AAA+ ATPases contribute to nearly all cellular activities. Nature builds these machines as homomeric rings with catalytic sites residing between each protomer. A highly conserved catalytic core is modified with task-specific structural elements to generate a myriad of functions. Structural details about how these motors work are becoming available. Here we describe studies of NtrC1, a member of the NtrC subfamily of AAA+ ATPases that bacteria use to regulate gene expression from the σ54-form of RNA polymearase. In NtrC-like ATPases the specificity motifs are two loops called L1 and L2, with the latter containing a ‘GAFTGA’ motif for direct binding to σ54 of RNAP. Interaction of the ATPase with the polymerase remodels the sigma factor enabling it to melt promoter DNA so that transcription can begin. We show by SAS that while NtrC1 variant E239A is unable to hydrolyze ATP it undergoes nucleotide-driven conformational changes typical of the wild type protein and stably binds to σ54. An ATP-bound crystal structure revealed for the first time the γ-phosphate interacting with the catalytically crucial R-finger. Comparing the new structure with a prior ADP-bound suggests that R-finger engagement propagates a series of conformational changes on the R-finger side of the protomer/protomer interface, causing the L1-GAFTGA motif to extend several Angstroms above the plane of the ring to bind σ54. Neighbor/neighbor contacts between protomers, notably in a rigid body formed between the bulk of the L1- and L2-loops, suggest that nucleotide binding and subsequent conformational change will be complex, and likely cooperative. To test this hypothesis we took advantage of recent developments at the BioCAT beam line to perform static and time-resolved SAXS experiments to monitor conformational changes as nucleotide occupancy progresses from apo to fully bound state. The results reveal a series of changes with at least one intermediate state.