Electron transport through electrically conductive nanofilaments in Rhodopseudomonas palustris strain RP2

Venkidusamy, Krishnaveni; Megharaj, Mallavarapu; Schröder, Uwe; Karouta, F.; Mohan, S. Venkata; Naidu, Ravi

doi:10.1039/c5ra08742b

Cited by 44 publications

(40 citation statements)

References 40 publications

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“…5A) but were still orders of magnitude lower than the conductivity of the G. metallireducens pili. Rhodopseudomonas palustris filaments of unknown composition that are thought to be involved in extracellular electron transfer (30) had much lower conductivities (0.053 S/cm), but these filaments were also chemically fixed and dried, which may have affected their conductivity.…”

Section: Resultsmentioning

confidence: 99%

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

Tan

Adhikari

Malvankar

et al. 2017

mBio

139

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The electrically conductive pili (e-pili) of Geobacter sulfurreducens serve as a model for a novel strategy for long-range extracellular electron transfer. e-pili are also a new class of bioelectronic materials. However, the only other Geobacter pili previously studied, which were from G. uraniireducens, were poorly conductive. In order to obtain more information on the range of pili conductivities in Geobacter species, the pili of G. metallireducens were investigated. Heterologously expressing the PilA gene of G. metallireducens in G. sulfurreducens yielded a G. sulfurreducens strain, designated strain MP, that produced abundant pili. Strain MP exhibited phenotypes consistent with the presence of e-pili, such as high rates of Fe(III) oxide reduction and high current densities on graphite anodes. Individual pili prepared at physiologically relevant pH 7 had conductivities of 277 ± 18.9 S/cm (mean ± standard deviation), which is 5,000-fold higher than the conductivity of G. sulfurreducens pili at pH 7 and nearly 1 million-fold higher than the conductivity of G. uraniireducens pili at the same pH. A potential explanation for the higher conductivity of the G. metallireducens pili is their greater density of aromatic amino acids, which are known to be important components in electron transport along the length of the pilus. The G. metallireducens pili represent the most highly conductive pili found to date and suggest strategies for designing synthetic pili with even higher conductivities.

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Section: Resultsmentioning

confidence: 99%

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

Tan

Adhikari

Malvankar

et al. 2017

mBio

139

140

View full text Add to dashboard Cite

show abstract

“…For example, the 300 μS/cm conductivity of the G. uraniireducens pili is probably too low to support extracellular respiration. Yet Rhodopseudomonas palustris filaments of unknown composition implicated in Fe(III) oxide reduction had electrical resistances that correspond to conductivities of only 35–72 μS/cm (Supplementary Equation S2 ; Venkidusamy et al, 2015 ). However, the R. palustris filaments were chemically fixed and critical point dried prior to the conductivity measurements, which may have altered the filament structure and conductivity.…”

Section: Resultsmentioning

confidence: 99%

The Low Conductivity of Geobacter uraniireducens Pili Suggests a Diversity of Extracellular Electron Transfer Mechanisms in the Genus Geobacter

et al. 2016

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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.

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“…Diverse microorganisms such as Aeromonas hydrophila (Castro et al, 2013), Acidithiobacillus ferroxidans (Li and Li, 2014), Desulfovibrio desulfuricans (Eaktasang et al, 2016) and Rhodopseudomonas palustris (Venkidusamy et al, 2015) can produce electrically conductive protein filaments. However, uncertainties about the physiological roles of these filaments exist because of the following: (1) the protein composition of the filaments has not been determined;…”

Section: Discussionmentioning

confidence: 99%

Electrically conductive pili from pilin genes of phylogenetically diverse microorganisms

et al. 2017

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The possibility that bacteria other than Geobacter species might contain genes for electrically conductive pili (e-pili) was investigated by heterologously expressing pilin genes of interest in Geobacter sulfurreducens. Strains of G. sulfurreducens producing high current densities, which are only possible with e-pili, were obtained with pilin genes from Flexistipes sinusarabici, Calditerrivibrio nitroreducens and Desulfurivibrio alkaliphilus. The conductance of pili from these strains was comparable to native G. sulfurreducens e-pili. The e-pili derived from C. nitroreducens, and D. alkaliphilus pilin genes are the first examples of relatively long (>100 amino acids) pilin monomers assembling into e-pili. The pilin gene from Candidatus Desulfofervidus auxilii did not yield e-pili, suggesting that the hypothesis that this sulfate reducer wires itself with e-pili to methane-oxidizing archaea to enable anaerobic methane oxidation should be reevaluated. A high density of aromatic amino acids and a lack of substantial aromatic-free gaps along the length of long pilins may be important characteristics leading to e-pili. This study demonstrates a simple method to screen pilin genes from difficult-to-culture microorganisms for their potential to yield e-pili; reveals new sources for biologically based electronic materials; and suggests that a wide phylogenetic diversity of microorganisms may use e-pili for extracellular electron exchange.

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Electron transport through electrically conductive nanofilaments in Rhodopseudomonas palustris strain RP2

Cited by 44 publications

References 40 publications

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

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

The Low Conductivity of Geobacter uraniireducens Pili Suggests a Diversity of Extracellular Electron Transfer Mechanisms in the Genus Geobacter

Electrically conductive pili from pilin genes of phylogenetically diverse microorganisms

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