Skip to main content
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1983 Aug;155(2):565–577. doi: 10.1128/jb.155.2.565-577.1983

Genetics of methyl-accepting chemotaxis proteins in Escherichia coli: organization of the tar region.

M K Slocum, J S Parkinson
PMCID: PMC217724  PMID: 6307970

Abstract

The tar locus of Escherichia coli specifies one of the major species of methyl-accepting proteins involved in the chemotactic behavior of this organism. The physical and genetic organization of the tar region was investigated with a series of specialized lambda transducing phages and plasmid clones. The tar gene was mapped at the promoter-proximal end of an operon containing five other chemotaxis-related loci. Four of those genes (cheR, cheB, cheY and cheZ) are required for all chemotactic responses; consequently, polar mutations in the tar gene resulted in a generally nonchemotactic phenotype. The fifth gene, tap, was mapped between the tar and cheR loci and specified the production of a 65-kilodalton methyl-accepting protein. Unlike the tar locus, which is required for chemotaxis to aspartate and maltose, mutants lacking only the tap function had no obvious defects in chemotactic ability. Genetic and physical maps of the tar-tap region were constructed with Mu d1 (Apr lac) insertion mutations, whose polar properties conferred a phenotype suitable for deletion mapping studies. Restriction endonuclease analyses of phage and plasmid clones indicated that all of the genetic coding capacity in the tar region is now accounted for.

Full text

PDF
565

Images in this article

Selected References

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

  1. 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]
  2. 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]
  3. Boyd A., Krikos A., Simon M. Sensory transducers of E. coli are encoded by homologous genes. Cell. 1981 Nov;26(3 Pt 1):333–343. doi: 10.1016/0092-8674(81)90202-6. [DOI] [PubMed] [Google Scholar]
  4. Boyd A., Simon M. I. Multiple electrophoretic forms of methyl-accepting chemotaxis proteins generated by stimulus-elicited methylation in Escherichia coli. J Bacteriol. 1980 Aug;143(2):809–815. doi: 10.1128/jb.143.2.809-815.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Casadaban M. J., Cohen S. N. Lactose genes fused to exogenous promoters in one step using a Mu-lac bacteriophage: in vivo probe for transcriptional control sequences. Proc Natl Acad Sci U S A. 1979 Sep;76(9):4530–4533. doi: 10.1073/pnas.76.9.4530. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Chelsky D., Dahlquist F. W. Structural studies of methyl-accepting chemotaxis proteins of Escherichia coli: evidence for multiple methylation sites. Proc Natl Acad Sci U S A. 1980 May;77(5):2434–2438. doi: 10.1073/pnas.77.5.2434. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. DeFranco A. L., Koshland D. E., Jr Multiple methylation in processing of sensory signals during bacterial chemotaxis. Proc Natl Acad Sci U S A. 1980 May;77(5):2429–2433. doi: 10.1073/pnas.77.5.2429. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Engström P., Hazelbauer G. L. Multiple methylation of methyl-accepting chemotaxis proteins during adaptation of E. coli to chemical stimuli. Cell. 1980 May;20(1):165–171. doi: 10.1016/0092-8674(80)90244-5. [DOI] [PubMed] [Google Scholar]
  9. Hedblom M. L., Adler J. Genetic and biochemical properties of Escherichia coli mutants with defects in serine chemotaxis. J Bacteriol. 1980 Dec;144(3):1048–1060. doi: 10.1128/jb.144.3.1048-1060.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Ish-Horowicz D., Burke J. F. Rapid and efficient cosmid cloning. Nucleic Acids Res. 1981 Jul 10;9(13):2989–2998. doi: 10.1093/nar/9.13.2989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Kihara M., Macnab R. M. Cytoplasmic pH mediates pH taxis and weak-acid repellent taxis of bacteria. J Bacteriol. 1981 Mar;145(3):1209–1221. doi: 10.1128/jb.145.3.1209-1221.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Kleene S. J., Toews M. L., Adler J. Isolation of glutamic acid methyl ester from an Escherichia coli membrane protein involved in chemotaxis. J Biol Chem. 1977 May 25;252(10):3214–3218. [PubMed] [Google Scholar]
  13. Koiwai O., Hayashi H. Studies on bacterial chemotaxis. IV. Interaction of maltose receptor with a membrane-bound chemosensing component. J Biochem. 1979 Jul;86(1):27–34. [PubMed] [Google Scholar]
  14. Komeda Y., Iino T. Regulation of expression of the flagellin gene (hag) in Escherichia coli K-12: analysis of hag-lac gene fusions. J Bacteriol. 1979 Sep;139(3):721–729. doi: 10.1128/jb.139.3.721-729.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. 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]
  16. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  17. 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]
  18. 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]
  19. Maeda K., Imae Y. Thermosensory transduction in Escherichia coli: inhibition of the thermoresponse by L-serine. Proc Natl Acad Sci U S A. 1979 Jan;76(1):91–95. doi: 10.1073/pnas.76.1.91. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Matsumura P., Silverman M., Simon M. Synthesis of mot and che gene products of Escherichia coli programmed by hybrid ColE1 plasmids in minicells. J Bacteriol. 1977 Dec;132(3):996–1002. doi: 10.1128/jb.132.3.996-1002.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. 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]
  22. 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]
  23. Parkinson J. S. Novel mutations affecting a signaling component for chemotaxis of Escherichia coli. J Bacteriol. 1980 Jun;142(3):953–961. doi: 10.1128/jb.142.3.953-961.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. 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]
  25. Rollins C., Dahlquist F. W. The methyl-accepting chemotaxis proteins of E. coli: a repellent-stimulated, covalent modification, distinct from methylation. Cell. 1981 Aug;25(2):333–340. doi: 10.1016/0092-8674(81)90051-9. [DOI] [PubMed] [Google Scholar]
  26. 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]
  27. Sherris D., Parkinson J. S. Posttranslational processing of methyl-accepting chemotaxis proteins in Escherichia coli. Proc Natl Acad Sci U S A. 1981 Oct;78(10):6051–6055. doi: 10.1073/pnas.78.10.6051. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. 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]
  29. 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]
  30. 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]
  31. Smith R. A., Parkinson J. S. Overlapping genes at the cheA locus of Escherichia coli. Proc Natl Acad Sci U S A. 1980 Sep;77(9):5370–5374. doi: 10.1073/pnas.77.9.5370. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. 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]
  33. 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]
  34. 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 U S A. 1977 Feb;74(2):533–537. doi: 10.1073/pnas.74.2.533. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. 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]
  36. 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]
  37. Tso W. W., Adler J. Negative chemotaxis in Escherichia coli. J Bacteriol. 1974 May;118(2):560–576. doi: 10.1128/jb.118.2.560-576.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Van Der Werf P., Koshland D. E., Jr Identification of a gamma-glutamyl methyl ester in bacterial membrane protein involved in chemotaxis. J Biol Chem. 1977 Apr 25;252(8):2793–2795. [PubMed] [Google Scholar]
  39. Wang E. A., Koshland D. E., Jr Receptor structure in the bacterial sensing system. Proc Natl Acad Sci U S A. 1980 Dec;77(12):7157–7161. doi: 10.1073/pnas.77.12.7157. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Wang E. A., Mowry K. L., Clegg D. O., Koshland D. E., Jr Tandem duplication and multiple functions of a receptor gene in bacterial chemotaxis. J Biol Chem. 1982 May 10;257(9):4673–4676. [PubMed] [Google Scholar]

Articles from Journal of Bacteriology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES