Catechol siderophores control tungsten uptake and toxicity in the nitrogen-fixing bacterium Azotobacter vinelandii

Molybdenum (Mo) and tungsten (W), which have similar chemistry, are present at roughly the same concentration in the earth's continental crust, and both are present in oxic systems as oxoanions, molybdate and tungstate. Molybdenum is a cofactor in the molybdenum-nitrogenase enzyme and is thus an important micronutrient for N-2-fixing bacteria such as Azotobacter vinelandii (A. vinelandii). Tungsten is known to be toxic to N2-fixing bacteria, partly by substituting for Mo in nitrogenase. We show that the catechol siderophores produced by A. vinelandii, in addition to being essential for iron acquisition, modulate the relative uptake of Mo and W. These catechol siderophores (particularly protochelin), whose concentrations in the growth medium increase sharply at high W, complex all the tungstate along with molybdate and some of the iron. The molybdenum-catechol complex is taken up much more rapidly than the W complex, allowing A. vinelandii to satisfy its Mo requirement and avoid W toxicity. Mutants deficient in the production of catechol siderophores are more sensitive to tungstate and have higher cellular W quotas than the wild type. The binding of metals by excreted catechol siderophores allows A. vinelandii to discriminate in its uptake of essential metals, such as Fe and Mo, over that of toxic metals, such as W, and to sustain high growth rates under adverse environmental conditions.