Skip to main content
PMC home page
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1987 Jan;169(1):371–379. doi: 10.1128/jb.169.1.371-379.1987

Phenol: a complex chemoeffector in bacterial chemotaxis.

Y Imae, K Oosawa, T Mizuno, M Kihara, R M Macnab
PMCID: PMC211777  PMID: 3025180

Abstract

Earlier observations that phenol is a repellent for Salmonella typhimurium but an attractant for Escherichia coli were confirmed. This behavioral difference was found to correlate with a difference in the effect phenol had on receptor methylation levels; it caused net demethylation in S. typhimurium but net methylation in E. coli. On the basis of mutant behavior and measurement of phenol-stimulated methylation, the attractant response of E. coli was shown to be mediated principally by the Tar receptor. In S. typhimurium, two receptors were found to be sensitive to phenol, namely, an unidentified receptor, which mediated the repellent response and showed phenol-stimulated demethylation; and the Tar receptor, which (as with E. coli) mediated the attractant response and showed phenol-stimulated methylation. In wild-type S. typhimurium, the former receptor dominated the Tar receptor, with respect to both behavior and methylation changes. However, when the amount of Tar receptor was artificially increased by the use of Tar-encoding plasmids, S. typhimurium cells exhibited an attractant response to phenol. No protein analogous to the phenol-specific repellent receptor was evident in E. coli, explaining the different behavioral responses of the two species toward phenol.

Full text

PDF

Images in this article

375Image
on p.375
375Image
on p.375
377Image
on p.377

Selected References

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

  1. Adler J., Hazelbauer G. L., Dahl M. M. Chemotaxis toward sugars in Escherichia coli. J Bacteriol. 1973 Sep;115(3):824–847. doi: 10.1128/jb.115.3.824-847.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. 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]
  3. 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]
  4. Bollinger J., Park C., Harayama S., Hazelbauer G. L. Structure of the Trg protein: Homologies with and differences from other sensory transducers of Escherichia coli. Proc Natl Acad Sci U S A. 1984 Jun;81(11):3287–3291. doi: 10.1073/pnas.81.11.3287. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. 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]
  6. Bullas L. R., Ryu J. I. Salmonella typhimurium LT2 strains which are r- m+ for all three chromosomally located systems of DNA restriction and modification. J Bacteriol. 1983 Oct;156(1):471–474. doi: 10.1128/jb.156.1.471-474.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. 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]
  8. Dahl M. K., Manson M. D. Interspecific reconstitution of maltose transport and chemotaxis in Escherichia coli with maltose-binding protein from various enteric bacteria. J Bacteriol. 1985 Dec;164(3):1057–1063. doi: 10.1128/jb.164.3.1057-1063.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Dang C. V., Niwano M., Ryu J., Taylor B. L. Inversion of aerotactic response in Escherichia coli deficient in cheB protein methylesterase. J Bacteriol. 1986 Apr;166(1):275–280. doi: 10.1128/jb.166.1.275-280.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Harayama S., Palva E. T., Hazelbauer G. L. Transposon-insertion mutants of Escherichia coli K12 defective in a component common to galactose and ribose chemotaxis. Mol Gen Genet. 1979 Mar 20;171(2):193–203. doi: 10.1007/BF00270005. [DOI] [PubMed] [Google Scholar]
  11. 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]
  12. Ingolia T. D., Koshland D. E., Jr Response to a metal ion-citrate complex in bacterial sensing. J Bacteriol. 1979 Dec;140(3):798–804. doi: 10.1128/jb.140.3.798-804.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. 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]
  14. Kihara M., Macnab R. M. Chemotaxis of Salmonella typhimurium toward citrate. J Bacteriol. 1979 Oct;140(1):297–300. doi: 10.1128/jb.140.1.297-300.1979. [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. 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]
  17. Krikos A., Mutoh N., Boyd A., Simon M. I. Sensory transducers of E. coli are composed of discrete structural and functional domains. Cell. 1983 Jun;33(2):615–622. doi: 10.1016/0092-8674(83)90442-7. [DOI] [PubMed] [Google Scholar]
  18. Lederberg J. Linear Inheritance in Transductional Clones. Genetics. 1956 Nov;41(6):845–871. doi: 10.1093/genetics/41.6.845. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Manson M. D., Blank V., Brade G., Higgins C. F. Peptide chemotaxis in E. coli involves the Tap signal transducer and the dipeptide permease. Nature. 1986 May 15;321(6067):253–256. doi: 10.1038/321253a0. [DOI] [PubMed] [Google Scholar]
  20. Mizuno T., Imae Y. Conditional inversion of the thermoresponse in Escherichia coli. J Bacteriol. 1984 Jul;159(1):360–367. doi: 10.1128/jb.159.1.360-367.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Mizuno T., Mutoh N., Panasenko S. M., Imae Y. Acquisition of maltose chemotaxis in Salmonella typhimurium by the introduction of the Escherichia coli chemosensory transducer gene. J Bacteriol. 1986 Mar;165(3):890–895. doi: 10.1128/jb.165.3.890-895.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. 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]
  23. Oosawa K., Imae Y. Demethylation of methyl-accepting chemotaxis proteins in Escherichia coli induced by the repellents glycerol and ethylene glycol. J Bacteriol. 1984 Feb;157(2):576–581. doi: 10.1128/jb.157.2.576-581.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Oosawa K., Imae Y. Glycerol and ethylene glycol: members of a new class of repellents of Escherichia coli chemotaxis. J Bacteriol. 1983 Apr;154(1):104–112. doi: 10.1128/jb.154.1.104-112.1983. [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., 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]
  27. 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]
  28. 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]
  29. Russo A. F., Koshland D. E., Jr Identification of the tip-encoded receptor in bacterial sensing. J Bacteriol. 1986 Jan;165(1):276–282. doi: 10.1128/jb.165.1.276-282.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. 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]
  31. Shioi J., Taylor B. L. Oxygen taxis and proton motive force in Salmonella typhimurium. J Biol Chem. 1984 Sep 10;259(17):10983–10988. [PubMed] [Google Scholar]
  32. 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]
  33. Slocum M. K., Parkinson J. S. Genetics of methyl-accepting chemotaxis proteins in Escherichia coli: null phenotypes of the tar and tap genes. J Bacteriol. 1985 Aug;163(2):586–594. doi: 10.1128/jb.163.2.586-594.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Slocum M. K., Parkinson J. S. Genetics of methyl-accepting chemotaxis proteins in Escherichia coli: organization of the tar region. J Bacteriol. 1983 Aug;155(2):565–577. doi: 10.1128/jb.155.2.565-577.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Slonczewski J. L., Macnab R. M., Alger J. R., Castle A. M. Effects of pH and repellent tactic stimuli on protein methylation levels in Escherichia coli. J Bacteriol. 1982 Oct;152(1):384–399. doi: 10.1128/jb.152.1.384-399.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. 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]
  37. 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]
  38. 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]
  39. 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]
  40. 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]

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

RESOURCES