Rapid evolution of a bacterial iron acquisition system

• Published in: Molecular microbiology Vol. 108; no. 1; pp. 90 - 100
• Main Authors: Chatterjee, Anushila, O'Brian, Mark R.
• Format: Journal Article
• Language: English
• Published: England Blackwell Publishing Ltd 01-04-2018
• Subjects: Adaptation, Biological - genetics; Adaptation, Biological - physiology; Bacteria; Bacterial Proteins - genetics; Bacterial Proteins - metabolism; Bradyrhizobium - genetics; Bradyrhizobium - metabolism; Cation Transport Proteins - genetics; Cation Transport Proteins - metabolism; Cell Membrane - metabolism; Chelates; Chelating agents; Cytoplasm - metabolism; Ferric Compounds - metabolism; Ferrous Compounds - metabolism; Gain of Function Mutation; Genes; Gram-negative bacteria; Iron; Iron - metabolism; Membrane proteins; Membrane Transport Proteins - genetics; Membrane Transport Proteins - metabolism; Missense mutation; Mutation; Mutation, Missense; Nutritional requirements; Periplasm; Periplasm - metabolism; Siderophores; Siderophores - genetics; Siderophores - metabolism; Stress, Physiological
• ISSN: 0950-382X; 1365-2958
• DOI: 10.1111/mmi.13918

Summary
Under iron limitation, bacteria scavenge ferric (Fe3+) iron bound to siderophores or other chelates from the environment to fulfill their nutritional requirement. In gram‐negative bacteria, the siderophore uptake system prototype consists of an outer membrane transporter, a periplasmic binding protein and a cytoplasmic membrane transporter, each specific for a single ferric siderophore or siderophore family. Here, we show that spontaneous single gain‐of‐function missense mutations in outer membrane transporter genes of Bradyrhizobium japonicum were sufficient to confer on cells the ability to use synthetic or natural iron siderophores, suggesting that selectivity is limited primarily to the outer membrane and can be readily modified. Moreover, growth on natural or synthetic chelators required the cytoplasmic membrane ferrous (Fe2+) iron transporter FeoB, suggesting that iron is both dissociated from the chelate and reduced to the ferrous form within the periplasm prior to cytoplasmic entry. The data suggest rapid adaptation to environmental iron by facile mutation of selective outer membrane transporter genes and by non‐selective uptake components that do not require mutation to accommodate new iron sources.
Unlike E. coli, selectivity for uptake of nutritional iron chelates is limited to the outer membrane in Bradyrhizobium japonicum. Gain‐of‐function mutations in genes encoding outer membrane transporters are sufficient to allow B. japonicum to readily adapt to new iron sources in the environment.