Bacterial chemoreceptors: high-performance signaling in networked arrays

Abstract

Chemoreceptors are crucial components in the bacterial sensory systems that mediate chemotaxis. Chemotactic responses exhibit exquisite sensitivity, extensive dynamic range and precise adaptation. The mechanisms that mediate these high-performance functions involve not only actions of individual proteins but also interactions among clusters of components, localized in extensive patches of thousands of molecules. Recently, these patches have been imaged in native cells, important features of chemoreceptor structure and on-off switching have been identified, and new insights have been gained into the structural basis and functional consequences of higher order interactions among sensory components. These new data suggest multiple levels of molecular interactions, each of which contribute specific functional features and together create a sophisticated signaling device. High-performance signaling in bacterial chemotaxisThe high-performance chemotaxis signaling system of Escherichia coli (Box 1) involves a limited number of components but notable sophistication [1][2][3][4]. This system has become a paradigm for molecular characterization of biological signaling mechanisms. Transmembrane chemoreceptors, known as methyl-accepting chemotaxis proteins (MCPs), direct cell locomotion by regulating the histidine kinase CheA; CheA phosphorylates a response regulator, which in turn controls the rotational direction of the flagellar motor. Chemotactic sensitivity and the range of signal detection are regulated by adaptational modification of chemoreceptors via reversible glutamyl methylation. The resulting interplay between motor control and sensory adaptation produces directed motile behavior. E. coli chemoreceptors are the most extensively studied representatives of the MCP super-family, central components of homologous systems that mediate tactic responses [5,6] across the phylogenetic diversity of bacteria and archaea [7].In E. coli chemotaxis proteins cluster in membrane-associated patches [8]. Interaction within patches is thought to contribute to notable features of the signaling system: high sensitivity, wide dynamic range, extensive cooperativity and precise adaptation. Delineating the molecular mechanisms underlying these features will require knowledge of structures of the components, complexes and higher order arrays. In addition it will require definition of organization at the multiple levels of interaction among signaling components and an understanding of the changes in components and their interactions that mediate signaling at each level. In the past few years, notable progress has been made toward acquiring the NIH Public Access NIH-PA Author ManuscriptNIH-PA Author Manuscript NIH-PA Author Manuscript information and insights necessary for understanding these molecular mechanisms. This review describes that progress. Here we follow the lead of most investigators in the area, and do not distinguish between studies of first cousins E. coli and Salmonella enterica serovar Typhimurium. Thus, referenc...

Campylobacter jejuni proteins Cj0952c and Cj0951c affect chemotactic behaviour towards formic acid and are important for invasion of host cells

“…In this way, the HAMP domain serves as a linker region that is suggested to be conserved in histidine kinases, adenylyl cyclases, methylaccepting chemotaxis proteins and phosphatases, and converts ligand-induced conformational changes into kinase-controlling signals (Aravind & Ponting, 1999;Butler & Falke, 1998;Le Moual & Koshland, 1996;Williams & Stewart, 1999). Cj0951c shows strong homologies to the cytoplasmic signalling domains of MCPs, being composed of an adaptation region with methylation sites, a flexible region with a conserved glycine hinge, and a protein-interaction region for binding of the chemotaxis protein CheW and the kinase CheA (Hazelbauer et al, 2008).…”

“…CheW interacts with the histidine kinase CheA, mediating the signal from the receptor, while CheY represents a chemotaxis regulator that interacts with the flagellar motor in a phosphorylated form. Furthermore, the proteins CheR and CheB serve as methyltransferase and methylesterase, respectively, for reversible chemoreceptor methylation (Hazelbauer et al, 2008). Finally, the presence of two aerotaxis genes and 10 putative chemoreceptor genes, designated Tlps for transducer-like proteins, has been revealed.…”

Sensor–response regulator interactions in a cross-regulated signal transduction network

“…It is possible that they form heterologous clusters, as shown for the paralogous CitA and DcuS sensors (Scheu et al, 2008). Heteromeric chemoreceptor clusters have documented roles in signalling (Hazelbauer et al, 2008). However, the physiological function for heteromeric sensor clusters remains obscure (Scheu et al, 2012).…”

Active State of Sensory Rhodopsin II: Structural Determinants for Signal Transfer and Proton Pumping

“…This activation occurs at the level of the membrane. How this signal is then transmitted to signal domain thereby modulating the activity of the histidine kinase CheA and triggering the cytoplasmic two component signaling cascade is not known yet 2,5,9,10 .…”