Abstract
The Gram-negative bacterium Sideroxydans lithotrophicus ES-1 (ES-1) grows on FeCO3 or FeS at oxic–anoxic interfaces at circumneutral pH, and the ES-1-mediated Fe(II) oxidation occurs extracellularly. However, the molecular mechanisms underlying ES-1’s ability to oxidize Fe(II) remain unknown. Survey of the ES-1 genome for candidate genes for microbial extracellular Fe(II) oxidation revealed that it contained a three-gene cluster encoding homologs of Shewanella oneidensis MR-1 (MR-1) MtrA, MtrB, and CymA that are involved in extracellular Fe(III) reduction. Homologs of MtrA and MtrB were also previously shown to be involved in extracellular Fe(II) oxidation by Rhodopseudomonas palustris TIE-1. To distinguish them from those found in MR-1, the identified homologs were named MtoAB and CymAES-1. Cloned mtoA partially complemented an MR-1 mutant without MtrA with regards to ferrihydrite reduction. Characterization of purified MtoA showed that it was a decaheme c-type cytochrome and oxidized soluble Fe(II). Oxidation of Fe(II) by MtoA was pH- and Fe(II)-complexing ligand-dependent. Under conditions tested, MtoA oxidized Fe(II) from pH 7 to pH 9 with the optimal rate at pH 9. MtoA oxidized Fe(II) complexed with different ligands at different rates. The reaction rates followed the order Fe(II)Cl2 > Fe(II)–citrate > Fe(II)–NTA > Fe(II)–EDTA with the second-order rate constants ranging from 6.3 × 10−3 μM−1 s−1 for oxidation of Fe(II)Cl2 to 1.0 × 10−3 μM−1 s−1 for oxidation of Fe(II)–EDTA. Thermodynamic modeling showed that redox reaction rates for the different Fe(II)-complexes correlated with their respective estimated reaction-free energies. Collectively, these results demonstrate that MtoA is a functional Fe(II)-oxidizing protein that, by working in concert with MtoB and CymAES-1, may oxidize Fe(II) at the bacterial surface and transfer released electrons across the bacterial cell envelope to the quinone pool in the inner membrane during extracellular Fe(II) oxidation by ES-1.
Highlights
The contribution of Fe(II)-oxidizing bacteria (FeOB) to iron cycling in freshwater, groundwater, and marine environments, as well as in most soils and sediments, has been well recognized (Emerson et al, 2010)
IDENTIFICATION OF MtoAB AND CymAES-1 Search of the ES-1 genome did not reveal any homologs for Cyc-2/Rus/Cyc-1 of A. ferrooxidans or FoxEYZ of Rhodobacter strain SW2, but identified a gene cluster that encoded an MtrA/PioA homolog (Slit_2497) and an MtrB/PioB homolog (Slit_2496)
To distinguish them from those found in MR-1 and PioAB of R. palustris TIE-1, we named these genes and their encoding proteins mtoAB–cymA and MtoAB/CymAES-1, respectively (Figure 1)
Summary
The contribution of Fe(II)-oxidizing bacteria (FeOB) to iron cycling in freshwater, groundwater, and marine environments, as well as in most soils and sediments, has been well recognized (Emerson et al, 2010). A variety of neutrophilic and acidophilic Fe(II)-oxidizing microorganisms have the ability to derive energy for growth from the oxidation of dissolved or structural Fe(II) under either oxic or anoxic conditions. Recent studies indicate that aerobic neutrophilic FeOB would play a key role in microoxic niches with low levels of O2 concentration, where microbial Fe(II)-oxidation can compete with the chemical oxidation of Fe(II). ES-1 does not grow on Mn(II) oxides, sulfide, or organic carbon sources, such as acetate, pyruvate, and glucose, and does not reduce Fe(III) oxides. Fe(III) (oxy)(hydr)oxide precipitates are closely associated with the ES-1 cells, but do not form sheath- or stalk-like structures (Emerson and Moyer, 1997). The molecular mechanism by which ES-1 oxidizes Fe(II) remains unknown
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