Stimulus response coupling in bacterial chemotaxis: receptor dimers in signalling arrays

Abstract

SummaryIn the Escherichia coli chemotaxis system, a family of chemoreceptors in the cytoplasmic membrane binds stimulatory ligands and regulates the activity of an associated histidine kinase CheA to modulate swimming behaviour and thereby cause a net migration towards attractants and away from repellents. The chemoreceptors themselves have been shown to be predominantly dimeric, but in the presence of the kinase CheA plus an adapter protein, CheW, much higher order structures have been observed. Recent results indicate that transmembrane signalling occurs within receptor clusters rather than through isolated dimers. We propose that the mechanism involves receptor arrays where binding of ligands at the outside surface of the membrane affects lateral packing interactions that cause perturbations in the organization of the signalling array at the opposing surface of the membrane. Results with receptor chimeras as well as findings with tyrosine kinase receptors suggest that this mechanism may represent a common theme in membrane receptor function. Bacterial chemotaxis and chemoreceptorsDuring the last 10 years the signal transduction system that mediates chemotaxis in Escherichia coli has become a paradigm for understanding basic mechanisms by which cellular regulatory networks effect adaptive responses to environmental signals (for recent reviews see Stock and Surette, 1996;Falke et al., 1997;Goudreau and Stock, 1998;Manson et al., 1998). E. coli cells monitor the chemical composition of their surroundings through a family of five different transmembrane chemoreceptors: Tar for aspartate, Tsr for serine, Trg for ribose and galactose, Tap for dipeptides, and Aer for O 2 and cellular redox potential (Fig. 1). In some cases, the chemoreceptors bind ligands directly (e.g. Tar binds aspartate, Tsr binds serine), whereas in other instances chemoreceptor interactions with smallmolecule ligands are mediated by soluble periplasmic binding proteins (e.g. Trg senses ribose and galactose through the binding proteins for these sugars).The chemoreceptors function within ternary complexes with a histidine protein kinase, CheA, and an adapter protein, CheW (Fig. 1). Repellent stimuli enhance the rate at which CheA autophosphorylates on a histidine residue. The phosphoryl group is then rapidly transferred to an aspartate residue in a soluble response regulator protein, CheY. In its phosphorylated form CheY binds to a flagella switch component, FliM, to induce a change in the direction a cell is swimming. Conversely, binding of an attractant inhibits CheA autophosphorylation, thus decreasing the level of phospho-CheY, so that a cell tends to continue moving towards attractants. Bacteria sense changes in repellent and attractant concentrations rather then their absolute levels. This ability depends on an adaptation mechanism that involves two additional enzymes: a methyltransferase, CheR, and an esterase/amidase, CheB. CheR and CheB catalyse the methylation and demethylation or deamidation of specific glutamate and glutamine residue...

Sensing of Cytoplasmic pH by Bacterial Chemoreceptors Involves the Linker Region That Connects the Membrane-spanning and the Signal-modulating Helices

“…Therefore, interactions within and/or among receptor-kinase complexes might also play critical roles in pH sensing, as has been suggested for receptor signaling and/or signal amplification (Ref. 9 and references therein).…”

Motility and Chemotaxis of Filamentous Cells of Escherichia coli

“…MCPs have been shown to be concentrated at the poles of normal-sized E. coli cells (22). It has been proposed that this localization is involved in the proper response of the bacteria to ligand during chemotaxis (4,18,20). Since cephalexin-induced filaments undergo chemotactic responses, we sought to determine the subcellular location of the chemoreceptors in such filaments.…”

Evolutionary Conservation of Methyl-Accepting Chemotaxis Protein Location in Bacteria and Archaea

“…The regulation of E. coli chemotaxis may be modulated by proximity of the MCPs (4,8,20). Here we report that the MCPs are polarly localized in a panel of bacteria that are evolutionarily similar (Vibrio sp.…”

“…In these species, the MCPs are concentrated primarily at the cell poles. The location of the MCPs may be involved in the regulation of E. coli chemotaxis (4,8,20), as MCP clustering has been implicated in regulating ligand binding and signaling in this bacterium (7,10,19,21,22,34). An understanding of MCP localization in a wide range of other bacteria and archaea could illuminate the relationship between MCP location and regulation of chemotaxis.…”