Geobacter species "breathe" minerals instead of oxygen by transferring electrons along protein nanowire "pilli" via "electron hopping".

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Electricity is necessary to bring our machinery and devices alive. Similarly, biological organisms need to keep electrons flowing to keep cellular machinery up and running. An important component of that system is a molecule that is able to accept electrons, particularly those generated from the digestion (oxidation) of food sources. In most species, such as humans and other mammals, oxygen acts as the electron receptor. However, certain microorganisms are able to survive by using minerals to do the job. Some organisms use chemical shuttles to transport electrons while others rely on direct contact with the mineral even when it exists outside its “body”.

One such example is Geobacter sulfurreducens which produces pilli (long, extracellular tubules) that act as protein nanowires to conduct the flow of electrons to the solid mineral. In a process called “electron hopping,” electrons are transferred down the wire by progressively hopping from charged areas in the protein strands. The “bucket brigade” analogy is often used to visualize the process. In terms of physics, this kind of progressive transfer is referred to as superexchange. The pilli of geobacter species can grow up to 20 microns in length which is astonishing given that the bacteria is only about 1 micron in length. The transfer of electrons down this microbial nanowire proceeds with high efficiency up to the interface between the pilli and the external mineral.

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“The mechanism of EET by Geobacter and Shewanella spp. involves superexchange in which electrons are conducted by a succession of electron transfer reactions among redox proteins associated with the outer cell membranes, aligned along pilus-like filaments (e.g. pili), and/or throughout the extracellular matrix.” (Strycharz-Glaven et al. 2011:4366)

Geobacter spp. form thick biofilms, through which electron transfer occurs to the anode from cells many cell lengths away from the anode surface…Recent results implicate microbial nanowires, defined here as proteinaceous pilus-like filaments demonstrated to possess electrical conductivity, as playing a central role in EET.” (Strycharz-Glaven et al. 2011:4367)

G. sulfurreducens nanowires are reported to be type IV pili that are primarily composed of the pilin protein structural subunit PilA…Nanowires of G. sulfurreducens measure 3–5 nm in diameter and up to 20 μm in length (by comparison, G. sulfurreducens cell bodies are typically 1 μm long), extend into the extracellular domain, and are secreted through the outer cell membrane where they anchor to the cell body…G. sulfurreducens relies on a network of membrane associated and periplasmic proteins for Fe(III) oxide mineral reduction, including PilA, OmcS, OmcE, OmcB, OmpB and OmpC…At least one, OmcS, is localized along pili and has been proposed to be the terminal mediator for electron transfer from pili to minerals…In this perspective we present a mechanism of conduction known as superexchange originally developed to describe electrical conductivity within polymers containing bound discrete redox groups (redox polymers).” (Strycharz-Glaven et al. 2011:4367-8)

“Owing to the molecular (vs. crystalloid) nature of microbes, [and] the prevalence of redox proteins such as outer membrane cytochromes…we subscribe to the theory that EET by Geobacter and Shewanella spp. involves electron superexchange by which electrons are conducted in a bucket-brigade manner by a sequence of bimolecular electron transfer reactions between adjacent redox proteins…In discrete, non-periodic amorphous materials such as redox polymers this phenomenon is most commonly referred to as electron hopping.” (Strycharz-Glaven et al. 2011:4368-9)

“The measurements of nanowire conductivity described above have led many investigators to suggest that these structures are responsible for EET to anodes directly…the ex vivo demonstrations of electron conduction by individual nanowires described above while dry result from electric field driven superexchange…nanowires are pili that contain electronically delocalized domains that conduct electrons much like conducting polymers such as polyaniline or polypyrolle…in the case of ., pili may be relied upon by cells farther from the electrode surface for EET, and the maximum thickness of PilA deficient biofilms may be the point at which cells are effectively electron acceptor limited owing to their distance from the electrode. Pili may therefore play a role in relieving electron acceptor limitations, possibly through increasing the cell surface area for cytochrome localization and electron storage in order to reoxidize periplasmic and inner membrane electron carriers” (Strycharz-Glaven et al. 2011:4375)

Journal article
On the electrical conductivity of microbial nanowires and biofilmsSarah M. Strycharz-Glaven, Rachel M. Snider, Anthony Guiseppi-Eliec, Leonard M. Tender

Journal article
Extracellular electron transfer via microbial nanowiresNatureJune 22, 2005
Gemma Reguera, Kevin D. McCarthy, Teena Mehta, Julie S. Nicoll, Mark T. Tuominen, Derek R. Lovley

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