Abstract
Certain cheU mutants of Salmonella show inverted chemotactic behavior, being repelled by attractants and attracted by repellents. Such a dramatic change in behavioral pattern would seem at first glance to require drastic and complex alterations in the sensory processing system. In fact, the behavior can be explained by a simple shift in the level of a response regulator and the subtle effects of this shift on flagellar function. Flagella can exist in either a left-handed or a right-handed structure depending on applied torsion. Wild-type cells swim smoothly by counterclockwise rotation of a left-handed helical bundle and tumble when the motors briefly reverse to clockwise rotation (normal random motility). The cheU mutation causes a shift in response regulator level relative to the critical threshold value, resulting in extended clockwise operation so that the flagella are fully converted to the right-handed helical form. These cells therefore swim smoothly by clockwise rotation of a right-handed bundle and tumble when the motor briefly reverses to counterclockwise rotation (inverse random motility). Thus, tumbling is associated with brief reversals and not with a particular sense of rotation. A wild-type cell, with its steady-state response regulator level placing it initially in normal random motility, will swim smoothly on addition of attractant, whereas a cheU mutant with inverse random motility will tumble given the same stimulus. The phenomenon illustrates the profound behavioral consequences that can result from a single mutation in a key gene.
Keywords: flagella, polymorphism, cheU gene, response regulator
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- Adler J. Chemotaxis in bacteria. Annu Rev Biochem. 1975;44:341–356. doi: 10.1146/annurev.bi.44.070175.002013. [DOI] [PubMed] [Google Scholar]
- 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]
- 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]
- Hotani H. Light microscope study of mixed helices in reconstituted Salmonella flagella. J Mol Biol. 1976 Sep 5;106(1):151–166. doi: 10.1016/0022-2836(76)90305-3. [DOI] [PubMed] [Google Scholar]
- KERRIDGE D. The effect of amino acid analogues on the synthesis of bacterial flagella. Biochim Biophys Acta. 1959 Feb;31(2):579–581. doi: 10.1016/0006-3002(59)90048-4. [DOI] [PubMed] [Google Scholar]
- Kamiya R., Asakura S. Helical transformations of Salmonella flagella in vitro. J Mol Biol. 1976 Sep 5;106(1):167–186. doi: 10.1016/0022-2836(76)90306-5. [DOI] [PubMed] [Google Scholar]
- Koshland D. E., Jr A response regulator model in a simple sensory system. Science. 1977 Jun 3;196(4294):1055–1063. doi: 10.1126/science.870969. [DOI] [PubMed] [Google Scholar]
- 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]
- Macnab R. M. Bacterial flagella rotating in bundles: a study in helical geometry. Proc Natl Acad Sci U S A. 1977 Jan;74(1):221–225. doi: 10.1073/pnas.74.1.221. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- 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]
- 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]
- Macnab R., Koshland D. E., Jr Bacterial motility and chemotaxis: light-induced tumbling response and visualization of individual flagella. J Mol Biol. 1974 Apr 15;84(3):399–406. doi: 10.1016/0022-2836(74)90448-3. [DOI] [PubMed] [Google Scholar]
- 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]
- Shimada K., Kamiya R., Asakura S. Left-handed to right-handed helix conversion in Salmonella flagella. Nature. 1975 Mar 27;254(5498):332–334. doi: 10.1038/254332a0. [DOI] [PubMed] [Google Scholar]
- Silverman M., Simon M. I. Bacterial flagella. Annu Rev Microbiol. 1977;31:397–419. doi: 10.1146/annurev.mi.31.100177.002145. [DOI] [PubMed] [Google Scholar]
- 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]
- Spudich J. L., Koshland D. E., Jr Non-genetic individuality: chance in the single cell. Nature. 1976 Aug 5;262(5568):467–471. doi: 10.1038/262467a0. [DOI] [PubMed] [Google Scholar]
- 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]
- 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]
- Vary P. S., Stocker B. A. Nonsense motility mutants in Salmonella typhimurium. Genetics. 1973 Feb;73(2):229–245. doi: 10.1093/genetics/73.2.229. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Warrick H. M., Taylor B. L., Koshland D. E., Jr Chemotactic mechanism of Salmonella typhimurium: preliminary mapping and characterization of mutants. J Bacteriol. 1977 Apr;130(1):223–231. doi: 10.1128/jb.130.1.223-231.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]