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Journal of Bacteriology, May 2004, p. 2664-2672, Vol. 186, No. 9
0021-9193/04/$08.00+0     DOI: 10.1128/JB.186.9.2664-2672.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.

Chemotactic Signaling by an Escherichia coli CheA Mutant That Lacks the Binding Domain for Phosphoacceptor Partners

Knut Jahreis,{dagger} Tom B. Morrison,{ddagger} Andrés Garzón,§ and John S. Parkinson1*

Biology Department, University of Utah, Salt Lake City, Utah 84112

Received 24 November 2003/ Accepted 23 January 2004

CheA is a multidomain histidine kinase for chemotaxis in Escherichia coli. CheA autophosphorylates through interaction of its N-terminal phosphorylation site domain (P1) with its central dimerization (P3) and ATP-binding (P4) domains. This activity is modulated through the C-terminal P5 domain, which couples CheA to chemoreceptor control. CheA phosphoryl groups are donated to two response regulators, CheB and CheY, to control swimming behavior. The phosphorylated forms of CheB and CheY turn over rapidly, enabling receptor signaling complexes to elicit fast behavioral responses by regulating the production and transmission of phosphoryl groups from CheA. To promote rapid phosphotransfer reactions, CheA contains a phosphoacceptor-binding domain (P2) that serves to increase CheB and CheY concentrations in the vicinity of the adjacent P1 phosphodonor domain. To determine whether the P2 domain is crucial to CheA's signaling specificity, we constructed CheA{Delta}P2 deletion mutants and examined their signaling properties in vitro and in vivo. We found that CheA{Delta}P2 autophosphorylated and responded to receptor control normally but had reduced rates of phosphotransfer to CheB and CheY. This defect lowered the frequency of tumbling episodes during swimming and impaired chemotactic ability. However, expression of additional P1 domains in the CheA{Delta}P2 mutant raised tumbling frequency, presumably by buffering the irreversible loss of CheA{Delta}P2-generated phosphoryl groups from CheB and CheY, and greatly improved its chemotactic ability. These findings suggest that P2 is not crucial for CheA signaling specificity and that the principal determinants that favor appropriate phosphoacceptor partners, or exclude inappropriate ones, most likely reside in the P1 domain.

* Corresponding author. Mailing address: Biology Department, University of Utah, Salt Lake City, UT 84112. Phone: (801) 581-7639. Fax: (801) 581-4668. E-mail: Parkinson{at}biology.utah.edu.

{dagger} Present address: Fachbereich Biologie/Chemie, Universität Osnabrück, Osnabrück 49069, Germany.

{ddagger} Present address: BioTrove, Inc., Woburn, MA 01801-1728.

§ Present address: Centro Andaluz de Biología del Desarrollo, Universidad Pablo de Olavide/CSIC, E-41013 Seville, Spain.

Journal of Bacteriology, May 2004, p. 2664-2672, Vol. 186, No. 9
0021-9193/04/$08.00+0     DOI: 10.1128/JB.186.9.2664-2672.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.



This article has been cited by other articles:

  • Zhao, J., Parkinson, J. S. (2006). Cysteine-Scanning Analysis of the Chemoreceptor-Coupling Domain of the Escherichia coli Chemotaxis Signaling Kinase CheA.. J. Bacteriol. 188: 4321-4330 [Abstract] [Full Text]  
  • Zhao, J., Parkinson, J. S. (2006). Mutational Analysis of the Chemoreceptor-Coupling Domain of the Escherichia coli Chemotaxis Signaling Kinase CheA. J. Bacteriol. 188: 3299-3307 [Abstract] [Full Text]  
  • Studdert, C. A., Parkinson, J. S. (2005). Insights into the organization and dynamics of bacterial chemoreceptor clusters through in vivo crosslinking studies. Proc. Natl. Acad. Sci. USA 102: 15623-15628 [Abstract] [Full Text]  
  • Porter, S. L., Armitage, J. P. (2004). Chemotaxis in Rhodobacter sphaeroides Requires an Atypical Histidine Protein Kinase. J. Biol. Chem. 279: 54573-54580 [Abstract] [Full Text]  


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