Skip to main content
NCBI home page
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1980 Dec;144(3):1048–1060. doi: 10.1128/jb.144.3.1048-1060.1980

Genetic and biochemical properties of Escherichia coli mutants with defects in serine chemotaxis.

M L Hedblom, J Adler
PMCID: PMC294770  PMID: 6777365

Abstract

In Escherichia coli, taxis to certain chemoeffectors is mediated through an intrinsic membrane protein called methyl-accepting chemotaxis protein I (MCP I), which is the product of the tsr gene. Mutants were selected that are defective in taxis toward all MCP I-mediated attractants (alpha-aminoisobutyrate, L-alanine, glycine, and L-serine) but are normal to MCP I-mediated repellents and to chemoeffectors mediated by other MCPs. The mutants could be divided into two classes based on their ability to respond to various concentrations of L-serine. Two MCP I-mediated L-serine systems appear to function in the wild type: one of high and one of lower affinity. The mutations responsible for the serine taxis defects map at about 99 min on the E. coli chromosome and are not complemented by episomes carrying mutations in the tsr gene; this suggests that they are defective in tsr function. Low concentrations of L-[14C]serine specifically bound to wild-type membranes with a Km of 5 microM; in contrast, there was greatly decreased binding to vesicles prepared from the new mutants or from the tsr mutant AW518. Binding of labeled serine to wild-type vesicles was inhibited by MCP I-mediated attractants, but not by MCP II-mediated attractants. The data suggest that MCP I may function as the L-serine chemoreceptor in E. coli.

Full text

PDF
1048

Images in this article

1053Image
on p.1053
1055Image
on p.1055

Selected References

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

  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. Chemotaxis in bacteria. Science. 1966 Aug 12;153(3737):708–716. doi: 10.1126/science.153.3737.708. [DOI] [PubMed] [Google Scholar]
  3. Adler J., Epstein W. Phosphotransferase-system enzymes as chemoreceptors for certain sugars in Escherichia coli chemotaxis. Proc Natl Acad Sci U S A. 1974 Jul;71(7):2895–2899. doi: 10.1073/pnas.71.7.2895. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. 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]
  5. Aksamit R. R., Koshland D. E., Jr Identification of the ribose binding protein as the receptor for ribose chemotaxis in Salmonella typhimurium. Biochemistry. 1974 Oct 22;13(22):4473–4478. doi: 10.1021/bi00719a001. [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. 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]
  8. 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]
  9. 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]
  10. Cosloy S. D. D-serine transport system in Escherichia coli K-12. J Bacteriol. 1973 May;114(2):679–684. doi: 10.1128/jb.114.2.679-684.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. 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]
  12. 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]
  13. Galloway D. R., Furlong C. E. The role of ribose-binding protein in transport and chemotaxis in Escherichia coli K12. Arch Biochem Biophys. 1977 Dec;184(2):496–504. doi: 10.1016/0003-9861(77)90459-3. [DOI] [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. Hazelbauer G. L., Adler J. Role of the galactose binding protein in chemotaxis of Escherichia coli toward galactose. Nat New Biol. 1971 Mar 24;230(12):101–104. doi: 10.1038/newbio230101a0. [DOI] [PubMed] [Google Scholar]
  16. Hazelbauer G. L. Maltose chemoreceptor of Escherichia coli. J Bacteriol. 1975 Apr;122(1):206–214. doi: 10.1128/jb.122.1.206-214.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Hazelbauer G. L., Mesibov R. E., Adler J. Escherichia coli mutants defective in chemotaxis toward specific chemicals. Proc Natl Acad Sci U S A. 1969 Dec;64(4):1300–1307. doi: 10.1073/pnas.64.4.1300. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. 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]
  19. Koman A., Harayama S., Hazelbauer G. L. Relation of chemotactic response to the amount of receptor: evidence for different efficiencies of signal transduction. J Bacteriol. 1979 Jun;138(3):739–747. doi: 10.1128/jb.138.3.739-747.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. 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]
  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. LENNOX E. S. Transduction of linked genetic characters of the host by bacteriophage P1. Virology. 1955 Jul;1(2):190–206. doi: 10.1016/0042-6822(55)90016-7. [DOI] [PubMed] [Google Scholar]
  23. LOWRY O. H., ROSEBROUGH N. J., FARR A. L., RANDALL R. J. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951 Nov;193(1):265–275. [PubMed] [Google Scholar]
  24. Langer R., Fefferman M., Gryska P., Bergman K. A simple method for studying chemotaxis using sustained release of attractants from inert polymers. Can J Microbiol. 1980 Feb;26(2):274–278. doi: 10.1139/m80-045. [DOI] [PubMed] [Google Scholar]
  25. Lengeler J. Nature and properties of hexitol transport systems in Escherichia coli. J Bacteriol. 1975 Oct;124(1):39–47. doi: 10.1128/jb.124.1.39-47.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. 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]
  27. 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]
  28. Mesibov R., Ordal G. W., Adler J. The range of attractant concentrations for bacterial chemotaxis and the threshold and size of response over this range. Weber law and related phenomena. J Gen Physiol. 1973 Aug;62(2):203–223. doi: 10.1085/jgp.62.2.203. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Muskavitch M. A., Kort E. N., Springer M. S., Goy M. F., Adler J. Attraction by repellents: an error in sensory information processing by bacterial mutants. Science. 1978 Jul 7;201(4350):63–65. doi: 10.1126/science.351803. [DOI] [PubMed] [Google Scholar]
  30. Ordal G. W., Adler J. Isolation and complementation of mutants in galactose taxis and transport. J Bacteriol. 1974 Feb;117(2):509–516. doi: 10.1128/jb.117.2.509-516.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Ordal G. W., Adler J. Properties of mutants in galactose taxis and transport. J Bacteriol. 1974 Feb;117(2):517–526. doi: 10.1128/jb.117.2.517-526.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Ordal G. W., Villani D. P., Nicholas R. A., Hamel F. G. Independence of proline chemotaxis and transport in Bacillus subtilis. J Biol Chem. 1978 Jul 25;253(14):4916–4919. [PubMed] [Google Scholar]
  33. 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]
  34. 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]
  35. Piperno J. R., Oxender D. L. Amino acid transport systems in Escherichia coli K-12. J Biol Chem. 1968 Nov 25;243(22):5914–5920. [PubMed] [Google Scholar]
  36. 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]
  37. Robbins J. C., Oxender D. L. Transport systems for alanine, serine, and glycine in Escherichia coli K-12. J Bacteriol. 1973 Oct;116(1):12–18. doi: 10.1128/jb.116.1.12-18.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. SWANSTROM M., ADAMS M. H. Agar layer method for production of high titer phage stocks. Proc Soc Exp Biol Med. 1951 Nov;78(2):372–375. doi: 10.3181/00379727-78-19076. [DOI] [PubMed] [Google Scholar]
  39. Short S. A., Kaback H. R., Kohn L. D. Localization of D-lactate dehydrogenase in native and reconstituted Escherichia coli membrane vesicles. J Biol Chem. 1975 Jun 10;250(11):4291–4296. [PubMed] [Google Scholar]
  40. 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]
  41. 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]
  42. 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]
  43. 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]
  44. Strange P. G., Koshland D. E., Jr Receptor interactions in a signalling system: competition between ribose receptor and galactose receptor in the chemotaxis response. Proc Natl Acad Sci U S A. 1976 Mar;73(3):762–766. doi: 10.1073/pnas.73.3.762. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Toews M. L., Adler J. Methanol formation in vivo from methylated chemotaxis proteins in Escherichia coli. J Biol Chem. 1979 Mar 25;254(6):1761–1764. [PubMed] [Google Scholar]
  46. 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]
  47. 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]
  48. 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]
  49. Wargel R. J., Shadur C. A., Neuhaus F. C. Mechanism of D-cycloserine action: transport systems for D-alanine, D-cycloserine, L-alanine, and glycine. J Bacteriol. 1970 Sep;103(3):778–788. doi: 10.1128/jb.103.3.778-788.1970. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Wu T. T. A model for three-point analysis of random general transduction. Genetics. 1966 Aug;54(2):405–410. doi: 10.1093/genetics/54.2.405. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES