Electrons can be transferred from microorganisms to multivalent metal ions that are associated with minerals and vice versa. As the microbial cell envelope is neither physically permeable to minerals nor electrically conductive, microorganisms have evolved strategies to exchange electrons with extracellular minerals. In this Review, we discuss the molecular mechanisms that underlie the ability of microorganisms to exchange electrons, such as c-type cytochromes and microbial nanowires, with extracellular minerals and with microorganisms of the same or different species. Microorganisms that have extracellular electron transfer capability can be used for biotechnological applications, including bioremediation, biomining and the production of biofuels and nanomaterials.

Extracellular electron transfer mechanisms between microorganisms and minerals

Microbial fuel cell (MFC) is of great interest as a promising green energy source to harvest electricity from various organic matters. However, low bacterial loading capacity and low extracellular electron transfer efficiency between the bacteria and the anode often limit the practical applications of MFC. In this work, a macroporous and monolithic MFC anode based on polyaniline hybridized three-dimensional (3D) graphene is demonstrated. It outperforms the planar carbon electrode because of its abilities to three-dimensionally interface with bacterial biofilm, facilitate electron transfer, and provide multiplexed and highly conductive pathways. This study adds a new dimension to the MFC anode design as well as to the emerging graphene applications.

Macroporous and Monolithic Anode Based on Polyaniline Hybridized Three-Dimensional Graphene for High-Performance Microbial Fuel Cells

Immunogold localization revealed that OmcS, a cytochrome that is required for Fe(III) oxide reduction by Geobacter sulfurreducens, was localized along the pili. The apparent spacing between OmcS molecules suggests that OmcS facilitates electron transfer from pili to Fe(III) oxides rather than promoting electron conduction along the length of the pili.

Alignment of the c-type cytochrome OmcS along pili of Geobacter sulfurreducens.

Bioelectrochemical systems rely on microorganisms to link complex oxidation/reduction reactions to electrodes. For example, in Shewanella oneidensis strain MR-1, an electron transfer conduit consisting of cytochromes and structural proteins, known as the Mtr respiratory pathway, catalyzes electron flow from cytoplasmic oxidative reactions to electrodes. Reversing this electron flow to drive microbial reductive metabolism offers a possible route for electrosynthesis of high value fuels and chemicals. We examined electron flow from electrodes into Shewanella to determine the feasibility of this process, the molecular components of reductive electron flow, and what driving forces were required. Addition of fumarate to a film of S. oneidensis adhering to a graphite electrode poised at −0.36 V versus standard hydrogen electrode (SHE) immediately led to electron uptake, while a mutant lacking the periplasmic fumarate reductase FccA was unable to utilize electrodes for fumarate reduction. Deletion of the gene encoding the outer membrane cytochrome-anchoring protein MtrB eliminated 88% of fumarate reduction. A mutant lacking the periplasmic cytochrome MtrA demonstrated more severe defects. Surprisingly, disruption of menC, which prevents menaquinone biosynthesis, eliminated 85% of electron flux. Deletion of the gene encoding the quinone-linked cytochrome CymA had a similar negative effect, which showed that electrons primarily flowed from outer membrane cytochromes into the quinone pool, and back to periplasmic FccA. Soluble redox mediators only partially restored electron transfer in mutants, suggesting that soluble shuttles could not replace periplasmic protein-protein interactions. This work demonstrates that the Mtr pathway can power reductive reactions, shows this conduit is functionally reversible, and provides new evidence for distinct CymA:MtrA and CymA:FccA respiratory units.

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Towards electrosynthesis in shewanella: energetics of reversing the mtr pathway for reductive metabolism.

A rapid and economical route based on an efficient microwave–hydrothermal process has been developed to synthesize monodisperse α-Fe2O3 nanocrystals with continuous aspect-ratio tuning and fine shape control, which takes advantage of microwave irradiation and hydrothermal effects. This method easily programs the experimental conditions (e.g., temperature and time) and significantly shortens the synthesis time to minutes. It allows the creation of numerous recipes for optimizing and scaling up production. The effects of experimental conditions including reaction temperature and reactant concentration on the morphology of α-Fe2O3 have been investigated systematically. Results reveal that the initial molar ratio of Fe3+ to PO plays a crucial role in the final morphology of the α-Fe2O3 products. Several morphologies, which include ellipsoids/spindles with aspect ratios that range from 1.1 to 6.3, nanosheets, nanorings, and spheres can be obtained. The as-formed α-Fe2O3 exhibits shape-dependent infrared optical properties. The growth process of colloidal α-Fe2O3 crystals in the presence of phosphate ions is discussed. The products have been characterized by using X-ray diffraction, scanning electron microscopy, transmission electron microscopy, and infrared spectroscopy. This work presents an efficient and cost-effective approach that is potentially competitive for scaling-up industrial production. The as-formed α-Fe2O3 crystals with controllable morphologies not only provide flexible building blocks for advanced functional devices, but are also ideal candidates for studying their nanoarchitecture-dependent performance in optical, catalytic, and magnetic applications.

Continuous Aspect-Ratio Tuning and Fine Shape Control of Monodisperse α-Fe2O3 Nanocrystals by a Programmed Microwave-Hydrothermal Method

Electrochemical Interaction of Shewanella Oneidensis Mr-1 and Its Outer Membrane Cytochromes Omca and MTRC with Hematite Electrodes

Cytochrome c interaction with hematite (α-Fe2O3) surfaces

Structural and redox properties of mitochondrial cytochrome c co-sorbed with phosphate on hematite (α-Fe2O3) surfaces

Redox-linked conformation change and electron transfer between monoheme c-type cytochromes and oxides

The interaction of cytochromes (heme proteins) with mineral surfaces is important from an environmental perspective (e.g. heavy metal remediation and reductive dehalogenation reactions), for designing biosensors and bioanalytical systems, and for emerging photovoltaic applications. In addition, the cytochrome studied here shares properties with some cytochromes from Fe-reducing bacteria and its general behavior sheds light on how other cytochromes might behave during Fe(III) reduction. The objectives of this study were to characterize the direct electrochemistry and sorption mechanism of horse heart ferricytochrome c (a mitochondrial cytochrome referred to as Hcc) on hematite surfaces as a function of pH, time of sorption and ionic strength. Hcc sorption on hematite mainly occurs between pH 8 and 10, the pH range in which hematite surfaces and Hcc are oppositely charged. Calculated net attractive forces correspond closely with the pH range of peak sorption, suggesting that sorption is mainly electrostatically controlled. Hcc sorption with ionic strength is consistent with this conclusion. The pH-dependent conformation of Hcc sorbed on hematite appears to be different from that in solution as indicated by UV-visible spectroscopy and its more negative reduction potential compared to native Hcc. Sorption kinetics were rapid and pH-independent across the pH range 3–10 with slow conformational changes occurring at >60 h. Our results suggest that the electrostatic attraction of the cytochrome towards the surface orient the cytochrome for favorable electron transfer between the heme group of the cytochrome and hematite.

Nidhi Khare

Papers

Electrochemical Interaction of Shewanella Oneidensis Mr-1 and Its Outer Membrane Cytochromes Omca and MTRC with Hematite Electrodes

Cytochrome c interaction with hematite (α-Fe2O3) surfaces

Structural and redox properties of mitochondrial cytochrome c co-sorbed with phosphate on hematite (α-Fe2O3) surfaces

Redox-linked conformation change and electron transfer between monoheme c-type cytochromes and oxides

Sorption and direct electrochemistry of mitochondrial cytochrome C on hematite surfaces