Stepping stones in the electron transport from cells to electrodes in Geobacter sulfurreducens biofilms

Abstract

Geobacter sulfurreducens bacteria grow on biofilms and have the particular ability of using polarized electrodes as the final electron acceptor of their respiratory chain. In these biofilms, electrons are transported through distances of more than 50 μm before reaching the electrode. The way in which electrons are transported across the biofilm matrix through such large distances remains under intense discussion. None of the two mechanisms proposed for explaining the process, electron hopping through outer membrane cytochromes and metallic like conduction through conductive PilA filaments, can account for all the experimental evidence collected so far. Aiming at providing new elements for understanding the basis for electron transport, in this perspective article we present a modelled structure of Geobacter pilus. Its analysis in combination with already existing experimental evidence gives support to the proposal of the "stepping stone" mechanism, in which the combined action of pili and cytochromes allows long range electron transport through the biofilm.

A Geobacter sulfurreducens Strain Expressing Pseudomonas aeruginosa Type IV Pili Localizes OmcS on Pili but Is Deficient in Fe(III) Oxide Reduction and Current Production

“…Geobacter sulfurreducens, and presumably other Geobacter species, produce electrically conductive pili that have been proposed to serve as a conduit for extracellular electron transfer (2,3), but the mechanisms for electron transfer along G. sulfurreducens pili is a matter of considerable debate (4)(5)(6). Laboratories that have experimentally investigated G. sulfurreducens pili have concluded that electron transport along the pili is an intrinsic function of the pili itself and does not involve electron hopping/tunneling between traditional electron transfer proteins, such as cytochromes (2,3,7,8), even though the c-type cytochrome OmcS is associated with the pili (9,10).…”

Conductivity of individual Geobacter pili

“…4,5 However, this concept has been challenged repeatedly on the basis of theoretical modelling or inferences from biolm behaviour. [6][7][8][9][10][11][12] Remarkably, amongst this controversy the most basic data requirement, an estimate of the conductivity of individual pili, has been missing. Therefore, a low-noise nano-electrode measurement platform was devised to directly measure the conductivity of individual pili ( Fig.…”

Comparative Proteomics Implicates a Role for Multiple Secretion Systems in Electrode-Respiring Geobacter sulfurreducens Biofilms

“…It has been proposed that electrons harvested from the cytoplasmic metabolic processes of surface-attached G. sulfurreducens are transported to the solid electrode via a complex assembly of cytochrome conduits spanning the inner membrane through to the extracellular milieu 8,24 , Specifically, electrons may be transferred from the menaquinone pool to periplasmic c-type cytochromes, such as GSU1996 24 , via an inner membrane-associated redox protein, such as cytochrome c ImcH…”

“…Two mechanisms are proposed; i) electron hopping through redox proteins (c-type cytochromes) present in the outer membrane 5,6 and, ii) metallic-like conductivity through Type IV pili (nanowires) 7 . Evidence has been presented to support and oppose both conjectures but, as yet, no published consensus has been reached 8 .…”