Identification of the ribose binding protein as the receptor for ribose chemotaxis in Salmonella typhimurium

Aksamit, Robert R.; Koshland, D E

doi:10.1021/bi00719a001

Cited by 107 publications

(65 citation statements)

References 22 publications

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“…Yet this result is not simply explained because (as shown in Table 1) ribose cannot bind to the purified galactose receptor. Previous studies had shown a good correlation between the specificity of binding to the purified receptor and the specificity of response of the intact organism (14,16 (Fig. 4).…”

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confidence: 60%

“…The purities of sugars were checked where necessary by chromatography on silica gel in isopropanol:ethyl acetate:water, 7:2:1 (vol/vol), visualizing with aniline phthalate, or on cellulose in n-butanol:ethanol:water, 25:16:9 (vol/vol), visualizing with alkaline silver nitrate. Strains ST1, ST48, and ST29 are derived from Salmonella typhimurium LT2 as described (14).The capillary assay was performed essentially as described by Adler (17) except that a capillary tube (Microcaps-Drummond Scientific) containing attractant was placed in the commercially supplied holder containing the bacterial suspension. Bacteria were grown to midlogarithmic phase at 300 and were centrifuged (5000 rpm, 15 min); the pellet was resuspended gently in Vogel-Bonner citrate buffer (18) at 8 X 108 cells per ml.…”

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confidence: 99%

“…The galactose-ribose system of Salmonella typhimurium was selected for this study because Ordal and Adler had reported a single mutant that removed both properties in the closely related Escherichia coli (9) and work in our laboratory had delineated properties of the purified ribose receptor (14)(15)(16) and receptor mutants (14) which would be particularly helpful.…”

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

Strange¹,

Koshland²

1976

Proc. Natl. Acad. Sci. U.S.A.

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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...

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

Strange¹,

Koshland²

1976

Proc. Natl. Acad. Sci. U.S.A.

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“…Firstly, amino acid taxis is much stronger (Mesibov et al, 1973); for instance, it is hard to see smooth swimming by B. subtilis following addition of sugar but easy following addition of amino acid. Secondly, amino acid chemoreceptors do not have a transport function (Ordal et al, 1978) but sugar receptors do (Adler & Epstein, 1974;Aksamit & Koshland, 1974;Hazelbauer, 1975;Hazelbauer & Adler, 1971 As a prelude to biochemical studies of the function of sugar chemoreceptors, we have sought to determine the sugar attractants and discover specificities of chemoreceptors for B. subtilis. Similar experiments have already been done for E. coli .…”

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Chemotaxis Towards Sugars by Bacillus subtilis

Ordal

Villani

Rosendahl

1979

Journal of General Microbiology

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Many sugars and derivatives were tested in the capillary assay for their attraction of Bacillus subtilis. The major attractants were 2-deoxy-~-ghcose, D-fructose, gentiobiose, D-glucose, maltose, D-mannitol, D-mannose, N-acetylglucosamine, a-methyl-D-glucoside, P-methyl-Dglucoside, N-acetylmannosamine, a-methyl-D-mannoside, D-sorbitol, L-sorbose, sucrose, trehalose and D-XylOSe. Only glucose chemotaxis was completely constitutive. Competition experiments were carried out to determine the specificities of chemoreceptors. There were 25 instances of no influence of two sugars on each other's taxis, 92 instances of one sugar interfering non-reciprocally with chemotaxis towards another and 49 instances of two sugars reciprocally competing. However, in most of the last instances, other sugars were identified that interfered with chemotaxis towards one member of the pair but not the other. Thus, nearly all sugars and related compounds appear to be detected by their own chemoreceptors, but many secondary interactions exist.

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A signal sequence mutant defective in export of ribose-binding protein and a corresponding pseudorevertant isolated without imposed selection.

Iida¹,

Groarke²,

Park³

et al. 1985

The EMBO Journal

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Ribose‐binding protein is exported to the periplasmic compartment of Escherichia coli by a process that involves proteolytic cleavage of an amino‐terminal extension of amino acids from the precursor form of the protein. In a collection of mutants isolated as defective in the Rbs transport system, a strain was identified that contained only precursor ribose‐binding protein, none of which was exported to its normal location in the periplasm. The mutated rbsB contained a base substitution that results in a change of leucine to a proline at position‐17 in the signal sequence. A pseudorevertant of the mutant contained proteolytically processed, active ribose‐binding protein in the periplasm. The pseudorevertant rbsB carried a second mutation: serine at position‐15 in the signal sequence was changed to phenylalanine. Isolation of a signal sequence mutant and a corresponding pseudorevertant without specific selection or site‐directed mutagenesis emphasizes the possibility of obtaining export mutants without the use of procedures that could bias or limit the range of mutations found. Explanation of the extreme phenotype of the mutant and the effective correction of that phenotype in the pseudorevertant requires extension of current notions of critical features of signal sequences.

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Identification of the ribose binding protein as the receptor for ribose chemotaxis in Salmonella typhimurium

Abstract: The ribose binding protein of Salmonella typhimurium has been shown to be the receptor for ribose

Cited by 107 publications

References 22 publications

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

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

Chemotaxis Towards Sugars by Bacillus subtilis

A signal sequence mutant defective in export of ribose-binding protein and a corresponding pseudorevertant isolated without imposed selection.

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