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Low Energy Atomic Models Suggesting a Pilus Structure that could Account for Electrical Conductivity of Geobacter sulfurreducens Pili.

ABSTRACT: The metallic-like electrical conductivity of Geobacter sulfurreducens pili has been documented with multiple lines of experimental evidence, but there is only a rudimentary understanding of the structural features which contribute to this novel mode of biological electron transport. In order to determine if it was feasible for the pilin monomers of G. sulfurreducens to assemble into a conductive filament, theoretical energy-minimized models of Geobacter pili were constructed with a previously described approach, in which pilin monomers are assembled using randomized structural parameters and distance constraints. The lowest energy models from a specific group of predicted structures lacked a central channel, in contrast to previously existing pili models. In half of the no-channel models the three N-terminal aromatic residues of the pilin monomer are arranged in a potentially electrically conductive geometry, sufficiently close to account for the experimentally observed metallic like conductivity of the pili that has been attributed to overlapping pi-pi orbitals of aromatic amino acids. These atomic resolution models capable of explaining the observed conductive properties of Geobacter pili are a valuable tool to guide further investigation of the metallic-like conductivity of the pili, their role in biogeochemical cycling, and applications in bioenergy and bioelectronics.

SUBMITTER: Xiao K

PROVIDER: S-EPMC4802205 | biostudies-literature | 2016 Mar

REPOSITORIES: biostudies-literature

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Low Energy Atomic Models Suggesting a Pilus Structure that could Account for Electrical Conductivity of Geobacter sulfurreducens Pili.

Xiao Ke K Malvankar Nikhil S NS Shu Chuanjun C Martz Eric E Lovley Derek R DR Sun Xiao X

Scientific reports 20160322

The metallic-like electrical conductivity of Geobacter sulfurreducens pili has been documented with multiple lines of experimental evidence, but there is only a rudimentary understanding of the structural features which contribute to this novel mode of biological electron transport. In order to determine if it was feasible for the pilin monomers of G. sulfurreducens to assemble into a conductive filament, theoretical energy-minimized models of Geobacter pili were constructed with a previously de ...[more]

PMID: 27001169

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Project description:UnlabelledIt has been proposed that Geobacter sulfurreducens requires conductive pili for long-range electron transport to Fe(III) oxides and for high-density current production in microbial fuel cells. In order to investigate this further, we constructed a strain of G. sulfurreducens, designated Aro-5, which produced pili with diminished conductivity. This was accomplished by modifying the amino acid sequence of PilA, the structural pilin protein. An alanine was substituted for each of the five aromatic amino acids in the carboxyl terminus of PilA, the region in which G. sulfurreducens PilA differs most significantly from the PilAs of microorganisms incapable of long-range extracellular electron transport. Strain Aro-5 produced pili that were properly decorated with the multiheme c-type cytochrome OmcS, which is essential for Fe(III) oxide reduction. However, pili preparations of the Aro-5 strain had greatly diminished conductivity and Aro-5 cultures were severely limited in their capacity to reduce Fe(III) compared to the control strain. Current production of the Aro-5 strain, with a graphite anode serving as the electron acceptor, was less than 10% of that of the control strain. The conductivity of the Aro-5 biofilms was 10-fold lower than the control strain's. These results demonstrate that the pili of G. sulfurreducens must be conductive in order for the cells to be effective in extracellular long-range electron transport.ImportanceExtracellular electron transfer by Geobacter species plays an important role in the biogeochemistry of soils and sediments and has a number of bioenergy applications. For example, microbial reduction of Fe(III) oxide is one of the most geochemically significant processes in anaerobic soils, aquatic sediments, and aquifers, and Geobacter organisms are often abundant in such environments. Geobacter sulfurreducens produces the highest current densities of any known pure culture, and close relatives are often the most abundant organisms colonizing anodes in microbial fuel cells that harvest electricity from wastewater or aquatic sediments. The finding that a strain of G. sulfurreducens that produces pili with low conductivity is limited in these extracellular electron transport functions provides further insight into these environmentally significant processes.

Project description:Studies on the mechanisms for extracellular electron transfer in Geobacter species have primarily focused on Geobacter sulfurreducens, but the poor conservation of genes for some electron transfer components within the Geobacter genus suggests that there may be a diversity of extracellular electron transport strategies among Geobacter species. Examination of the gene sequences for PilA, the type IV pilus monomer, in Geobacter species revealed that the PilA sequence of Geobacter uraniireducens was much longer than that of G. sulfurreducens. This is of interest because it has been proposed that the relatively short PilA sequence of G. sulfurreducens is an important feature conferring conductivity to G. sulfurreducens pili. In order to investigate the properties of the G. uraniireducens pili in more detail, a strain of G. sulfurreducens that expressed pili comprised the PilA of G. uraniireducens was constructed. This strain, designated strain GUP, produced abundant pili, but generated low current densities and reduced Fe(III) very poorly. At pH 7, the conductivity of the G. uraniireducens pili was 3 × 10(-4) S/cm, much lower than the previously reported 5 × 10(-2) S/cm conductivity of G. sulfurreducens pili at the same pH. Consideration of the likely voltage difference across pili during Fe(III) oxide reduction suggested that G. sulfurreducens pili can readily accommodate maximum reported rates of respiration, but that G. uraniireducens pili are not sufficiently conductive to be an effective mediator of long-range electron transfer. In contrast to G. sulfurreducens and G. metallireducens, which require direct contact with Fe(III) oxides in order to reduce them, G. uraniireducens reduced Fe(III) oxides occluded within microporous beads, demonstrating that G. uraniireducens produces a soluble electron shuttle to facilitate Fe(III) oxide reduction. The results demonstrate that Geobacter species may differ substantially in their mechanisms for long-range electron transport and that it is important to have information beyond a phylogenetic affiliation in order to make conclusions about the mechanisms by which Geobacter species are transferring electrons to extracellular electron acceptors.

Project description:Geobacter sulfurreducens is commonly employed as a model for the study of extracellular electron transport mechanisms in the Geobacter species. Deletion of pilB, which is known to encode the pilus assembly motor protein for type IV pili in other bacteria, has been proposed as an effective strategy for evaluating the role of electrically conductive pili (e-pili) in G. sulfurreducens extracellular electron transfer. In those studies, the inhibition of e-pili expression associated with pilB deletion was not demonstrated directly but was inferred from the observation that pilB deletion mutants produced lower current densities than wild-type cells. Here, we report that deleting pilB did not diminish current production. Conducting probe atomic force microscopy revealed filaments with the same diameter and similar current-voltage response as e-pili harvested from wild-type G. sulfurreducens or when e-pili are expressed heterologously from the G. sulfurreducens pilin gene in Escherichia coli. Immunogold labeling demonstrated that a G. sulfurreducens strain expressing a pilin monomer with a His tag continued to express His tag-labeled filaments when pilB was deleted. These results suggest that a reinterpretation of the results of previous studies on G. sulfurreducens pilB deletion strains may be necessary. IMPORTANCE Geobacter sulfurreducens is a model microbe for the study of biogeochemically and technologically significant processes, such as the reduction of Fe(III) oxides in soils and sediments, bioelectrochemical applications that produce electric current from waste organic matter or drive useful processes with the consumption of renewable electricity, direct interspecies electron transfer in anaerobic digestors and methanogenic soils and sediments, and metal corrosion. Elucidating the phenotypes associated with gene deletions is an important strategy for determining the mechanisms for extracellular electron transfer in G. sulfurreducens. The results reported here demonstrate that we cannot replicate the key phenotype reported for a gene deletion that has been central to the development of models for long-range electron transport in G. sulfurreducens.

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Low Energy Atomic Models Suggesting a Pilus Structure that could Account for Electrical Conductivity of Geobacter sulfurreducens Pili.

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Low Energy Atomic Models Suggesting a Pilus Structure that could Account for Electrical Conductivity of Geobacter sulfurreducens Pili.

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