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. 1986 Dec;168(3):1172–1179. doi: 10.1128/jb.168.3.1172-1179.1986

Genetic evidence for a switching and energy-transducing complex in the flagellar motor of Salmonella typhimurium.

S Yamaguchi, S Aizawa, M Kihara, M Isomura, C J Jones, R M Macnab
PMCID: PMC213619  PMID: 3536867

Abstract

The flaAII.2, flaQ, and flaN genes of Salmonella typhimurium are important for assembly, rotation, and counterclockwise-clockwise switching of the flagellar motor. Paralyzed and nonchemotactic mutants were subjected to selection pressure for partial acquisition of motility and chemotaxis, and the suppressor mutations of the resulting pseudorevertants were mapped and isolated. Many of the intergenic suppressor mutations were in one of the other two genes. Others were in genes for cytoplasmic components of the chemotaxis system, notably cheY and cheZ; one of the mutations was found in the cheA gene and one in a motility gene, motB. Suppression among the three fla genes was allele specific, and many of the pseudorevertants were either cold sensitive or heat sensitive. We conclude that the FlaAII.2, FlaQ, and FlaN proteins form a complex which determines the rotational sense, either counterclockwise or clockwise, of the motor and also participates in the conversion of proton energy into mechanical work of rotation. This switch complex is probably mounted to the base of the flagellar basal body and, via binding of the CheY and CheZ proteins, receives sensory information and uses it to control flagellar operation.

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Selected References

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  1. Aizawa S. I., Dean G. E., Jones C. J., Macnab R. M., Yamaguchi S. Purification and characterization of the flagellar hook-basal body complex of Salmonella typhimurium. J Bacteriol. 1985 Mar;161(3):836–849. doi: 10.1128/jb.161.3.836-849.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. 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]
  3. 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]
  4. Clegg D. O., Koshland D. E., Jr Identification of a bacterial sensing protein and effects of its elevated expression. J Bacteriol. 1985 Apr;162(1):398–405. doi: 10.1128/jb.162.1.398-405.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. 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]
  6. DePamphilis M. L., Adler J. Fine structure and isolation of the hook-basal body complex of flagella from Escherichia coli and Bacillus subtilis. J Bacteriol. 1971 Jan;105(1):384–395. doi: 10.1128/jb.105.1.384-395.1971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Dean G. E., Aizawa S. I., Macnab R. M. flaAII (motC, cheV) of Salmonella typhimurium is a structural gene involved in energization and switching of the flagellar motor. J Bacteriol. 1983 Apr;154(1):84–91. doi: 10.1128/jb.154.1.84-91.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Dean G. E., Macnab R. M., Stader J., Matsumura P., Burks C. Gene sequence and predicted amino acid sequence of the motA protein, a membrane-associated protein required for flagellar rotation in Escherichia coli. J Bacteriol. 1984 Sep;159(3):991–999. doi: 10.1128/jb.159.3.991-999.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Dimmitt K., Simon M. Purification and thermal stability of intact Bacillus subtilis flagella. J Bacteriol. 1971 Jan;105(1):369–375. doi: 10.1128/jb.105.1.369-375.1971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Enomoto M. Genetic studies of paralyzed mutant in Salmonella. I. Genetic fine structure of the mot loci in Salmonella typhimurium. Genetics. 1966 Sep;54(3):715–726. doi: 10.1093/genetics/54.3.715. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Jarvik J., Botstein D. Conditional-lethal mutations that suppress genetic defects in morphogenesis by altering structural proteins. Proc Natl Acad Sci U S A. 1975 Jul;72(7):2738–2742. doi: 10.1073/pnas.72.7.2738. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. 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]
  13. Kuo S. C., Koshland D. E., Jr Sequence of the flaA (cheC) locus of Escherichia coli and discovery of a new gene. J Bacteriol. 1986 Jun;166(3):1007–1012. doi: 10.1128/jb.166.3.1007-1012.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Kutsukake K., Iino T., Komeda Y., Yamaguchi S. Functional homology of fla genes between Salmonella typhimurium and Escherichia coli. Mol Gen Genet. 1980 Apr;178(1):59–67. doi: 10.1007/BF00267213. [DOI] [PubMed] [Google Scholar]
  15. 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]
  16. Macnab R. M., Aizawa S. Bacterial motility and the bacterial flagellar motor. Annu Rev Biophys Bioeng. 1984;13:51–83. doi: 10.1146/annurev.bb.13.060184.000411. [DOI] [PubMed] [Google Scholar]
  17. Macnab R. M. Examination of bacterial flagellation by dark-field microscopy. J Clin Microbiol. 1976 Sep;4(3):258–265. doi: 10.1128/jcm.4.3.258-265.1976. [DOI] [PMC free article] [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. Manson M. D., Tedesco P., Berg H. C., Harold F. M., Van der Drift C. A protonmotive force drives bacterial flagella. Proc Natl Acad Sci U S A. 1977 Jul;74(7):3060–3064. doi: 10.1073/pnas.74.7.3060. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. 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]
  21. 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]
  22. Parkinson J. S., Parker S. R., Talbert P. B., Houts S. E. Interactions between chemotaxis genes and flagellar genes in Escherichia coli. J Bacteriol. 1983 Jul;155(1):265–274. doi: 10.1128/jb.155.1.265-274.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. 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]
  24. Ravid S., Eisenbach M. Direction of flagellar rotation in bacterial cell envelopes. J Bacteriol. 1984 Apr;158(1):222–230. doi: 10.1128/jb.158.1.222-230.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Ravid S., Matsumura P., Eisenbach M. Restoration of flagellar clockwise rotation in bacterial envelopes by insertion of the chemotaxis protein CheY. Proc Natl Acad Sci U S A. 1986 Oct;83(19):7157–7161. doi: 10.1073/pnas.83.19.7157. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. 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]
  27. Rubik B. A., Koshland D. E., Jr Potentiation, desensitization, and inversion of response in bacterial sensing of chemical stimuli. Proc Natl Acad Sci U S A. 1978 Jun;75(6):2820–2824. doi: 10.1073/pnas.75.6.2820. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. 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]
  29. Silverman M., Simon M. Operon controlling motility and chemotoxis in E. coli. Nature. 1976 Dec 9;264(5586):577–580. doi: 10.1038/264577a0. [DOI] [PubMed] [Google Scholar]
  30. Stader J., Matsumura P., Vacante D., Dean G. E., Macnab R. M. Nucleotide sequence of the Escherichia coli motB gene and site-limited incorporation of its product into the cytoplasmic membrane. J Bacteriol. 1986 Apr;166(1):244–252. doi: 10.1128/jb.166.1.244-252.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Suzuki T., Iino T., Horiguchi T., Yamaguchi S. Incomplete flagellar structures in nonflagellate mutants of Salmonella typhimurium. J Bacteriol. 1978 Feb;133(2):904–915. doi: 10.1128/jb.133.2.904-915.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Yamaguchi S., Fujita H., Ishihara A., Aizawa S., Macnab R. M. Subdivision of flagellar genes of Salmonella typhimurium into regions responsible for assembly, rotation, and switching. J Bacteriol. 1986 Apr;166(1):187–193. doi: 10.1128/jb.166.1.187-193.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Yamaguchi S., Iino T., Horiguchi T., Ota K. Genetic analysis of fla and mot cistrons closely linked to H1 in Salmonella abortusequi and its derivatives. J Gen Microbiol. 1972 Apr;70(1):59–75. doi: 10.1099/00221287-70-1-59. [DOI] [PubMed] [Google Scholar]

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