TonB-dependent uptake systems of Gram-negative bacterial pathogens constitute prominent virulence factors, allowing nutrients - primarily siderophore-bound iron - to cross the highly impermeable outer membrane (OM). Remarkably, the ferredoxin uptake system (Fus) of Pectobacteriaceae, a group of soft rot-inducing plant pathogens, imports an entire folded host protein, ferredoxin, into the periplasm and extracts its bound iron. The inner membrane protein FusB, a TonB homologue, plays two roles in the process. First, it remodels the globular plug domain obstructing the lumen of the OM receptor FusA to allow ferredoxin passage. Unusually for a TonB protein, FusB then interacts directly with the substrate emerging in the periplasm to finalise its import. Here we elucidate at the molecular level three partially overlapping FusB interfaces - involved in receptor and ferredoxin binding as well as homodimerisation. We postulate that under resting conditions FusB exists as a homodimer, stabilised by an intermolecular Arg241-D322 salt bridge. The homodimer dissociates when the N-terminal “FusB-box” region of the receptor emerges and outcompetes one protomer, with FusB R241 switching to D53 of the receptor. In agreement with the proposed sequence of events, ferredoxin binding displaces the receptor from FusB, whereas FusB undergoes a structural rearrangement, expanding its β-sheet from three to four strands. The newly formed C-terminal hairpin, comprising the majority of ferredoxin binding interface, is stabilised by a Arg241-D322 salt bridge – this time in cis. In addition to R241 we identify several critical residues involved in FusB-ferredoxin and FusB-receptor interactions and propose a mechanistic model for ferredoxin import in which Arg241 acts as a molecular switch. The results expand our understanding of structural and functional complexity of TonB proteins and provide insight into a system that can be exploited for antimicrobial delivery and biotechnological applications.