Cooperation of two distinct coupling proteins creates chemosensory network connections

Abstract

<p id="d6883848e167">Signal transduction systems are important pathways that organisms use to sense and respond to their environments. Chemotaxis is controlled by a signal transduction system that allows bacteria to coordinate their movement in response to their environment. This response requires proper assembly and localization of large multiprotein chemotaxis complexes, which are built by interactions between coupling proteins. The significance of having multiple types of coupling proteins in a single signal transduction system is poorly understood. Here, we show that multiple coupling proteins allow bacteria to build superprotein interaction networks and localize them to cell poles, a role that is required for optimal chemotaxis. </p><p class="first" id="d6883848e170">Although it is appreciated that bacterial chemotaxis systems rely on coupling, also called scaffold, proteins to both connect input receptors with output kinases and build interkinase connections that allow signal amplification, it is not yet clear why many systems use more than one coupling protein. We examined the distinct functions for multiple coupling proteins in the bacterial chemotaxis system of <i>Helicobacter pylori</i>, which requires two nonredundant coupling proteins for chemotaxis: CheW and CheV1, a hybrid of a CheW and a phosphorylatable receiver domain. We report that CheV1 and CheW have largely redundant abilities to interact with chemoreceptors and the CheA kinase, and both similarly activated CheA’s kinase activity. We discovered, however, that they are not redundant for formation of the higher order chemoreceptor arrays that are known to form via CheA–CheW interactions. In support of this possibility, we found that CheW and CheV1 interact with each other and with CheA independent of the chemoreceptors. Therefore, it seems that some microbes have modified array formation to require CheW and CheV1. Our data suggest that multiple coupling proteins may be used to provide flexibility in the chemoreceptor array formation. </p>