Abstract
A central question in microbial ecology is whether microbial interactions are predominantly cooperative or competitive. The secretion of siderophores, microbial iron chelators, is a model system for cooperative interactions. However, siderophores have also been shown to mediate competition by sequestering available iron and making it unavailable to competitors. The details of how siderophores mediate competition are not well understood, especially considering the complex distribution of iron phases in the environment. One pertinent question is whether sequestering iron through siderophores can indeed be effective in natural conditions; many natural environments are characterized by large pools of precipitated iron, and it is conceivable that any soluble iron that is sequestered by siderophores is replenished by the dissolution of these precipitated iron sources. Our goal here was to address this issue, and investigate the magnitude and mechanism of siderophore-mediated competition in the presence of precipitated iron. We combined experimental work with thermodynamic modeling, using Pseudomonas aeruginosa as a model system and ferrihydrite precipitates as the iron source with low solubility. Our experiments show that competitive growth inhibition by the siderophore pyochelin is indeed efficient, and that inhibition of a competitor can even have a stronger growth-promoting effect than solubilization of precipitated iron. Based on the results of our thermodynamic models we conclude that the observed inhibition of a competitor is effective because sequestered iron is only very slowly replenished by the dissolution of precipitated iron. Our research highlights the importance of competitive benefits mediated by siderophores, and underlines that the dynamics of siderophore production and uptake in environmental communities could be a signature of competitive, not just cooperative, dynamics.
Highlights
Bacteria rely on iron for survival and growth, apart from rare exceptions
If bacteria produce sufficient siderophores, iron sequestration could be an important function of pyochelin under these conditions, where we found growth promotion of a pyochelinusing strain to be mediated largely by competition, not iron solubilization (Figure 3)
Our findings support the hypothesis that siderophores in environmental systems inhibit other bacteria that lack the specific siderophore receptor system, as supported by previous observational studies (Vachée et al, 1997; Gram et al, 1999; Khare and Tavazoie, 2015)
Summary
Bacteria face low iron availability in most environments, as under aerobic, pH-neutral conditions, the solubility of the predominant iron species, ferric iron, is only around 10−17 M (Andrews et al, 2003). Even though the absolute iron concentration may be several magnitudes higher, iron above this solubility limit precipitates and is not available for direct uptake by bacteria. Many bacteria secrete iron-chelating molecules called siderophores (Hider and Kong, 2010). The primary role of siderophores is thought to be increasing iron availability through solubilization of precipitated environmental iron sources (Andrews et al, 2003). Based on the use of siderophores as a model system for cooperation in laboratory studies, the distribution of siderophore production and receptor genes in the environment has been interpreted mainly as a result of cooperative interactions (Cordero et al, 2012; Andersen et al, 2015)
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