This Article
Right arrow Full Text
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Feng, X.
Right arrow Articles by Hazelbauer, G. L.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Feng, X.
Right arrow Articles by Hazelbauer, G. L.

 Previous Article  |  Next Article 

Journal of Bacteriology, May 1999, p. 3164-3171, Vol. 181, No. 10
0021-9193/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.

Enhanced Function Conferred on Low-Abundance Chemoreceptor Trg by a Methyltransferase-Docking Site

Xiuhong Feng, Angela A. Lilly, and Gerald L. Hazelbauer*

Department of Biochemistry and Biophysics, Washington State University, Pullman, Washington 99164-4660

Received 28 September 1998/Accepted 12 March 1999

In Escherichia coli, high-abundance chemoreceptors are present in cellular amounts approximately 10-fold higher than those of low-abundance receptors. These two classes exhibit inherent differences in functional activity. As sole cellular chemoreceptors, high-abundance receptors are effective in methyl-accepting activity, in establishing a functional balance between the two directions of flagellar rotation, in timely adaptation, and in mediating efficient chemotaxis. Low-abundance receptors are not, even when their cellular content is increased. We found that the low-abundance receptor Trg acquired essential functional features of a high-abundance receptor by the addition of the final 19 residues of the high-abundance receptor Tsr. The carboxy terminus of this addition carried a methyltransferase-binding pentapeptide, NWETF, present in high-abundance receptors but absent in the low-abundance class. Provision of this docking site not only enhanced steady-state and adaptational methylation but also shifted the abnormal, counterclockwise bias of flagellar rotation toward a more normal rotational balance and vastly improved chemotaxis in spatial gradients. These improvements can be understood as the result of both enhanced kinase activation by the more methylated receptor and timely adaptation by more efficient methyl-accepting activity. We conclude that the crucial functional difference between the low-abundance receptor Trg and its high-abundance counterparts is the level of methyl-accepting activity conferred by the methyltransferase-docking site.

* Corresponding author. Mailing address: Department of Biochemistry and Biophysics, Washington State University, Pullman, WA 99164-4660. Phone: (509) 335-2174. Fax: (509) 335-9688. E-mail: hazelbau{at}membrane.chem.wsu.edu.

Journal of Bacteriology, May 1999, p. 3164-3171, Vol. 181, No. 10
0021-9193/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.


This article has been cited by other articles:

  • Liu, X., Parales, R. E. (2008). Chemotaxis of Escherichia coli to Pyrimidines: a New Role for the Signal Transducer Tap. J. Bacteriol. 190: 972-979 [Abstract] [Full Text]  
  • Meier, V. M., Muschler, P., Scharf, B. E. (2007). Functional Analysis of Nine Putative Chemoreceptor Proteins in Sinorhizobium meliloti. J. Bacteriol. 189: 1816-1826 [Abstract] [Full Text]  
  • Wang, Q., Mariconda, S., Suzuki, A., McClelland, M., Harshey, R. M. (2006). Uncovering a Large Set of Genes That Affect Surface Motility in Salmonella enterica Serovar Typhimurium. J. Bacteriol. 188: 7981-7984 [Abstract] [Full Text]  
  • Lai, W.-C., Hazelbauer, G. L. (2005). Carboxyl-Terminal Extensions beyond the Conserved Pentapeptide Reduce Rates of Chemoreceptor Adaptational Modification. J. Bacteriol. 187: 5115-5121 [Abstract] [Full Text]  
  • Antommattei, F. M., Munzner, J. B., Weis, R. M. (2004). Ligand-Specific Activation of Escherichia coli Chemoreceptor Transmethylation. J. Bacteriol. 186: 7556-7563 [Abstract] [Full Text]  
  • Li, M., Hazelbauer, G. L. (2004). Cellular Stoichiometry of the Components of the Chemotaxis Signaling Complex. J. Bacteriol. 186: 3687-3694 [Abstract] [Full Text]  
  • Bibikov, S. I., Miller, A. C., Gosink, K. K., Parkinson, J. S. (2004). Methylation-Independent Aerotaxis Mediated by the Escherichia coli Aer Protein. J. Bacteriol. 186: 3730-3737 [Abstract] [Full Text]  
  • Barnakov, A. N., Barnakova, L. A., Hazelbauer, G. L. (2002). Allosteric Enhancement of Adaptational Demethylation by a Carboxyl-terminal Sequence on Chemoreceptors. J. Biol. Chem. 277: 42151-42156 [Abstract] [Full Text]  
  • Shiomi, D., Zhulin, I. B., Homma, M., Kawagishi, I. (2002). Dual Recognition of the Bacterial Chemoreceptor by Chemotaxis-specific Domains of the CheR Methyltransferase. J. Biol. Chem. 277: 42325-42333 [Abstract] [Full Text]  
  • Shiomi, D., Homma, M., Kawagishi, I. (2002). Intragenic suppressors of a mutation in the aspartate chemoreceptor gene that abolishes binding of the receptor to methyltransferase. Microbiology 148: 3265-3275 [Abstract] [Full Text]  
  • Ames, P., Studdert, C. A., Reiser, R. H., Parkinson, J. S. (2002). From the Cover: Collaborative signaling by mixed chemoreceptor teams in Escherichia coli. Proc. Natl. Acad. Sci. USA 99: 7060-7065 [Abstract] [Full Text]  
  • Martin, A. C., Wadhams, G. H., Shah, D. S. H., Porter, S. L., Mantotta, J. C., Craig, T. J., Verdult, P. H., Jones, H., Armitage, J. P. (2001). CheR- and CheB-Dependent Chemosensory Adaptation System of Rhodobacter sphaeroides. J. Bacteriol. 183: 7135-7144 [Abstract] [Full Text]  
  • Beel, B. D., Hazelbauer, G. L. (2001). Substitutions in the Periplasmic Domain of Low-Abundance Chemoreceptor Trg That Induce or Reduce Transmembrane Signaling: Kinase Activation and Context Effects. J. Bacteriol. 183: 671-679 [Abstract] [Full Text]  
  • Lybarger, S. R., Maddock, J. R. (2000). Differences in the polar clustering of the high- and low-abundance chemoreceptors of Escherichia coli. Proc. Natl. Acad. Sci. USA 10.1073/pnas.130195397v1 [Abstract] [Full Text]  
  • Barnakov, A. N., Barnakova, L. A., Hazelbauer, G. L. (1999). Efficient adaptational demethylation of chemoreceptors requires the same enzyme-docking site as efficient methylation. Proc. Natl. Acad. Sci. USA 96: 10667-10672 [Abstract] [Full Text]  
  • Barnakov, A. N., Barnakova, L. A., Hazelbauer, G. L. (2001). Location of the Receptor-interaction Site on CheB, the Methylesterase Response Regulator of Bacterial Chemotaxis. J. Biol. Chem. 276: 32984-32989 [Abstract] [Full Text]  
  • Lybarger, S. R., Maddock, J. R. (2000). Differences in the polar clustering of the high- and low-abundance chemoreceptors of Escherichia coli. Proc. Natl. Acad. Sci. USA 97: 8057-8062 [Abstract] [Full Text]  


Copyright © 2009 by the American Society for Microbiology.   For an alternate route to Journals.ASM.org, visit: http://intl-journals.asm.org | More Info»