Bacterial transcription initiation requires RNA polymerase to unwind promoter DNA, a step that is often inefficient and sometimes aided by activator proteins. Most activators stimulate transcription by contacting both RNA polymerase and the promoter. Here, we report an alternative mechanism employed by the multiple antibiotic resistance activator MarA in Escherichia coli. We show that when bound upstream of the flgBCDEFGHIJ/KL operon, MarA locally perturbs DNA base pairing near its binding site, facilitating promoter melting by Sigma28-dependent RNA polymerase. Supporting this model, introducing a base pair mismatch at the appropriate position mimics the effect of MarA and eliminates the need for the regulator. Our findings suggest that in this case DNA structural changes alone can be sufficient to activate transcription, and this mechanism may be widespread, particularly for promoters recognised by alternative sigma factors. These results reveal a new strategy of transcription initiation by activator proteins and expand our understanding of bacterial gene control.