Geobacter Strains Expressing Poorly Conductive Pili Reveal Constraints on Direct Interspecies Electron Transfer Mechanisms

Toshiyuki Ueki,Joy E Ward,Derek R Lovley,Trevor L Woodard,Amelia-Elena Rotaru,Li-Ying Wang,Kelly P Nevin,Eleftherios T Papoutsakis

doi:10.1128/mbio.01273-18

Toshiyuki Ueki, Joy E Ward + Show 6 more

Open Access

https://doi.org/10.1128/mbio.01273-18

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Abstract

ABSTRACTCytochrome-to-cytochrome electron transfer and electron transfer along conduits of multiple extracellular magnetite grains are often proposed as strategies for direct interspecies electron transfer (DIET) that do not require electrically conductive pili (e-pili). However, physical evidence for these proposed DIET mechanisms has been lacking. To investigate these possibilities further, we constructed Geobacter metallireducens strain Aro-5, in which the wild-type pilin gene was replaced with the aro-5 pilin gene that was previously shown to yield poorly conductive pili in Geobacter sulfurreducens strain Aro-5. G. metallireducens strain Aro-5 did not reduce Fe(III) oxide and produced only low current densities, phenotypes consistent with expression of poorly conductive pili. Like G. sulfurreducens strain Aro-5, G. metallireducens strain Aro-5 displayed abundant outer surface cytochromes. Cocultures initiated with wild-type G. metallireducens as the electron-donating strain and G. sulfurreducens strain Aro-5 as the electron-accepting strain grew via DIET. However, G. metallireducens Aro-5/G. sulfurreducens wild-type cocultures did not. Cocultures initiated with the Aro-5 strains of both species grew only when amended with granular activated carbon (GAC), a conductive material known to be a conduit for DIET. Magnetite could not substitute for GAC. The inability of the two Aro-5 strains to adapt for DIET in the absence of GAC suggests that there are physical constraints on establishing DIET solely through cytochrome-to-cytochrome electron transfer or along chains of magnetite. The finding that DIET is possible with electron-accepting partners that lack highly conductive pili greatly expands the range of potential electron-accepting partners that might participate in DIET.

Highlights

Cytochrome-to-cytochrome electron transfer and electron transfer along conduits of multiple extracellular magnetite grains are often proposed as strategies for direct interspecies electron transfer (DIET) that do not require electrically conductive pili (e-pili)
Geobacter strains with poorly conductive pili and the ability to produce abundant outer surface c-type cytochromes offer an experimental model to evaluate whether microorganisms can adapt for DIET via cytochrome-to-cytochrome electron transfer
The G. sulfurreducens strain with poorly conductive pili grows as the electronaccepting partner for DIET

Summary

Introduction

Cytochrome-to-cytochrome electron transfer and electron transfer along conduits of multiple extracellular magnetite grains are often proposed as strategies for direct interspecies electron transfer (DIET) that do not require electrically conductive pili (e-pili). A model for DIET in environments in which Geobacter species function as the electron-donating partner is that electrically conductive pili (e-pili [16]) are the conduit for long-range electron transport between cells (Fig. 1a). The density, conductivity, and physical flexibility of e-pili in DIET aggregates provide a high possibility that an electron-donating partner can make an electrical contact with an electronaccepting partner.

Results

Conclusion