Bacterial receiver domains modulate intracellular responses to external stimuli in two-component systems. Sma0114 is the first structurally characterized representative from the family of receiver domains that are substrates for histidine-tryptophan-glutamate (HWE) kinases. We report the NMR structure of Sma0114 bound by Ca(2+) and BeF3(-), a phosphate analogue that stabilizes the activated state. Differences between the NMR structures of the inactive and activated states occur in helix α1, the active site loop that connects strand β3 and helix α3, and in the segment from strand β5 to helix α5 of the 455 (α4-β5-α5) face. Structural rearrangements of the 455 face typically make receiver domains competent for binding downstream target molecules. In Sma0114 the structural changes accompanying activation result in a more negatively charged surface for the 455 face. Coupling between the 455 face and active site phosphorylation is usually mediated through the rearrangement of a threonine and tyrosine residue, in a mechanism called Y-T coupling. The NMR structure indicates that Sma0114 lacks Y-T coupling and that communication between the active site and the 455 face is achieved through a conserved lysine residue that stabilizes the acyl phosphate in receiver domains. (15)N-NMR relaxation experiments were used to investigate the backbone dynamics of the Sma0114 apoprotein, the binary Sma0114·Ca(2+) complex, and the ternary Sma0114·Ca(2+)·BeF3(-) complex. The loss of entropy due to ligand binding at the active site is compensated by increased flexibility in the 455 face. The dynamic character of the 455 face in Sma0114, which results in part from the replacement of helix α4 by a flexible loop, may facilitate induced-fit recognition of target molecules.