Hatfull G. F., Donachie W. D. Identification of new genes in a cell envelope-cell division gene cluster of Escherichia coli: cell division gene ftsQ. J Bacteriol. 1980 Oct;144(1):435–437. doi: 10.1128/jb.144.1.435-437.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Berg H. C., Anderson R. A. Bacteria swim by rotating their flagellar filaments. Nature. 1973 Oct 19;245(5425):380–382. doi: 10.1038/245380a0. [DOI] [PubMed] [Google Scholar]
  9. Berg H. C. Bacterial behaviour. Nature. 1975 Apr 3;254(5499):389–392. doi: 10.1038/254389a0. [DOI] [PubMed] [Google Scholar]
  10. Berg H. C., Brown D. A. Chemotaxis in Escherichia coli analysed by three-dimensional tracking. Nature. 1972 Oct 27;239(5374):500–504. doi: 10.1038/239500a0. [DOI] [PubMed] [Google Scholar]
  11. Berg H. C., Purcell E. M. Physics of chemoreception. Biophys J. 1977 Nov;20(2):193–219. doi: 10.1016/S0006-3495(77)85544-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Berg H. C., Tedesco P. M. Transient response to chemotactic stimuli in Escherichia coli. Proc Natl Acad Sci U S A. 1975 Aug;72(8):3235–3239. doi: 10.1073/pnas.72.8.3235. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Black R. A., Hobson A. C., Adler J. Involvement of cyclic GMP in intracellular signaling in the chemotactic response of Escherichia coli. Proc Natl Acad Sci U S A. 1980 Jul;77(7):3879–3883. doi: 10.1073/pnas.77.7.3879. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Block S. M., Segall J. E., Berg H. C. Impulse responses in bacterial chemotaxis. Cell. 1982 Nov;31(1):215–226. doi: 10.1016/0092-8674(82)90421-4. [DOI] [PubMed] [Google Scholar]
  15. Boyd A., Simon M. Bacterial chemotaxis. Annu Rev Physiol. 1982;44:501–517. doi: 10.1146/annurev.ph.44.030182.002441. [DOI] [PubMed] [Google Scholar]
  16. Clarke S., Koshland D. E., Jr Membrane receptors for aspartate and serine in bacterial chemotaxis. J Biol Chem. 1979 Oct 10;254(19):9695–9702. [PubMed] [Google Scholar]
  17. DeFranco A. L., Koshland D. E., Jr Molecular cloning of chemotaxis genes and overproduction of gene products in the bacterial sensing system. J Bacteriol. 1981 Aug;147(2):390–400. doi: 10.1128/jb.147.2.390-400.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Dreyer F., Peper K. Iontophoretic application of acetylcholine: advantages of high resistance micropipettes in connection with an electronic current pump. Pflugers Arch. 1974 Apr 22;348(3):263–272. doi: 10.1007/BF00587417. [DOI] [PubMed] [Google Scholar]
  19. Engström P., Hazelbauer G. L. Methyl-accepting chemotaxis proteins are distributed in the membrane independently from basal ends of bacterial flagella. Biochim Biophys Acta. 1982 Mar 23;686(1):19–26. doi: 10.1016/0005-2736(82)90147-x. [DOI] [PubMed] [Google Scholar]
  20. Goulbourne E. A., Jr, Greenberg E. P. A voltage clamp inhibits chemotaxis of Spirochaeta aurantia. J Bacteriol. 1983 Feb;153(2):916–920. doi: 10.1128/jb.153.2.916-920.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Goulbourne E. A., Jr, Greenberg E. P. Chemotaxis of Spirochaeta aurantia: involvement of membrane potential in chemosensory signal transduction. J Bacteriol. 1981 Dec;148(3):837–844. doi: 10.1128/jb.148.3.837-844.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Goy M. F., Springer M. S., Adler J. Failure of sensory adaptation in bacterial mutants that are defective in a protein methylation reaction. Cell. 1978 Dec;15(4):1231–1240. doi: 10.1016/0092-8674(78)90049-1. [DOI] [PubMed] [Google Scholar]
  23. Greenwood D., O'Grady F. Comparison of the responses of Escherichia coli and proteus mirabilis to seven beta-lactam antibodies. J Infect Dis. 1973 Aug;128(2):211–222. doi: 10.1093/infdis/128.2.211. [DOI] [PubMed] [Google Scholar]
  24. HODGKIN A. L., KEYNES R. D. Movements of labelled calcium in squid giant axons. J Physiol. 1957 Sep 30;138(2):253–281. doi: 10.1113/jphysiol.1957.sp005850. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Hazelbauer G. L., Harayama S. Sensory transduction in bacterial chemotaxis. Int Rev Cytol. 1983;81:33–70. doi: 10.1016/s0074-7696(08)62334-7. [DOI] [PubMed] [Google Scholar]
  26. Imae Y., Mizuno T., Maeda K. Chemosensory and thermosensory excitation in adaptation-deficient mutants of Escherichia coli. J Bacteriol. 1984 Jul;159(1):368–374. doi: 10.1128/jb.159.1.368-374.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Ishihara A., Segall J. E., Block S. M., Berg H. C. Coordination of flagella on filamentous cells of Escherichia coli. J Bacteriol. 1983 Jul;155(1):228–237. doi: 10.1128/jb.155.1.228-237.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Keith A. D., Snipes W. Viscosity of cellular protoplasm. Science. 1974 Feb 15;183(4125):666–668. doi: 10.1126/science.183.4125.666. [DOI] [PubMed] [Google Scholar]
  29. Khan S., Macnab R. M. The steady-state counterclockwise/clockwise ratio of bacterial flagellar motors is regulated by protonmotive force. J Mol Biol. 1980 Apr 15;138(3):563–597. doi: 10.1016/s0022-2836(80)80018-0. [DOI] [PubMed] [Google Scholar]
  30. Kosower E. M. Selection of ion channel elements in the serine and aspartate methyl-accepting chemotaxis proteins of bacteria. Biochem Biophys Res Commun. 1983 Sep 15;115(2):648–652. doi: 10.1016/s0006-291x(83)80193-4. [DOI] [PubMed] [Google Scholar]
  31. Krieg N. R., Tomelty J. P., Wells J. S., Jr Inhibitio of flagellar coordination in Spirillum volutans. J Bacteriol. 1967 Nov;94(5):1431–1436. doi: 10.1128/jb.94.5.1431-1436.1967. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Larsen S. H., Reader R. W., Kort E. N., Tso W. W., Adler J. Change in direction of flagellar rotation is the basis of the chemotactic response in Escherichia coli. Nature. 1974 May 3;249(452):74–77. doi: 10.1038/249074a0. [DOI] [PubMed] [Google Scholar]
  33. Macnab R. M., Koshland D. E., Jr The gradient-sensing mechanism in bacterial chemotaxis. Proc Natl Acad Sci U S A. 1972 Sep;69(9):2509–2512. doi: 10.1073/pnas.69.9.2509. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Macnab R. M., Ornston M. K. Normal-to-curly flagellar transitions and their role in bacterial tumbling. Stabilization of an alternative quaternary structure by mechanical force. J Mol Biol. 1977 May 5;112(1):1–30. doi: 10.1016/s0022-2836(77)80153-8. [DOI] [PubMed] [Google Scholar]
  35. Margolin Y., Eisenbach M. Voltage clamp effects on bacterial chemotaxis. J Bacteriol. 1984 Aug;159(2):605–610. doi: 10.1128/jb.159.2.605-610.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. McCloskey M., Poo M. M. Protein diffusion in cell membranes: some biological implications. Int Rev Cytol. 1984;87:19–81. doi: 10.1016/s0074-7696(08)62439-0. [DOI] [PubMed] [Google Scholar]
  37. Mesibov R., Adler J. Chemotaxis toward amino acids in Escherichia coli. J Bacteriol. 1972 Oct;112(1):315–326. doi: 10.1128/jb.112.1.315-326.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Miller J. B., Koshland D. E., Jr Sensory electrophysiology of bacteria: relationship of the membrane potential to motility and chemotaxis in Bacillus subtilis. Proc Natl Acad Sci U S A. 1977 Nov;74(11):4752–4756. doi: 10.1073/pnas.74.11.4752. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Ordal G. W. Calcium ion regulates chemotactic behaviour in bacteria. Nature. 1977 Nov 3;270(5632):66–67. doi: 10.1038/270066a0. [DOI] [PubMed] [Google Scholar]
  40. Parkinson J. S. Behavioral genetics in bacteria. Annu Rev Genet. 1977;11:397–414. doi: 10.1146/annurev.ge.11.120177.002145. [DOI] [PubMed] [Google Scholar]
  41. Parkinson J. S. Complementation analysis and deletion mapping of Escherichia coli mutants defective in chemotaxis. J Bacteriol. 1978 Jul;135(1):45–53. doi: 10.1128/jb.135.1.45-53.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Parkinson J. S., Houts S. E. Isolation and behavior of Escherichia coli deletion mutants lacking chemotaxis functions. J Bacteriol. 1982 Jul;151(1):106–113. doi: 10.1128/jb.151.1.106-113.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Parkinson J. S., Parker S. R., Talbert P. B., Houts S. E. Interactions between chemotaxis genes and flagellar genes in Escherichia coli. J Bacteriol. 1983 Jul;155(1):265–274. doi: 10.1128/jb.155.1.265-274.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Parkinson J. S., Revello P. T. Sensory adaptation mutants of E. coli. Cell. 1978 Dec;15(4):1221–1230. doi: 10.1016/0092-8674(78)90048-x. [DOI] [PubMed] [Google Scholar]
  45. Ravid S., Eisenbach M. Direction of flagellar rotation in bacterial cell envelopes. J Bacteriol. 1984 Apr;158(1):222–230. doi: 10.1128/jb.158.1.222-230.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Reader R. W., Tso W. W., Springer M. S., Goy M. F., Adler J. Pleiotropic aspartate taxis and serine taxis mutants of Escherichia coli. J Gen Microbiol. 1979 Apr;111(2):363–374. doi: 10.1099/00221287-111-2-363. [DOI] [PubMed] [Google Scholar]
  47. Rolinson G. N. Effect of beta-lactam antibiotics on bacterial cell growth rate. J Gen Microbiol. 1980 Oct;120(2):317–323. doi: 10.1099/00221287-120-2-317. [DOI] [PubMed] [Google Scholar]
  48. Russo A. F., Koshland D. E., Jr Separation of signal transduction and adaptation functions of the aspartate receptor in bacterial sensing. Science. 1983 Jun 3;220(4601):1016–1020. doi: 10.1126/science.6302843. [DOI] [PubMed] [Google Scholar]
  49. Segall J. E., Manson M. D., Berg H. C. Signal processing times in bacterial chemotaxis. Nature. 1982 Apr 29;296(5860):855–857. doi: 10.1038/296855a0. [DOI] [PubMed] [Google Scholar]
  50. Silverman M. R., Simon M. I. Flagellar assembly mutants in Escherichia coli. J Bacteriol. 1972 Nov;112(2):986–993. doi: 10.1128/jb.112.2.986-993.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Silverman M., Matsumura P., Simon M. The identification of the mot gene product with Escherichia coli-lambda hybrids. Proc Natl Acad Sci U S A. 1976 Sep;73(9):3126–3130. doi: 10.1073/pnas.73.9.3126. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Silverman M., Simon M. Flagellar rotation and the mechanism of bacterial motility. Nature. 1974 May 3;249(452):73–74. doi: 10.1038/249073a0. [DOI] [PubMed] [Google Scholar]
  53. Snyder M. A., Stock J. B., Koshland D. E., Jr Role of membrane potential and calcium in chemotactic sensing by bacteria. J Mol Biol. 1981 Jun 25;149(2):241–257. doi: 10.1016/0022-2836(81)90300-4. [DOI] [PubMed] [Google Scholar]
  54. Springer M. S., Goy M. F., Adler J. Protein methylation in behavioural control mechanisms and in signal transduction. Nature. 1979 Jul 26;280(5720):279–284. doi: 10.1038/280279a0. [DOI] [PubMed] [Google Scholar]
  55. Spudich J. L., Koshland D. E., Jr Quantitation of the sensory response in bacterial chemotaxis. Proc Natl Acad Sci U S A. 1975 Feb;72(2):710–713. doi: 10.1073/pnas.72.2.710. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Szmelcman S., Adler J. Change in membrane potential during bacterial chemotaxis. Proc Natl Acad Sci U S A. 1976 Dec;73(12):4387–4391. doi: 10.1073/pnas.73.12.4387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Tanner J. E. Intracellular diffusion of water. Arch Biochem Biophys. 1983 Jul 15;224(2):416–428. doi: 10.1016/0003-9861(83)90228-x. [DOI] [PubMed] [Google Scholar]
  58. Tsang N., Macnab R., Koshland D. E., Jr Common mechanism for repellents and attractants in bacterial chemotaxis. Science. 1973 Jul 6;181(4094):60–63. doi: 10.1126/science.181.4094.60. [DOI] [PubMed] [Google Scholar]
  59. Yonekawa H., Hayashi H., Parkinson J. S. Requirement of the cheB function for sensory adaptation in Escherichia coli. J Bacteriol. 1983 Dec;156(3):1228–1235. doi: 10.1128/jb.156.3.1228-1235.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]

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