Cell-surface signaling (CSS) pathways are highly conserved systems in Gram-negative bacteria that allow the cell to efficiently respond to environmental stimuli through transcriptional regulation. Three distinct proteins are involved in this process: an outer membrane (OM) protein that senses the extracellular signal, an inner membrane (IM) sigma regulator protein that transmits the signal from the OM protein to the cytoplasm, and an extracytoplasmic function (ECF) sigma factor that initiates transcription of stimulus response genes. One such CSS pathway regulates bacterial iron acquisition- an essential process for bacterial survival and pathogenesis. Under iron-limited conditions, expression of the OM transporter is upregulated by signal transduction through the IM protein to the sigma factor. The goal of this work is to provide a structural rationale for distinctive signal transduction through the CSS pathway that regulates ferric siderophore uptake in Gram-negative bacteria, by structurally characterizing these proteins from Pseudomonas capeferrum, with a focus on the IM protein, PupR. The solution structures of an OM transporter, PupA, an OM transducer, PupB, a PupAPupB-NTSD chimera, and the OM proteins with the PupR C-terminal cell-surface signaling domain (CCSSD) were probed by SEC-SAXS to examine global architectural differences amongst the OM proteins. The X-ray crystal structure of the PupB N-terminal signaling domain (NTSD):PupR-CCSSD complex was determined. The PupB-NTSD exhibits a conserved βαβ-repeat motif. Unexpectedly, the CCSSD subdomain contains the same fold, which is the first time this fold had been identified at a protein’s C-terminus. The other subdomain of the CCSSD, designated the C-terminal juxtamembrane (CJM) subdomain, has a novel, β-solenoid-like motif. Analysis of the CCSSD by CD spectroscopy and SEC-SAXS indicated that the domain is highly flexible, and is significantly stabilized by the PupB-NTSD. Concurrently, the PupB-NTSD structure was determined by NMR, and contrasted with published NTSDs to evaluate structural variation that may account for disparities in functionality. The PupR N-terminal anti-sigma domain (ASD) was solved by X-ray crystallography and presents as a dimer in solution- the first description of a transmembrane ASD to assume an oligomeric form. Structural characterization of these proteins suggests novel implications for CSS through the TonB-dependent ferric siderophore uptake pathway.