The role of heterologous receptors in McpB-mediated signalling in Bacillus subtilis chemotaxis.
Asparagine chemotaxis in Bacillus subtilis appears to involve two partially redundant adaptation mechanisms: a receptor methylation-independent process that operates at low attractant concentrations and a receptor methylation-dependent process that is required for optimal responses to high concentrations. In order to elucidate these processes, chemotactic responses were assessed for strains expressing methylation-defective mutations in the asparagine receptor, McpB, in which all 10 putative receptors (10del), five receptors (5del) or only the native copy of mcpB were deleted. This was done in both the presence and the absence of the methylesterase CheB. We found that: (i) only responses to high concentrations of asparagine were impaired; (ii) the presence of all heterologous receptors fully compensated for this defect, whereas responses progressively worsened as more receptors were taken away; (iii) methyl-group turnover occurred on heterologous receptors after the addition of asparagine, and these methylation changes were required for the restoration of normal swimming behaviour; (iv) in the absence of the methyleste-rase, the presence of heterologous receptors in some cases caused impaired chemotaxis; and (v) either a certain threshold number of receptors must be present to promote basal CheA activity, or one or more of the receptors missing in the 10del background (but present in the 5del background) is required for establishing basal CheA activity. Taken together, these findings suggest that many or all chemoreceptors work as an ensemble that constitutes a robust chemotaxis system. We propose that the ability of non-McpB receptors to compensate for the methylation-defective McpB mutations involves lateral transmission of the adapted conformational change across the ensemble.
Zimmer
Michael A
MA
Department of Biochemistry, Colleges of Medicine and Liberal Arts and Sciences, University of Illinois, Urbana, IL 61801, USA.
Szurmant
Hendrik
H
Saulmon
Michael M
MM
Collins
Marissa A
MA
Bant
Jason S
JS
Ordal
George W
GW
D000222:Adaptation, Physiological / Q000235:genetics; D019943:Amino Acid Substitution; D001216:Asparagine / Q000494:pharmacology; D001412:Bacillus subtilis / Q000235:genetics / Q000502:physiology*; D001426:Bacterial Proteins / Q000235:genetics / Q000502:physiology*; D002265:Carboxylic Ester Hydrolases / Q000502:physiology; D002628:Chemoreceptor Cells / Q000502:physiology*; D002633:Chemotaxis / Q000235:genetics / Q000502:physiology*; D017353:Gene Deletion; D005816:Genetic Complementation Test; D046911:Macromolecular Substances; D008565:Membrane Proteins / Q000235:genetics / Q000502:physiology; D000432:Methanol / Q000378:metabolism; D000072236:Methyl-Accepting Chemotaxis Proteins; D008745:Methylation; D016297:Mutagenesis, Site-Directed; D011487:Protein Conformation; D011499:Protein Processing, Post-Translational; D020239:Receptor Cross-Talk; D015534:Trans-Activators
D001426:Bacterial Proteins; D046911:Macromolecular Substances; D008565:Membrane Proteins; D000072236:Methyl-Accepting Chemotaxis Proteins; D015534:Trans-Activators; C089891:tipA protein, Streptomyces; D001216:Asparagine; D002265:Carboxylic Ester Hydrolases; C041144:chemotactic protein methylesterase; D000432:Methanol