Going Wireless: Fe(III) Oxide Reduction without Pili by Geobacter sulfurreducens Strain JS-1

Abstract

Previous studies have suggested that the conductive pili of Geobacter sulfurreducens are essential for extracellular electron transfer to Fe(III) oxides and for optimal long-range electron transport through current-producing biofilms. The KN400 strain of G. sulfurreducens reduces poorly crystalline Fe(III) oxide more rapidly than the more extensively studied DL-1 strain. Deletion of the gene encoding PilA, the structural pilin protein, in strain KN400 inhibited Fe(III) oxide reduction. However, low rates of Fe(III) reduction were detected after extended incubation (>30 days) in the presence of Fe(III) oxide. After seven consecutive transfers, the PilA-deficient strain adapted to reduce Fe(III) oxide as fast as the wild type. Microarray, whole-genome resequencing, proteomic, and gene deletion studies indicated that this adaptation was associated with the production of larger amounts of the c-type cytochrome PgcA, which was released into the culture medium. It is proposed that the extracellular cytochrome acts as an electron shuttle, promoting electron transfer from the outer cell surface to Fe(III) oxides. The adapted PilA-deficient strain competed well with the wild-type strain when both were grown together on Fe(III) oxide. However, when 50% of the culture medium was replaced with fresh medium every 3 days, the wild-type strain outcompeted the adapted strain. A possible explanation for this is that the necessity to produce additional PgcA, to replace the PgcA being continually removed, put the adapted strain at a competitive disadvantage, similar to the apparent selection against electron shuttle-producing Fe(III) reducers in many anaerobic soils and sediments. Despite increased extracellular cytochrome production, the adapted PilA-deficient strain produced low levels of current, consistent with the concept that long-range electron transport through G. sulfurreducens biofilms is more effective via pili.

Significance of a Posttranslational Modification of the PilA Protein of Geobacter sulfurreducens for Surface Attachment, Biofilm Formation, and Growth on Insoluble Extracellular Electron Acceptors

“…Two possible explanations for this behavior are that the population somehow adapted to the situation or that a suppressor mutant arose in the population (62-64). While we cannot choose between these two with the data presented, we favor the possibility that a suppressor mutant arose because it was shown elsewhere that pilA deletion mutants readily acquire suppressors enabling their growth under similar selective conditions (64). Therefore, it is possible that the lack of current production observed for the pilAY32F strain can be attributed to a deficiency in pilus-mediated attachment or to a combination of impairments in attachment and electron transfer.…”

Expressing the Geobacter metallireducens PilA in Geobacter sulfurreducens Yields Pili with Exceptional Conductivity

“…Whereas G. sulfurreducens requires direct contact to reduce Fe(III) oxides (19), G. uraniireducens produced an electron shuttle for long-range electron transport (17). Furthermore, G. uraniireducens was not capable of producing high current densities (20).…”

The Colorful World of Extracellular Electron Shuttles

“…Whether and/or how electrons traverse through nanowires, cables, or some type of extracellular matrix is still being debated (74, 86, 114, 127). We simply note that in some organisms, such as the mineral-reducing bacteria Shewanella and Geobacter species, the proteinaceous machinery that is required for extracellular electron transfer can interact with and reduce EESs of different types (16, 66, 71, 109, 116). Thus, it is important to be mindful of the potential involvement of EESs in any context where extracellular electron transfer matters, be it the soil of the rhizosphere or the inflamed tissues of chronic infections.…”