Shewanella oneidensis MR-1 Uses Overlapping Pathways for Iron Reduction at a Distance and by Direct Contact under Conditions Relevant for Biofilms

Abstract

We developed a new method to measure iron reduction at a distance based on depositing Fe(III) (hydr)oxide within nanoporous glass beads. In this "Fe-bead" system, Shewanella oneidensis reduces at least 86.5% of the iron in the absence of direct contact. Biofilm formation accompanies Fe-bead reduction and is observable both macro-and microscopically. Fe-bead reduction is catalyzed by live cells adapted to anaerobic conditions, and maximal reduction rates require sustained protein synthesis. The amount of reactive ferric iron in the Fe-bead system is available in excess such that the rate of Fe-bead reduction is directly proportional to cell density; i.e., it is diffusion limited. Addition of either lysates prepared from anaerobic cells or exogenous electron shuttles stimulates Fe-bead reduction by S. oneidensis, but iron chelators or additional Fe(II) do not. Neither dissolved Fe(III) nor electron shuttling activity was detected in culture supernatants, implying that the mediator is retained within the biofilm matrix. Strains with mutations in omcB or mtrB show about 50% of the wild-type levels of reduction, while a cymA mutant shows less than 20% of the wild-type levels of reduction and a menF mutant shows insignificant reduction. The Fe-bead reduction defect of the menF mutant can be restored by addition of menaquinone, but menaquinone itself cannot stimulate Fe-bead reduction. Because the menF gene encodes the first committed step of menaquinone biosynthesis, no intermediates of the menaquinone biosynthetic pathway are used as diffusible mediators by this organism to promote iron reduction at a distance. CymA and menaquinone are required for both direct and indirect mineral reduction, whereas MtrB and OmcB contribute to but are not absolutely required for iron reduction at a distance.

Shewanella secretes flavins that mediate extracellular electron transfer

“…alga BrY reduced iron oxides trapped within porous alginate beads. A more recent study by Lies et al (4) also demonstrated reduction of Fe(III) oxides precipitated within nanoporous glass beads by Shewanella oneidensis MR-1 (4). Importantly, these studies could not detect a compound to explain these observations or differentiate between a model where a redox active compound produced by Shewanella diffused into the bead and a model where Shewanella produced a molecule to chelate ferric iron to facilitate its return to the cell.…”

“…m (1)(2)(3), yet bacteria such as Shewanella demonstrate an ability to transfer electrons to metals located Ͼ50 m from cell surfaces (4,5). For example, in experiments by Nevin and Lovley (5), Shewanella.…”

Electrode materials for microbial fuel cells: nanomaterial approach

“…The outer membrane cytochrome (C-type) is involved in the direct transfer of electrons produced from NADH [14]. Electron transfer through mediators: Few genera of bacteria such as Shewanella and Pseudomonas secrete some chemical species such as flavins called shuttle molecules to transfer electrons from the outer membrane of bacteria to electrodes [15,16].…”

Structure of a bacterial cell surface decaheme electron conduit

“…(ii) indirect electron transfer mediated by flavin electron shuttles, or (iii) intercytochrome electron transfer, possibly along "nanowires" (8)(9)(10)(11)(12)(13)(14)(15)(16). Here we present the X-ray crystal structure of a decaheme terminus of an OM conduit, MtrF, and propose models from this structure into how these different types of extracellular electron transfer might occur.…”