The network controlling the general stress response in Bacillus subtilis requires both the RsbP phosphatase and the RsbQ alpha/beta 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 of rsbP yielded 17 independent bypass suppressors that had activity in an rsbQ null strain background. The altered residues clustered in three regions of RsbP: the coiled-coil and two predicted helices of the phosphatase domain. One helix (alpha0) is unique to a subfamily of bacterial PP2C phosphatases that possess N-terminal sensing domains. The other (alpha1) 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 alpha0-alpha1 helices, with RsbQ hydrolase activity and the PAS domain jointly comprising a positive sensing module that counters the coiled-coil. We propose that the alpha0 helix characterizes an extended PP2C domain in many bacterial signalling proteins, and suggest it provides a means to communicate information from diverse input domains.