Silicate minerals as a direct source of limiting nutrients: Siderophore synthesis and uptake promote ferric iron bioavailability from olivine and microbial growth.

Abstract

Iron is a micronutrient critical to fundamental biological processes including respiration and photosynthesis, and it can therefore impact primary and heterotrophic productivity. Yet in oxic environments, iron is highly insoluble, rendering it, in principle, unavailable as a nutrient for biological growth. Life has "solved" this problem via the invention of iron chelates, known as siderophores, that keep iron available for microbial productivity. In this work, we examined the impact of siderophore synthesis on the speciation, mobility, and bioavailability of iron from rock-forming silicate minerals-shedding new light on the mechanisms by which microbes use mineral substrates to support primary productivity, as well as the consequent effects on silicate dissolution. Growth experiments were performed with Shewanella oneidensis MR-1 in an oxic, iron-depleted minimal medium, amended with olivine minerals as the sole source of iron. Experiments included the wild-type strain MR-1, and a siderophore synthesis gene deletion mutant strain (ΔMR-1). Relative to MR-1, ΔMR-1 exhibited a very pronounced growth penalty and an extended lag phase. However, substantial growth of ΔMR-1, comparable to MR-1 growth, was observed when the mutant strain was provided with siderophores in the form of either filtrate from a well-grown MR-1 culture, or commercially available deferoxamine. These observations suggest that siderophores are critical for S. oneidensis to acquire iron from olivine. Growth-limiting concentrations of deferoxamine amendments were observed to be ≤5-10µM, concentrations significantly lower than previously recorded as necessary to impact mineral dissolution rates. X-ray photoelectric spectroscopy analyses of the incubated olivine surfaces suggest that siderophores deplete mineral surface layers of ferric iron. Combined, these results demonstrate that low micromolar concentrations of siderophores can effectively mobilize iron bound within silicate minerals, supporting very significant biological growth in limiting environments. The specific mechanism would involve siderophores removing a protective layer of nanometer-thick iron oxides, enhancing silicate dissolution and nutrient bioavailability.