Seeing is believing: novel imaging techniques help clarify microbial nanowire structure and function

Abstract

SummaryNovel imaging approaches have recently helped to clarify the properties of 'microbial nanowires'. Geobacter sulfurreducens pili are actual wires. They possess metallic-like conductivity, which can be attributed to overlapping pi-pi orbitals of key aromatic amino acids. Electrostatic force microscopy recently confirmed charge propagation along the pili, in a manner similar to carbon nanotubes. The pili are essential for long-range electron transport to insoluble electron acceptors and interspecies electron transfer. Previous claims that Shewanella oneidensis also produce conductive pili have recently been recanted, based on novel live-imaging studies. The putative pili are, in fact, long extensions of the cytochrome-rich outer membrane and periplasm that, when dried, collapse to form filaments with dimensions similar to pili. It has yet to be demonstrated whether the cytochrome-to-cytochrome electron hopping documented in the dried membrane extensions takes place in intact hydrated membrane extensions or whether the membrane extensions enhance electron transport to insoluble electron acceptors such as Fe(III) oxides or electrodes. These findings demonstrate that G. sulfurreducens conductive pili and the outer membrane extensions of S. oneidensis are fundamentally different in composition, mechanism of electron transport and physiological role. New methods for evaluating filament conductivity will facilitate screening the microbial world for nanowires and elucidating their function.

The electrically conductive pili of Geobacter species are a recently evolved feature for extracellular electron transfer

“…As previously noted in the analysis of the Geobacter sulfurreducens PilA sequence (Malvankar et al, 2015;Reardon & Mueller, 2013;Reguera et al, 2005), the N-termini of the epilin proteins share many similarities with previously described type IVa PilA found in members of genera such as Neisseria, Pseudomonas, Escherichia and Myxococcus (Giltner et al, 2012;Mattick, 2002). It is highly conserved and consists of one or two alpha helices and a transmembrane *Secondary structure predictions were made with the Jnet algorithm (Cuff & Barton, 2000) on the Jpred4 server ( (Drozdetskiy et al, 2015) Geobacter uraniireducens…”

“…Analysis of the structure of the Geobacter sulfurreducens e-pilus suggested that the lack of this C-terminus sequence permits the pilin monomers to pack more tightly than the larger pilin monomers found in most bacteria, yielding a thinner pilus diameter and positioning amino acids in patterns that confer conductivity (Malvankar et al, 2015).…”

“…The distance over which e-pili can conduct electrons and the apparent competitive advantage of this capability in a number of anaerobic environments distinguish electron transfer via e-pili from more typical forms of short-range biological electron transfer (Lovley & Malvankar, 2015;Malvankar et al, 2015;Vargas et al, 2013).…”

“…It has been speculated that the shorter pilus monomer permits tighter packing, positioning aromatic amino acids (Lovley & Malvankar, 2015) and charged amino acids (Feliciano et al, 2015), in a manner that promotes electron conduction along the length of the pilin. This hypothesis is supported by the finding that G. metallireducens, which also has a short PilA, produces e-pili (Y.…”

Electrically Conductive Pili from Pilin Genes of Phylogenetically Diverse Microorganisms

“…There is debate whether the aromatic amino acids contribute to a traditional electron-hopping electron transport mechanism or whether over-lapping π-π orbitals of the aromatics confer a metallic-like conductivity similar to that observed in synthetic conducting polymers (Lampa-Pastirk et al 2016, Lovley and Malvankar 2015, Vargas et al 2013. However, the uncertainty over these mechanistic details should not obscure the fact that long-range electron transport via epili is a remarkable strategy for long-range biological electron transfer.…”