Receptor interactions in a signalling system: competition between ribose receptor and galactose receptor in the chemotaxis response.

Abstract

Galactose and ribose receptors are shown to compete for a common site by comparing the specificities of the purified receptors with the specificity of the whole organism response. Ribose does not bind to the purified galactose receptor but inhibits the in vivo galactose response. A mutant lacking the ribose receptor shows no inhibition of the galactose response even at very high ribose concentrations. The results can. be explained by a mechanism involving (a) a ligand-induced conformational change in the receptor which produces a combining site with affinity for the molecule that serves as a first component of the signalling system and (b) a limited number of such first component molecules that cannot bind both receptors simultaneously. The mechanism may have considerable generality for sensory, hormonal, and transport systems.Receptors serve as the initiating point for responses to many stimuli, such as chemicals, light, sound and heat, and hormones. The initial stimulus is processed through a transmission system, usually complex and involving a number of proteins and chemical or electrical transmitters in order to give an overall biological response (1-3).In chemosensing systems the receptors are designed to bind a limited small number of molecules very tightly, thus insuring sensitivity to low concentrations of ligand. The tight binding of a few molecules is then transmitted and amplified to generate a final biological response. The nature of the interaction of the receptor molecule with the first molecule of the signalling system we shall call, for convenience, signal component I.Two broad categories for receptor-component I interaction are easily discerned. One involves a preassembled receptor-component I, either in one peptide chain or in a multiprotein complex. The second involves an association-dissociation mechanism in which the receptor and component I molecule associate only after receptor activation. Both categories may be further subdivided in terms of the nature of the assembly: a "parallel" pathway may be envisaged in which different receptor molecules interact with different component I molecules or a "focused" pathway in which different receptors compete for the same component I molecules. Suggestive findings in regard to receptor interactions in both of these categories have been accumulating in a variety of sensory, hormonal, and transport systems (4-11), but evidence with purified receptors is needed to resolve ambiguities. The receptor systems involved in bacterial chemotaxis offer some special advantages to provide such evidence since purified receptors with defined properties are available and genetic manipulation of the organism is relatively easy (12, 13).In the work reported here, receptor interactions have been examined by the isolation of two purified receptors and the comparison of the in vivo response of the entire organism with the in vitro properties of the purified receptor proteins. The galactose-ribose system of Salmonella typhimurium was selected for this study becaus...

Chemotaxis Towards Sugars by Bacillus subtilis

“…The signaller, defined by experiments on galactose and ribose chemotaxis in enteric bacteria, is a protein that monitors the number of binding proteins occupied by attractant. If competing-attractantreceptor complexes occupy most of the signallers, then the signallers will be less able to detect attractantreceptor complexes so that chemotaxis toward the attractant will be impaired (see, for example, Strange & Koshland, 1976). (iii) Each can be sensed by different receptors, but the competing attractant can also bind at the attractant's receptor as an antagonist.…”

“…(i) Both can be sensed by the same receptor (binding protein). (ii) Each can be sensed by different receptors (binding proteins), but both receptors can have a 'signaller' in common (Ordal & Adler, 1974;Strange & Koshland, 1976). The signaller, defined by experiments on galactose and ribose chemotaxis in enteric bacteria, is a protein that monitors the number of binding proteins occupied by attractant.…”

Mutations specifically affecting ligand interaction of the Trg chemosensory transducer

“…Trg generates sensory information about external concentrations of ribose and galactose by interacting with ligand-occupied ribose-and galactosebinding proteins, respectively (16,24). Competition experiments have shown that the presence of one sugar inhibits tactic response to the other sugar (2,10,39). A simple model for the competition is that the transducer has a single, common interaction site for both ligand-occupied binding proteins (39).…”

Receptor structure in the bacterial sensing system.

“…2 shows a schematic version of the receptor based on our current knowledge. The "floating receptor" mechanism appears to be well established for the interaction of the ribosebinding protein and the galactose-binding protein with the trg gene product (29,30). Competition studies show that the galactose-galactose-binding-protein complex and the riboseribose-binding-protein complex compete for a limited number of trg sites in the membrane (29).…”

“…The "floating receptor" mechanism appears to be well established for the interaction of the ribosebinding protein and the galactose-binding protein with the trg gene product (29,30). Competition studies show that the galactose-galactose-binding-protein complex and the riboseribose-binding-protein complex compete for a limited number of trg sites in the membrane (29). Mutations affecting the galactose-binding protein eliminate galactose-taxis (9); mutations affecting the ribose-binding protein eliminate ribose-taxis (7), and mutations affecting the trg protein eliminate both (31).…”