Extracellular electron transfer via microbial nanowires

Abstract

Microbes that can transfer electrons to extracellular electron acceptors, such as Fe(iii) oxides, are important in organic matter degradation and nutrient cycling in soils and sediments. Previous investigations on electron transfer to Fe(iii) have focused on the role of outer-membrane c-type cytochromes. However, some Fe(iii) reducers lack c-cytochromes. Geobacter species, which are the predominant Fe(iii) reducers in many environments, must directly contact Fe(iii) oxides to reduce them, and produce monolateral pili that were proposed, on the basis of the role of pili in other organisms, to aid in establishing contact with the Fe(iii) oxides. Here we report that a pilus-deficient mutant of Geobacter sulfurreducens could not reduce Fe(iii) oxides but could attach to them. Conducting-probe atomic force microscopy revealed that the pili were highly conductive. These results indicate that the pili of G. sulfurreducens might serve as biological nanowires, transferring electrons from the cell surface to the surface of Fe(iii) oxides. Electron transfer through pili indicates possibilities for other unique cell-surface and cell-cell interactions, and for bioengineering of novel conductive materials.

Harnessing the power of microbial nanowires

“…They are dynamic filaments that undergo cycles of polymerization and depolymerization of primarily one pilin peptide, to promote, among other functions, attachment to and/or translocation on surfaces, binding and uptake of DNA, and/or cell–cell aggregation and biofilm formation (Craig and Li, 2008; Maier and Wong, 2015). The genomes of several Geobacter bacteria encode all of the genes needed to make a functional T4P apparatus, but the pilin gene encodes a uniquely short peptide (Reguera et al ., 2005). Genetic studies in the model representative Geobacter sulfurreducens (GS) have provided insights into how the cells assemble the GS pilin into a conductive fibre.…”

“…The cytoplasmic protein PilM is then recruited by PilNO, an association that changes the orientation of PilM to promote interactions with the assembly protein PilC at the base of the pilus (Friedrich et al ., 2014). As in M. xanthus , the GS PilC is encoded in a separate gene cluster ( pilBTCSRA) containing the genes that code for the sensor ( pilS ) and response regulator ( pilR ) of pilus biogenesis (Juarez et al ., 2009) and the operon containing the pilA gene ( pilA‐N , encoding the PilA pilin) and a gene encoding a hypothetical protein ( pilA‐C ) (Reguera et al ., 2005). The cluster also includes the pilB and PilT4 genes, which code for the PilB and PilT4 ATPases that interact with PilC to power the extension and retraction of the T4P respectively (Speers et al ., 2016; Steidl et al ., 2016).…”

“…The reduction of Fe(III) oxides by the conductive T4P, for example, solubilizes one‐third of the ferric iron (Fe[III]) as the ferrous ion (Fe[II] aq ) and leaves the remaining Fe(II) as magnetite, a mineral of mix ferric‐ferrous valence that remains bound to the T4P (Fig. 2) (Reguera et al ., 2005). Yet, the reduction of the uranyl cation produces a fine‐grained, mononuclear mineral phase of U(IV) (Cologgi et al ., 2011), whose effective detachment from the T4P may require less retraction forces.…”

“…The ability of T4 pilins to polymerize spontaneously via hydrophobic interactions has inspired ‘bottom‐up’ fabrication protocols for the synthesis of protein nanotubes (Audette et al ., 2004a,b) and biocoatings that prevent the corrosion of metallic implants (Muruve et al ., 2016). The discovery that metal‐reducing bacteria in the genus Geobacter produce conductive T4P for the reduction of ferric (Fe[III]) oxide minerals (Reguera et al ., 2005) and the uranyl cation (Cologgi et al ., 2011) suggests novel applications are to be harnessed from the unique electronic and metal binding properties of these protein filaments and their peptide building blocks.…”

“…The model representative Shewanella oneidensis MR‐1 was also assumed to produce pilus ‘nanowires’ (Gorby et al ., 2006; El‐Naggar et al ., 2010), although MR‐1 T4P had previously been shown to be nonconductive (Reguera et al ., 2005). These ‘nanowires’ were later found to be dehydrated forms of outer membrane extensions, which this bacterium forms by fusing outer membrane vesicles (Pirbadian et al ., 2014).…”