• We are sorry, but NCBI web applications do not support your browser and may not function properly. More information
Logo of pnasPNASInfo for AuthorsSubscriptionsAboutThis Article
Proc Natl Acad Sci U S A. Sep 1978; 75(9): 4150–4154.
PMCID: PMC336069

Inversion of a behavioral response in bacterial chemotaxis: Explanation at the molecular level

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.

Full text

Full text is available as a scanned copy of the original print version. Get a printable copy (PDF file) of the complete article (1.5M), or click on a page image below to browse page by page. Links to PubMed are also available for Selected References.

Images in this article

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Adler J. Chemotaxis in bacteria. Annu Rev Biochem. 1975;44:341–356. [PubMed]
  • Koshland DE., Jr A response regulator model in a simple sensory system. Science. 1977 Jun 3;196(4294):1055–1063. [PubMed]
  • Silverman M, Simon MI. Bacterial flagella. Annu Rev Microbiol. 1977;31:397–419. [PubMed]
  • Rubik BA, Koshland DE., 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. [PMC free article] [PubMed]
  • Berg HC, Brown DA. Chemotaxis in Escherichia coli analysed by three-dimensional tracking. Nature. 1972 Oct 27;239(5374):500–504. [PubMed]
  • Macnab RM, Koshland DE., Jr The gradient-sensing mechanism in bacterial chemotaxis. Proc Natl Acad Sci U S A. 1972 Sep;69(9):2509–2512. [PMC free article] [PubMed]
  • Tsang N, Macnab R, Koshland DE., Jr Common mechanism for repellents and attractants in bacterial chemotaxis. Science. 1973 Jul 6;181(4094):60–63. [PubMed]
  • Larsen SH, Reader RW, Kort EN, Tso WW, 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. [PubMed]
  • Macnab RM, Ornston MK. 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. [PubMed]
  • Warrick HM, Taylor BL, Koshland DE., Jr Chemotactic mechanism of Salmonella typhimurium: preliminary mapping and characterization of mutants. J Bacteriol. 1977 Apr;130(1):223–231. [PMC free article] [PubMed]
  • 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. [PubMed]
  • Aswad D, Koshland DE., Jr Isolation, characterization and complementation of Salmonella typhimurium chemotaxis mutants. J Mol Biol. 1975 Sep 15;97(2):225–235. [PubMed]
  • Vary PS, Stocker BA. Nonsense motility mutants in Salmonella typhimurium. Genetics. 1973 Feb;73(2):229–245. [PMC free article] [PubMed]
  • VOGEL HJ, BONNER DM. Acetylornithinase of Escherichia coli: partial purification and some properties. J Biol Chem. 1956 Jan;218(1):97–106. [PubMed]
  • Macnab RM. Examination of bacterial flagellation by dark-field microscopy. J Clin Microbiol. 1976 Sep;4(3):258–265. [PMC free article] [PubMed]
  • Silverman M, Simon M. Flagellar rotation and the mechanism of bacterial motility. Nature. 1974 May 3;249(452):73–74. [PubMed]
  • Spudich JL, Koshland DE., Jr Non-genetic individuality: chance in the single cell. Nature. 1976 Aug 5;262(5568):467–471. [PubMed]
  • Macnab R, Koshland DE., Jr Bacterial motility and chemotaxis: light-induced tumbling response and visualization of individual flagella. J Mol Biol. 1974 Apr 15;84(3):399–406. [PubMed]
  • Hotani H. Light microscope study of mixed helices in reconstituted Salmonella flagella. J Mol Biol. 1976 Sep 5;106(1):151–166. [PubMed]
  • Shimada K, Kamiya R, Asakura S. Left-handed to right-handed helix conversion in Salmonella flagella. Nature. 1975 Mar 27;254(5498):332–334. [PubMed]
  • Kamiya R, Asakura S. Helical transformations of Salmonella flagella in vitro. J Mol Biol. 1976 Sep 5;106(1):167–186. [PubMed]
  • KERRIDGE D. The effect of amino acid analogues on the synthesis of bacterial flagella. Biochim Biophys Acta. 1959 Feb;31(2):579–581. [PubMed]
  • Macnab RM. Bacterial flagella rotating in bundles: a study in helical geometry. Proc Natl Acad Sci U S A. 1977 Jan;74(1):221–225. [PMC free article] [PubMed]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

Formats:

Related citations in PubMed

See reviews...See all...

Cited by other articles in PMC

See all...

Links

Recent Activity

Your browsing activity is empty.

Activity recording is turned off.

Turn recording back on

See more...