Aerobic iron-oxidizing bacteria secrete metabolites that markedly impede abiotic iron oxidation

Iron is one of the Earth's most abundant elements and is required for essentially all forms of life. Yet, iron's reactivity with oxygen and poor solubility in its oxidized form (Fe³⁺) mean that it is often a limiting nutrient in oxic, near-neutral pH environments like Earth's ocean. In addition to being a vital nutrient, there is a diversity of aerobic organisms that oxidize ferrous iron (Fe²⁺) to harness energy for growth and biosynthesis. Accordingly, these organisms rely on access to co-existing Fe²⁺ and O₂ to survive. It is generally presumed that such aerobic iron-oxidizing bacteria (FeOB) are relegated to low-oxygen regimes where abiotic iron oxidation rates are slower, yet some FeOB live in higher oxygen environments where they cannot rely on lower oxygen concentrations to overcome abiotic competition. We hypothesized that FeOB chemically alter their environment to limit abiotic interactions between Fe²⁺ and O₂. To test this, we incubated the secreted metabolites (collectively known as the exometabolome) of the deep-sea iron- and hydrogen-oxidizing bacterium Ghiorsea bivora TAG-1 with ferrous iron and oxygen. We found that this FeOB's iron-oxidizing exometabolome markedly impedes the abiotic oxidation of ferrous iron, increasing the half-life of Fe²⁺ 100-fold from ∼3 to ∼335 days in the presence of O₂, while the exometabolome of TAG-1 grown on hydrogen had no effect. Moreover, the few precipitates that formed in the presence of TAG-1's iron-oxidizing exometabolome were poorly crystalline, compared with the abundant iron particles that mineralized in the absence of abiotic controls. We offer an initial exploration of TAG-1's iron-oxidizing exometabolome and discuss potential key contributors to this process. Overall, our findings demonstrate that the exometabolome as a whole leads to a sustained accumulation of ferrous iron in the presence of oxygen, consequently altering the redox equilibrium. This previously unknown adaptation likely enables these microorganisms to persist in an iron-oxidizing and iron-precipitating world and could have impacts on the bioavailability of iron to FeOB and other life in iron-limiting environments.