Networked Chemoreceptors Benefit Bacterial Chemotaxis Performance

ABSTRACT Motile bacteria use large receptor arrays to detect and follow chemical gradients in their environment. Extended receptor arrays, composed of networked signaling complexes, promote cooperative stimulus control of their associated signaling kinases. Here, we used structural lesions at the communication interface between core complexes to create an Escherichia coli strain with functional but dispersed signaling complexes. This strain allowed us to directly study how networking of signaling complexes affects chemotactic signaling and gradient-tracking performance. We demonstrate that networking of receptor complexes provides bacterial cells with about 10-fold-heightened detection sensitivity to attractants while maintaining a wide dynamic range over which receptor adaptational modifications can tune response sensitivity. These advantages proved especially critical for chemotaxis toward an attractant source under conditions in which bacteria are unable to alter the attractant gradient. IMPORTANCE Chemoreceptor arrays are found in many motile bacteria. However, although our understanding of bacterial chemotaxis is quite detailed, the signaling and behavioral advantages of networked receptor arrays had not been directly studied in cells. We have recently shown that lesions in a key interface of the E. coli receptor array diminish physical connections and functional coupling between core signaling complexes while maintaining their basic signaling capacity. In this study, we exploited an interface 2 mutant to show, for the first time, that coupling between core complexes substantially enhances stimulus detection and chemotaxis performance. Chemoreceptor arrays are found in many motile bacteria. However, although our understanding of bacterial chemotaxis is quite detailed, the signaling and behavioral advantages of networked receptor arrays had not been directly studied in cells. We have recently shown that lesions in a key interface of the E. coli receptor array diminish physical connections and functional coupling between core signaling complexes while maintaining their basic signaling capacity. In this study, we exploited an interface 2 mutant to show, for the first time, that coupling between core complexes substantially enhances stimulus detection and chemotaxis performance.