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. 1983 May;154(2):604–611. doi: 10.1128/jb.154.2.604-611.1983

Correlation between bacteriophage chi adsorption and mode of flagellar rotation of Escherichia coli chemotaxis mutants.

S Ravid, M Eisenbach
PMCID: PMC217507  PMID: 6341356

Abstract

We studied the adsorption of phage chi to various behavioral mutants (che mutants) of Escherichia coli having different swimming modes. Bacteriophage chi infects only bacteria with active flagella, and it was therefore of interest to examine whether the mode of swimming has an effect on the susceptibility of the bacteria to the phage. Neither the mode of swimming (smooth swimming or tumbling) nor the direction of flagellar rotation affected the degree of chi adsorption to the bacterial cells. Furthermore, the tumbling frequency, the rotation speed (tethered cells of all of the strains examined had the same average speed of rotation), the time proportion of rotation, and the reversal frequency were not important in determining susceptibility to chi. The only variable that influenced chi adsorption was the fraction of the population whose flagella rotated incessantly. A direct, linear correlation was found between chi adsorption and the fraction of unceasing rotation in each population. It seems, therefore, that an individual bacterium whose flagella pause periodically and briefly during rotation is not susceptible to irreversible adsorption of the phage. Pausing of rotation thus seems to be a new feature of motility that is prevalent especially in che mutants. It is concluded that irreversible chi adsorption can serve as a quantitative assay only for incessant flagellar rotation of E. coli.

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Selected References

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

  1. Appelbaum P. C., Hugo N., Coetzee J. N. A flagellar phage for the proteus-providence group. J Gen Virol. 1971 Oct;13(1):153–162. doi: 10.1099/0022-1317-13-1-153. [DOI] [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. Armstrong J. B., Adler J. Genetics of motility in Escherichia coli: complementation of paralysed mutants. Genetics. 1967 Jul;56(3):363–373. doi: 10.1093/genetics/56.3.363. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bayer M. E., Bayer M. H. Fast responses of bacterial membranes to virus adsorption: a fluorescence study. Proc Natl Acad Sci U S A. 1981 Sep;78(9):5618–5622. doi: 10.1073/pnas.78.9.5618. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. 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]
  6. 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]
  7. 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]
  8. DeFranco A. L., Koshland D. E., Jr Construction and behavior of strains with mutations in two chemotaxis genes. J Bacteriol. 1982 Jun;150(3):1297–1301. doi: 10.1128/jb.150.3.1297-1301.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. 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]
  10. Eisenbach M., Adler J. Bacterial cell envelopes with functional flagella. J Biol Chem. 1981 Aug 25;256(16):8807–8814. [PubMed] [Google Scholar]
  11. 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]
  12. Hirota N., Matsuura S., Mochizuki N., Mutoh N., Imae Y. Use of lipophilic cation-permeable mutants for measurement of transmembrane electrical potential in metabolizing cells of Escherichia coli. J Bacteriol. 1981 Nov;148(2):399–405. doi: 10.1128/jb.148.2.399-405.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Icho T., Iino T. Isolation and characterization of motile Escherichia coli mutants resistant to bacteriophage chi. J Bacteriol. 1978 Jun;134(3):854–860. doi: 10.1128/jb.134.3.854-860.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Iino T., Mitani M. A mutant of Salmonella possessing straight flagella. J Gen Microbiol. 1967 Oct;49(1):81–88. doi: 10.1099/00221287-49-1-81. [DOI] [PubMed] [Google Scholar]
  15. Iino T., Mitani M. Infection of Serratia marcescens by bacteriophage chi. J Virol. 1967 Apr;1(2):445–447. doi: 10.1128/jvi.1.2.445-447.1967. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. 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]
  17. Komeda Y., Silverman M., Simon M. Identification of the structural gene for the hook subunit protein of Escherichia coli flagella. J Bacteriol. 1978 Jan;133(1):364–371. doi: 10.1128/jb.133.1.364-371.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. 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]
  19. 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]
  20. MEYNELL E. W. A phage, phi chi, which attacks motile bacteria. J Gen Microbiol. 1961 Jun;25:253–290. doi: 10.1099/00221287-25-2-253. [DOI] [PubMed] [Google Scholar]
  21. 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]
  22. 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]
  23. 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]
  24. 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]
  25. SECHAUD J., KELLENBERGER E. Lyse précoce, provoquée par le chloroforme, chez les bactéries infectées par du bactériophage. Ann Inst Pasteur (Paris) 1956 Jan;90(1):102–106. [PubMed] [Google Scholar]
  26. Schade S. Z., Adler J., Ris H. How bacteriophage chi attacks motile bacteria. J Virol. 1967 Jun;1(3):599–609. doi: 10.1128/jvi.1.3.599-609.1967. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Schade S., Adler J. Purification and chemistry of bacteriophage chi. J Virol. 1967 Jun;1(3):591–598. doi: 10.1128/jvi.1.3.591-598.1967. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Thipayathasana P., Valentine R. The requirement for energy transducing ATPase for anaerobic motility in Escherichia coli. Biochim Biophys Acta. 1974 Jun 28;347(3):464–468. doi: 10.1016/0005-2728(74)90083-8. [DOI] [PubMed] [Google Scholar]
  29. 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]
  30. Toews M. L., Goy M. F., Springer M. S., Adler J. Attractants and repellents control demethylation of methylated chemotaxis proteins in Escherichia coli. Proc Natl Acad Sci U S A. 1979 Nov;76(11):5544–5548. doi: 10.1073/pnas.76.11.5544. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. 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]

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