Divergent transcription of a regulatory gene and a cognate promoter under its control is a common theme in bacterial regulatory circuits. This genetic organization is found for the dmpR gene that encodes the substrate-responsive specific regulator of the σ54-dependent Po promoter, which controls (methyl)phenol catabolism. Here we identify the Pr promoter of dmpR as a σ70-dependent promoter that is regulated by a novel mechanism in which σ54-RNA polymerase occupancy of the non-overlapping σ54-Po promoter stimulates σ70-Pr output. In addition, we show that DmpR stimulates its own production through Po activity both in vivo and in vitro. Hence, the demonstrated regulatory circuit reveals a novel role for σ54-RNA polymerase, namely regulation of a σ70-dependent promoter, and a new mechanism that places a single promoter under dual control of two alternative forms of RNA polymerase. We present a model in which guanosine tetra-phosphate plays a major role in the interplay between σ54- and σ70-dependent transcription to ensure metabolic integration to couple σ70-Pr output to both low-energy conditions and the presence of substrate.