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Journal of Bacteriology, August 2005, p. 5115-5121, Vol. 187, No. 15
0021-9193/05/$08.00+0     doi:10.1128/JB.187.15.5115-5121.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.

Carboxyl-Terminal Extensions beyond the Conserved Pentapeptide Reduce Rates of Chemoreceptor Adaptational Modification

Wing-Cheung Lai and Gerald L. Hazelbauer*

Department of Biochemistry, 117 Schweitzer Hall, University of Missouri-Columbia, Columbia, Missouri 65211

Received 17 March 2005/ Accepted 25 April 2005

Sensory adaptation in bacterial chemotaxis is mediated by covalent modification of chemoreceptors. Specific glutamyl residues are methylated and demethylated in reactions catalyzed by methyltransferase CheR and methylesterase CheB. In the well-characterized chemosensory systems of Escherichia coli and Salmonella spp., efficient modification by either enzyme is dependent on a conserved pentapeptide sequence, NWETF or NWESF, present at the extreme carboxyl terminus of high-abundance chemoreceptors. To what extent is position at the extreme carboxyl terminus important for pentapeptide-mediated enhancement of adaptational modification? Is this position equally important for enhancement of both enzyme activities? To address these questions, we created forms of high-abundance receptor Tsr or Tar carrying one, six, or eight additional amino acids extending beyond the pentapeptide at their carboxyl termini and assayed methylation, demethylation, deamidation, and ability to mediate chemotaxis. In vitro and in vivo, all three carboxyl-terminal extensions reduced pentapeptide-mediated enhancement of rates of adaptational modification. CheB-catalyzed reactions were more affected than CheR-catalyzed reactions. Effects were less severe for the complete sensory system in vivo than for the minimal system of receptor and modification enzymes in vitro. Notably, extended receptors mediated chemotaxis as efficiently as wild-type receptors, providing a striking example of robustness in chemotactic systems. This could reflect compensatory reductions of rates for both modification reactions, mitigation of effects of slower reactions by the intertwined circuitry of signaling and adaptation, or tolerance of a range of reactions rates for adaptational modification. No matter what the mechanism, the observations provide a challenging test for mathematical models of chemotaxis.

* Corresponding author. Mailing address: Department of Biochemistry, 117 Schweitzer Hall, University of Missouri-Columbia, Columbia, Missouri 65211. Phone: (573) 882-4845. Fax: (573) 882-5635. E-mail: hazelbauerg{at}missouri.edu.

Journal of Bacteriology, August 2005, p. 5115-5121, Vol. 187, No. 15
0021-9193/05/$08.00+0     doi:10.1128/JB.187.15.5115-5121.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.



This article has been cited by other articles:

  • Dzinic, S. H., Shukla, M., Mandija, I., Ram, T. S., Ram, J. L. (2008). Variable length tandem repeat polyglutamine sequences in the flexible tether region of the Tsr chemotaxis receptor of Escherichia coli. Microbiology 154: 2380-2386 [Abstract] [Full Text]  
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  • Lai, W.-C., Barnakova, L. A., Barnakov, A. N., Hazelbauer, G. L. (2006). Similarities and differences in interactions of the activity-enhancing chemoreceptor pentapeptide with the two enzymes of adaptational modification.. J. Bacteriol. 188: 5646-5649 [Abstract] [Full Text]  
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