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. 1980 May;142(2):527–534. doi: 10.1128/jb.142.2.527-534.1980

Tumbling chemotaxis mutants of Escherichia coli: possible gene-dependent effect of methionine starvation.

H Kondoh
PMCID: PMC294018  PMID: 6991478

Abstract

Some mutants defective in chemotaxis show incessant tumbling behavior and are called tumbling mutants. Previously described tumbling mutations lie in two genes, cheB and cheZ (41.5 min on Escherichia coli map). Genetic analysis of various tumbling mutants, however, revealed that two more genetic loci, cheC (43 min) and cheE (99.2 min), could also mutate to produce tumbling mutants. The genetic map around cheC was revised: his flaP flaQ flaR flbD flaA (= cheC) flaE. flbD is a new gene. When cells were starved for methionine, the tumbling mutants changed their swimming behavior depending on the che gene mutated. cheZ mutants, like wild-type bacteria, ceased tumbling shortly after removal of methionine. The tumbling of cheB or cheE mutants was depressed after prolonged methionine starvation in the presence of a constant level of an attractant. cheC tumbling mutants appeared unique in that they did not cease tumbling even when cells were deprived of methionine. By contrast, arsenate treatment of the tumbling mutants resulted in smooth swimming of the cells in every case. These results suggest that two different processes are involved in regulation of tumbling; one requiring methionine and the other requiring some phosphorylated compound.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Adler J., Dahl M. M. A method for measuring the motility of bacteria and for comparing random and non-random motility. J Gen Microbiol. 1967 Feb;46(2):161–173. doi: 10.1099/00221287-46-2-161. [DOI] [PubMed] [Google Scholar]
  2. Armstrong J. B., Adler J. Complementation of nonchemotactic mutants of Escherichia coli. Genetics. 1969 Jan;61(1):61–66. doi: 10.1093/genetics/61.1.61. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. 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]
  4. 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]
  5. 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]
  6. Aswad D., Koshland D. E., Jr Isolation, characterization and complementation of Salmonella typhimurium chemotaxis mutants. J Mol Biol. 1975 Sep 15;97(2):225–235. doi: 10.1016/s0022-2836(75)80036-2. [DOI] [PubMed] [Google Scholar]
  7. Aswad D., Koshland D. E., Jr Role of methionine in bacterial chemotaxis. J Bacteriol. 1974 May;118(2):640–645. doi: 10.1128/jb.118.2.640-645.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Bachmann B. J., Low K. B., Taylor A. L. Recalibrated linkage map of Escherichia coli K-12. Bacteriol Rev. 1976 Mar;40(1):116–167. doi: 10.1128/br.40.1.116-167.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. 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]
  10. Berg H. C. Dynamic properties of bacterial flagellar motors. Nature. 1974 May 3;249(452):77–79. doi: 10.1038/249077a0. [DOI] [PubMed] [Google Scholar]
  11. Brown D. A., Berg H. C. Temporal stimulation of chemotaxis in Escherichia coli. Proc Natl Acad Sci U S A. 1974 Apr;71(4):1388–1392. doi: 10.1073/pnas.71.4.1388. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Collins A. L., Stocker B. A. Salmonella typhimurium mutants generally defective in chemotaxis. J Bacteriol. 1976 Dec;128(3):754–765. doi: 10.1128/jb.128.3.754-765.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Gardner J. F., Smith O. H. Operator-promoter functions in the threonine operon of Escherichia coli. J Bacteriol. 1975 Oct;124(1):161–166. doi: 10.1128/jb.124.1.161-166.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. 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]
  15. Goy M. F., Springer M. S., Adler J. Sensory transduction in Escherichia coli: role of a protein methylation reaction in sensory adaptation. Proc Natl Acad Sci U S A. 1977 Nov;74(11):4964–4968. doi: 10.1073/pnas.74.11.4964. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hayashi H., Koiwai O., Kozuka M. Studies on bacterial chemotaxis. II. Effect of cheB and cheZ mutations on the methylation of methyl-accepting chemotaxis protein of Escherichia coli. J Biochem. 1979 May;85(5):1213–1223. [PubMed] [Google Scholar]
  17. Khan S., Macnab R. M., DeFranco A. L., Koshland D. E., Jr Inversion of a behavioral response in bacterial chemotaxis: explanation at the molecular level. Proc Natl Acad Sci U S A. 1978 Sep;75(9):4150–4154. doi: 10.1073/pnas.75.9.4150. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Kondoh H., Ball C. B., Adler J. Identification of a methyl-accepting chemotaxis protein for the ribose and galactose chemoreceptors of Escherichia coli. Proc Natl Acad Sci U S A. 1979 Jan;76(1):260–264. doi: 10.1073/pnas.76.1.260. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kondoh H. Isolation and characterization of nondefective transducing lambda bacteriophages carrying fla genes of Escherichia coli K-12. J Bacteriol. 1977 May;130(2):736–745. doi: 10.1128/jb.130.2.736-745.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Kondoh H., Ozeki H. Deletion and amber mutants of fla loci in Escherichia coli K-12. Genetics. 1976 Nov;84(3):403–421. doi: 10.1093/genetics/84.3.403. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Kort E. N., Goy M. F., Larsen S. H., Adler J. Methylation of a membrane protein involved in bacterial chemotaxis. Proc Natl Acad Sci U S A. 1975 Oct;72(10):3939–3943. doi: 10.1073/pnas.72.10.3939. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Larsen S. H., Adler J., Gargus J. J., Hogg R. W. Chemomechanical coupling without ATP: the source of energy for motility and chemotaxis in bacteria. Proc Natl Acad Sci U S A. 1974 Apr;71(4):1239–1243. doi: 10.1073/pnas.71.4.1239. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. 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]
  24. 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]
  25. 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]
  26. Parkinson J. S. Data processing by the chemotaxis machinery of Escherichia coli. Nature. 1974 Nov 22;252(5481):317–319. doi: 10.1038/252317a0. [DOI] [PubMed] [Google Scholar]
  27. Parkinson J. S., Parker S. R. Interaction of the cheC and cheZ gene products is required for chemotactic behavior in Escherichia coli. Proc Natl Acad Sci U S A. 1979 May;76(5):2390–2394. doi: 10.1073/pnas.76.5.2390. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. 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]
  29. Parkinson J. S. cheA, cheB, and cheC genes of Escherichia coli and their role in chemotaxis. J Bacteriol. 1976 May;126(2):758–770. doi: 10.1128/jb.126.2.758-770.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. 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]
  31. Ridgway H. G., Silverman M., Simon M. I. Localization of proteins controlling motility and chemotaxis in Escherichia coli. J Bacteriol. 1977 Nov;132(2):657–665. doi: 10.1128/jb.132.2.657-665.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Shimada K., Weisberg R. A., Gottesman M. E. Prophage lambda at unusual chromosomal locations. I. Location of the secondary attachment sites and the properties of the lysogens. J Mol Biol. 1972 Feb 14;63(3):483–503. doi: 10.1016/0022-2836(72)90443-3. [DOI] [PubMed] [Google Scholar]
  33. Silverman M., Simon M. Chemotaxis in Escherichia coli: methylation of che gene products. Proc Natl Acad Sci U S A. 1977 Aug;74(8):3317–3321. doi: 10.1073/pnas.74.8.3317. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. 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]
  35. Silverman M., Simon M. Genetic analysis of bacteriophage Mu-induced flagellar mutants in Escherichia coli. J Bacteriol. 1973 Oct;116(1):114–122. doi: 10.1128/jb.116.1.114-122.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Silverman M., Simon M. Genetic analysis of flagellar mutants in Escherichia coli. J Bacteriol. 1973 Jan;113(1):105–113. doi: 10.1128/jb.113.1.105-113.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Silverman M., Simon M. Identification of polypeptides necessary for chemotaxis in Escherichia coli. J Bacteriol. 1977 Jun;130(3):1317–1325. doi: 10.1128/jb.130.3.1317-1325.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Silverman M., Simon M. Positioning flagellar genes in Escherichia coli by deletion analysis. J Bacteriol. 1974 Jan;117(1):73–79. doi: 10.1128/jb.117.1.73-79.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Springer M. S., Goy M. F., Adler J. Sensory transduction in Escherichia coli: a requirement for methionine in sensory adaptation. Proc Natl Acad Sci U S A. 1977 Jan;74(1):183–187. doi: 10.1073/pnas.74.1.183. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Springer M. S., Goy M. F., Adler J. Sensory transduction in Escherichia coli: two complementary pathways of information processing that involve methylated proteins. Proc Natl Acad Sci U S A. 1977 Aug;74(8):3312–3316. doi: 10.1073/pnas.74.8.3312. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Springer M. S., Kort E. N., Larsen S. H., Ordal G. W., Reader R. W., Adler J. Role of methionine in bacterial chemotaxis: requirement for tumbling and involvement in information processing. Proc Natl Acad Sci U S A. 1975 Nov;72(11):4640–4644. doi: 10.1073/pnas.72.11.4640. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. 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]
  43. Stock J. B., Koshland D. E., Jr A protein methylesterase involved in bacterial sensing. Proc Natl Acad Sci U S A. 1978 Aug;75(8):3659–3663. doi: 10.1073/pnas.75.8.3659. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. 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]
  45. VOGEL H. J., BONNER D. M. Acetylornithinase of Escherichia coli: partial purification and some properties. J Biol Chem. 1956 Jan;218(1):97–106. [PubMed] [Google Scholar]
  46. Vary P. S., Stocker B. A. Nonsense motility mutants in Salmonella typhimurium. Genetics. 1973 Feb;73(2):229–245. doi: 10.1093/genetics/73.2.229. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Warrick H. M., Taylor B. L., Koshland D. E., Jr Chemotactic mechanism of Salmonella typhimurium: preliminary mapping and characterization of mutants. J Bacteriol. 1977 Apr;130(1):223–231. doi: 10.1128/jb.130.1.223-231.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]

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