Summary: The multi‐heme, outer membrane c ‐type cytochrome ( c ‐ C yt) OmcB of G eobacter sulfurreducens was previously proposed to mediate electron transfer across the outer membrane. However, the underlying mechanism has remained uncharacterized. In G . sulfurreducens , the omcB gene is part of two tandem four‐gene clusters, each is predicted to encode a transcriptional factor ( OrfR / OrfS ), a porin‐like outer membrane protein ( OmbB / OmbC ), a periplasmic c‐ type cytochrome ( OmaB / OmaC ) and an outer membrane c ‐ C yt ( OmcB / OmcC ) respectively. Here, we showed that OmbB / OmbC , OmaB / OmaC and OmcB / OmcC of G . sulfurreducens PCA formed the porin‐cytochrome ( P cc) protein complexes, which were involved in transferring electrons across the outer membrane. The isolated P cc protein complexes reconstituted in proteoliposomes transferred electrons from reduced methyl viologen across the lipid bilayer of liposomes to F e( III )‐citrate and ferrihydrite. The pcc clusters were found in all eight sequenced G eobacter and 11 other bacterial genomes from six different phyla, demonstrating a widespread distribution of P cc protein complexes in phylogenetically diverse bacteria. Deletion of ombB‐omaB‐omcB‐orfS‐ombC‐omaC‐omcC gene clusters had no impact on the growth of G . sulfurreducens PCA with fumarate but diminished the ability of G . sulfurreducens PCA to reduce F e( III )‐citrate and ferrihydrite. Complementation with the ombB‐omaB‐omcB gene cluster restored the ability of G . sulfurreducens PCA to reduce F e( III )‐citrate and ferrihydrite.

Significance: In solar-terrestrial systems, solar energy input has long been recognized to have a profound impact on Earth. The well-known photosynthetic systems enable sustainable solar-to-chemical energy conversion. However, no evidence has yet emerged for the existence of a widespread geological light-harvesting system. This study reveals such a “photoelectric device,” where semiconducting Fe- and Mn (oxyhydr)oxide-mineral coatings are found to overlay vast expanses of natural rock/soil surfaces and exhibit highly responsive and stable photon-to-electron conversion. Our discovery may provide insight supporting vital photon-induced redox chemistry on Earth’s surface via widespread Fe- and Mn-mineral coatings.

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 CymA_ES-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 CymA_ES-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.