The network controlling the general stress response inBacillus subtilisrequires both the RsbP phosphatase and the RsbQ α/β hydrolase to convey signals of energy stress. RsbP contains three domains: an N-terminal PAS, a central coiled-coil and a C-terminal PP2C phosphatase. We report here a genetic analysis that established the functional interactions of the domains and their relationship to RsbQ. Random mutagenesis ofrsbPyielded 17 independent bypass suppressors that had activity in anrsbQnull strain background. The altered residues clustered in three regions of RsbP: the coiled-coil and two predicted helices of the phosphatase domain. One helix (α0) is unique to a subfamily of bacterial PP2C phosphatases that possess N-terminal sensing domains. The other (α1) is distinct from the active site in all solved PP2C structures. The phenotypes of the suppressors and directed deletions support a model in which the coiled-coil negatively controls phosphatase activity, perhaps via the α0-α1 helices, with RsbQ hydrolase activity and the PAS domain jointly comprising a positive sensing module that counters the coiled-coil. We propose that the α0 helix characterizes an extended PP2C domain in many bacterial signalling proteins, and suggest it provides a means to communicate information from diverse input domains.