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In addition to the yersiniabactin (Ybt) siderophore-dependent system, two inorganic iron ABC transport systems ofYersinia pestis , Yfe and Yfu, have been characterized. Here we show that the Yfu system functions inY. pestis : a Ybt− Yfe− Yfu− mutant exhibited a greater growth defect under iron-deficient conditions than its Ybt− Yfe− parental strain. We also demonstrate that another putativeY. pestis iron uptake system, Yiu, which potentially encodes an outer membrane receptor, YiuR, and an ABC iron transport cassette, YiuABC, is functional. The clonedyiuABC operon restored growth of an enterobactin-deficient mutantEscherichia coli strain, 1017, under iron-chelated conditions. Iron uptake by the Yiu system inY. pestis was demonstrated only when the Ybt, Yfe, and Yfu systems were mutated. Using ayiuA ::lacZ fusion, we show that theyiuABC promoter is repressed by iron through Fur. A mouse model of bubonic plague failed to show a significant role for the Yiu system in the disease process. These results demonstrate that two additional iron transporters are functional inY. pestis and indicate that there is a hierarchy of iron transporters, with Ybt being most effective and Yiu being the least effective of those systems which have been characterized.

Hierarchy of Iron Uptake Systems: Yfu and Yiu Are Functional in Yersinia pestis