A possible degree of motional freedom in bacterial chemoreceptor cytoplasmic domains and its potential role in signal transduction.

We describe an array of gaps in an antiparallel four-helix bundle structure, the cytoplasmic domains of bacterial chemoreceptors. For a given helix, the side chain interactions that define a helix's position are analyzed in terms of residue interfaces, the most important of which are a-a, g-g, d-d, g-d, and a-d. It was found that the interdigitation of the side groups does not entirely fill the space along the long axis of the structure, which results in a rather regular array of gaps. A simulated piston motion of helix CD1 along the helical axis direction by 1.2Å shows that 85% of the side chain interactions still satisfy Van der Waals criteria, while the remaining clashes could be avoided by small rotations of side chains. Therefore, two states could exist in the structure, related by a piston motion. Analysis of the crystal structure of a small four-helix bundle, the P1(short) domain of CheA in Thermotoga Maritima, reveals that the two coexisting states related by a 1.3-1.7Å piston motion are defined by the same mechanism. This two-state model is a plausible candidate mechanism for the long distance signal transduction in bacterial chemoreceptors and is qualitatively consistent with literature chemoreceptor mutagenesis results. Such a mechanism could exist in many other structures with interdigitating α-helices.