Benefits of siderophore release lie in mediating diffusion limitation at low iron solubility

Abstract

Siderophores are chelators released by many bacteria to take up iron. In contrast to iron receptors located at the cell surface, released siderophores are at risk of being lost to environmental sinks. Here, we asked the question whether the release itself is essential for the function of siderophores, which could explain why such a risky strategy is widespread. We developed a reaction-diffusion model to determine the impact of siderophore release on overcoming iron limitation caused by poor solubility in aerobic, pH-neutral environments. We found that secretion of siderophores can efficiently accelerate iron uptake at low solubility, since secreted siderophores solubilize slowly diffusing large iron aggregates to small, quickly diffusing iron-siderophore complexes. At high iron solubility, however, when the iron-siderophore complex is no longer considerably smaller than the iron source itself, siderophore secretion can also slow down iron uptake. In addition, we found that cells can synergistically share their siderophores, depending on their distance and the level of iron aggregation. Overall, our study helps understand why siderophore secretion is so widespread: Even though a large fraction of secreted siderophores is lost, the solubilization of iron through secreted siderophores can efficiently increase iron uptake, especially if siderophores are produced cooperatively by several cells.