Transmembrane chemoreceptors, also known as methyl-accepting chemotaxis proteins (MCPs), translate extracellular signals into intracellular responses in the bacterial chemotaxis system. MCPs control the activity of the kinase, CheA, via a coupling protein, CheW. The chemoreceptor, CheA and CheW form a ternary complex that is the central signaling unit in bacterial chemotaxis. Although the individual structures of the components of the ternary complex are known, the precise molecular associations of these proteins has yet to be identified. Here we present a soluble stable ternary complex from Thermotoga maritima that can be used to probe the molecular interactions between MCP, CheA and CheW. The stoichiometry of this soluble complex was determined to be one MCP dimer: one CheA dimer: two CheW dimers. In this complex the autophosphorylating activity of CheA was significantly inhibited by the soluble MCP, Tm14. The cytoplasmic portion of a T. maritima transmembrane MCP (Tm1143) also inhibited the activity of CheA to varying degrees depending on specific mutations that mimic conditions inside the cell. These results confirm the functional relevance of this ternary complex that will be further rationalized in terms of the structure of the complex. Although an X-ray crystal structure of the ternary complex could not be obtained, the structure of Tm14 was determined. Tm14 is distinct from previous MCP structures in that Tm14 naturally lacks a transmembrane region. The 2.15 Å resolution crystal structure of a T. maritima soluble receptor (Tm14) reveals distortions in its dimeric four-helix bundle that provide insight into the conformational states available to MCPs for propagating signals. A bulge in one helix generates asymmetry between subunits that displaces the kinase-interacting tip by >25 Å relative to a symmetric model. The maximum bundle distortion maps to the adaptation region of transmembrane MCP’s where reversible methylation of acidic residues tunes receptor activity. Minor alterations in coiled-coil packing geometry translates to major structural changes downstream. The Tm14 structure discloses how alterations in local helical structure, which could be induced by changes in methylation state and/or by conformational signals from membrane proximal regions, can reposition a remote domain that interacts with the CheA kinase.