scholarly journals Direct Observation of Electrically Conductive Pili Emanating from Geobacter sulfurreducens

2021 ◽  
Author(s):  
Xinying Liu ◽  
David Jeffrey Fraser Walker ◽  
Stephen Nonnenmann ◽  
Dezhi Sun ◽  
Derek R. Lovley
Keyword(s):  
Electron Transfer ◽  
Electron Transport ◽  
Long Range ◽  
Geobacter Sulfurreducens ◽  
Metal Corrosion ◽  
Extracellular Electron Transfer ◽  
Wild Type ◽  
Electrically Conductive ◽  
In The Wild ◽  
Pilin Gene

Geobacter sulfurreducens is a model microbe for elucidating the mechanisms for extracellular electron transfer in several biogeochemical cycles, bioelectrochemical applications, and microbial metal corrosion. Multiple lines of evidence previously suggested that electrically conductive pili (e-pili) are an essential conduit for long-range extracellular electron transport in G. sulfurreducens. However, it has recently been reported that G. sulfurreducens does not express e-pili and that filaments comprised of multi-heme c-type cytochromes are responsible for long-range electron transport. This possibility was directly investigated by examining cells, rather than filament preparations, with atomic force microscopy. Approximately 90 % of the filaments emanating from wild-type cells had a diameter (3 nm) and conductance consistent with previous reports of e-pili harvested from G. sulfurreducens or heterologously expressed in E. coli from the G. sulfurreducens pilin gene. The remaining 10% of filaments had a morphology consistent with filaments comprised of the c-type cytochrome OmcS. A strain expressing a modified pilin gene designed to yield poorly conductive pili expressed 90 % filaments with a 3 nm diameter, but greatly reduced conductance, further indicating that the 3 nm diameter conductive filaments in the wild-type strain were e-pili. A strain in which genes for five of the most abundant outer-surface c-type cytochromes, including OmcS, was deleted yielded only 3 nm diameter filaments with the same conductance as in the wild-type. These results demonstrate that e-pili are the most abundant conductive filaments expressed by G. sulfurreducens, consistent with previous functional studies demonstrating the need for e-pili for long-range extracellular electron transfer.

scholarly journals Improper Localization of the OmcS Cytochrome May Explain the Inability of thexapD-Deficient Mutant ofGeobacter sulfurreducensto Reduce Fe(III) Oxide

2017 ◽  
Author(s):  
Kelly A. Flanagan ◽  
Ching Leang ◽  
Joy E. Ward ◽  
Derek R. Lovley
Keyword(s):  
Electron Transfer ◽  
Electron Transport ◽  
Type Strain ◽  
Wild Type Strain ◽  
Geobacter Sulfurreducens ◽  
Extracellular Electron Transfer ◽  
Outer Cell ◽  
Wild Type ◽  
Redox Active ◽  
In The Wild

AbstractExtracellular electron transfer through a redox-active exopolysaccharide matrix has been proposed as a strategy for extracellular electron transfer to Fe(III) oxide byGeobacter sulfurreducens,based on the phenotype of axapD-deficient strain. Central to this model was the assertion that thexapD-deficient strain produced pili decorated with the multi-hemec-type cytochrome OmcS in manner similar to the wild-type strain. Further examination of thexapD-deficient strain with immunogold labeling of OmcS and transmission electron microscopy revealed that OmcS was associated with the outer cell surface rather than pili. PilA, the pilus monomer, could not be detected in thexapD-deficient strain under conditions in which it was readily detected in the wild-type strain. Multiple lines of evidence in previous studies have suggested that long-range electron transport to Fe(III) oxides proceeds through electrically conductive pili and that OmcS associated with the pili is necessary for electron transfer from the pili to Fe(III) oxides. Therefore, an alternative explanation for the Fe(III) oxide reduction phenotype of thexapD-deficientstrain is that the pili-OmcS route for extracellular electron transport to Fe(III) oxide has been disrupted in thexapD-deficient strain.

scholarly journals Cytochrome OmcS is not essential for long-range electron transport in Geobacter sulfurreducens strain KN400

2020 ◽  
Author(s):  
David J. F. Walker ◽  
Yang Li ◽  
David Meier ◽  
Samantha Pinches ◽  
Dawn E. Holmes ◽  
...  
Keyword(s):  
Electron Transfer ◽  
Electron Transport ◽  
Long Range ◽  
Geobacter Sulfurreducens ◽  
Extracellular Electron Transfer ◽  
Electrically Conductive ◽  
Closely Related Species ◽  
Direct Interspecies Electron Transfer ◽  
Interspecies Electron Transfer ◽  
Extracellular Electron Transport

AbstractThe multi-heme c-type cytochrome OmcS, is one of the central components for extracellular electron transport in Geobacter sulfurreducens strain DL-1, but its role in other microbes, including other strains of G. sulfurreducens is currently a matter of debate. Therefore, we investigated the function of OmcS in G. sulfurreducens strain KN400, which is even more effective in extracellular electron transfer than strain DL-1. We found that deleting omcS from strain KN400 did not negatively impact the rate of Fe(III) oxide reduction and did not affect the strain’s ability to accept electrons via direct interspecies electron transfer. The OmcS-deficient strain also continued to produce conductive filaments, consistent with the concept that electrically conductive pili are the primary conduit for long-range electron transfer in G. sulfurreducens and closely related species. These findings, coupled with the lack of OmcS homologs in most other microbes capable of extracellular electron transfer, suggest that OmcS is not a common critical component for extracellular electron transfer.

scholarly journals The electrically conductive pili of Geobacter soli

2020 ◽  
Author(s):  
Shiyan Zhuo ◽  
Guiqin Yang ◽  
Li Zhuang
Keyword(s):  
Electron Transfer ◽  
Outer Surface ◽  
Electronic Materials ◽  
Geobacter Sulfurreducens ◽  
Extracellular Electron Transfer ◽  
Oxide Reduction ◽  
Electrically Conductive ◽  
Current Production ◽  
Current Densities ◽  
Pilin Gene

AbstractElectrically conductive pili (e-pili) enable electron transport over multiple cell lengths to extracellular environments and play an important role in extracellular electron transfer (EET) of Geobacter species. To date, the studies of e-pili have mainly focused on Geobacter sulfurreducens and the closely related Geobacter metallireducens because of their developed genetic manipulation systems. We investigated the role of G. soli pili in EET by directly deleting the pilin gene, pilA, which is predicted to encode e-pili. Deletion of pilA, prevented the production of pili, resulting in poor Fe(III) oxide reduction and low current production, implying that G. soli pili is required for EET. To further evaluate the conductivity of G. soli pili compared with G. sulfurreducens pili, the pilA of G. soli was heterologously expressed in G. sulfurreducens, yielding the G. sulfurreducens strain GSP. This strain produced abundant pili with similar conductivity to the control strain that expressed native G. sulfurreducens pili, consistent with G. soli as determined by direct measurement, which suggested that G. soli pili is electrically conductive. Surprisingly, strain GSP was deficient in Fe(III) oxide reduction and current production due to the impaired content of outer-surface c-type cytochromes. These results demonstrated that heterologous pili of G. sulfurreducens severely reduces the content of outer-surface c-type cytochromes and consequently eliminates the capacity for EET, which strongly suggests an attention should be paid to the content of c-type cytochromes when employing G. sulfurreducens to heterologously express pili from other microorganisms.IMPORTANCEThe studies of electrically conductive pili (e-pili) of Geobacter species are of interest because of its application prospects in electronic materials. e-Pili are considered a substitution for electronic materials due to its renewability, biodegradability and robustness. Continued exploration of additional e-pili of Geobacter soli will improve the understanding of their biological role in extracellular electron transfer and expand the range of available electronic materials. Heterologously expressing the pilin genes from phylogenetically diverse microorganisms has been proposed as an emerging approach to screen potential e-pili according to high current densities. However, our results indicated that a Geobacter sulfurreducens strain heterologously expressing a pilin gene produced low current densities that resulted from a lack of content of c-type cytochromes, which were likely to possess e-pili. These results provide referential significance to yield e-pili from diverse microorganisms.

Long-range electron transport to Fe(III) oxide via pili with metallic-like conductivity

2012 ◽  
Vol 40 (6) ◽  
pp. 1186-1190 ◽  
Author(s):  
Derek R. Lovley
Keyword(s):  
Electron Transport ◽  
Long Range ◽  
Geobacter Sulfurreducens ◽  
Oxide Reduction ◽  
Electron Hopping ◽  
Electrically Conductive ◽  
Electron Conduction ◽  
Geobacter Species ◽  
Redox Active

The mechanisms for Fe(III) oxide reduction by Geobacter species are of interest because Geobacter species have been shown to play an important role in Fe(III) oxide reduction in a diversity of environments in which Fe(III) reduction is a geochemically significant process. Geobacter species specifically express pili during growth on Fe(III) oxide compared with growth on soluble chelated Fe(III), and mutants that cannot produce pili are unable to effectively reduce Fe(III) oxide. The pili of Geobacter sulfurreducens are electrically conductive along their length under physiologically relevant conditions and exhibit a metallic-like conductivity similar to that observed previously in synthetic organic metals. Metallic-like conductivity in a biological protein filament is a previously unrecognized mechanism for electron transport that differs significantly from the more well-known biological strategy of electron hopping/tunnelling between closely spaced redox-active proteins. The multihaem c-type cytochrome OmcS is specifically associated with pili and is necessary for Fe(III) oxide reduction. However, multiple lines of evidence, including the metallic-like conductivity of the pili and the fact that OmcS molecules are spaced too far apart for electron hopping/tunnelling, indicate that OmcS is not responsible for long-range electron conduction along the pili. The role of OmcS may be to facilitate electron transfer from the pili to Fe(III) oxide. Long-range electron transport via pili with metallic-like conductivity is a paradigm shift that has important implications not only for Fe(III) oxide reduction, but also for interspecies electron exchange in syntrophic microbial communities as well as microbe–electrode interactions and the emerging field of bioelectronics.

scholarly journals Direct Observation of Electrically Conductive Pili Emanating from Geobacter sulfurreducens

mBio ◽  
2021 ◽  
Vol 12 (4) ◽  
Author(s):  
Xinying Liu ◽  
David J. F. Walker ◽  
Stephen S. Nonnenmann ◽  
Dezhi Sun ◽  
Derek R. Lovley
Keyword(s):  
Electron Transport ◽  
Environmental Impacts ◽  
Long Range ◽  
Direct Observation ◽  
Geobacter Sulfurreducens ◽  
Electrically Conductive ◽  
Metal Cofactors

Electroactive microbes have significant environmental impacts, as well as applications in bioenergy and bioremediation. The composition, function, and even existence of electrically conductive pili (e-pili) has been one of the most contentious areas of investigation in electromicrobiology, in part because e-pili offer a mechanism for long-range electron transport that does not involve the metal cofactors common in much of biological electron transport.

scholarly journals Generation of High Current Densities in Geobacter sulfurreducens Lacking the Putative Gene for the PilB Pilus Assembly Motor

2021 ◽  
Author(s):  
Toshiyuki Ueki ◽  
David J. F. Walker ◽  
Kelly P. Nevin ◽  
Joy E. Ward ◽  
Trevor L. Woodard ◽  
...  
Keyword(s):  
Electron Transfer ◽  
Geobacter Sulfurreducens ◽  
Metal Corrosion ◽  
Extracellular Electron Transfer ◽  
Renewable Electricity ◽  
Gene Deletions ◽  
Putative Gene ◽  
Content Type ◽  
Soils And Sediments ◽  
Current Densities

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 .

scholarly journals Cytochromes in extracellular electron transfer in Geobacter

2021 ◽  
Author(s):  
Toshiyuki Ueki
Keyword(s):  
Electron Transfer ◽  
Critical Role ◽  
Geobacter Sulfurreducens ◽  
Electron Donors ◽  
Metal Corrosion ◽  
Extracellular Electron Transfer ◽  
Natural Environments ◽  
Anaerobic Digesters ◽  
Oxidation Reduction ◽  
Cellular Components

Extracellular electron transfer (EET) is an important biological process in microbial physiology as found in dissimilatory metal oxidation/reduction and interspecies electron transfer in syntrophy in natural environments. EET also plays a critical role in microorganisms relevant to environmental biotechnology in metal-contaminated areas, metal corrosion, bioelectrochemical systems, and anaerobic digesters. Geobacter species exist in a diversity of natural and artificial environments. One of the outstanding features of Geobacter species is the capability of direct EET with solid electron donors and acceptors including metals, electrodes, and other cells. Therefore, Geobacter species are pivotal in environmental biogeochemical cycles and biotechnology applications. Geobacter sulfurreducens, a representative Geobacter species, has been studied for the direct EET as a model microorganism. G. sulfurreducens employs electrically conductive pili (e-pili) and c-type cytochromes for the direct EET. The biological function and electronics applications of the e-pili have been reviewed recently and this review focuses on the cytochromes. Geobacter species have an unusually large number of cytochromes encoded in their genomes. Unlike most other microorganisms, Geobacter species localize multiple cytochromes in each subcellular fraction: outer membrane, periplasm, and inner membrane, as well as in the extracellular space, and differentially utilize these cytochromes for the EET with various electron donors and acceptors. Some of the cytochromes are functionally redundant. Thus, the EET in Geobacter is complicated. Geobacter coordinates the cytochromes with other cellular components in the elaborate EET system to flourish in the environment.

scholarly journals Adaptation to Disruption of the Electron Transfer Pathway for Fe(III) Reduction in Geobacter sulfurreducens

2005 ◽  
Vol 187 (17) ◽  
pp. 5918-5926 ◽  
Author(s):  
Ching Leang ◽  
L. A. Adams ◽  
K.-J. Chin ◽  
K. P. Nevin ◽  
B. A. Methé ◽  
...  
Keyword(s):  
Electron Transfer ◽  
Steady State ◽  
Electron Transport ◽  
Outer Membrane ◽  
Geobacter Sulfurreducens ◽  
Significant Shift ◽  
Deficient Mutant ◽  
Wild Type ◽  
Transcript Levels ◽  
Electron Transfer Pathway

ABSTRACT Previous studies demonstrated that an outer membrane c-type cytochrome, OmcB, was involved in Fe(III) reduction in Geobacter sulfurreducens. An OmcB-deficient mutant was greatly impaired in its ability to reduce both soluble and insoluble Fe(III). Reintroducing omcB restored the capacity for Fe(III) reduction at a level proportional to the level of OmcB production. Here, we report that the OmcB-deficient mutant gradually adapted to grow on soluble Fe(III) but not insoluble Fe(III). The adapted OmcB-deficient mutant reduced soluble Fe(III) at a rate comparable to that of the wild type, but the cell yield of the mutant was only ca. 60% of that of the wild type under steady-state culturing conditions. Analysis of proteins and transcript levels demonstrated that expression of several membrane-associated cytochromes was higher in the adapted mutant than in the wild type. Further comparison of transcript levels during steady-state growth on Fe(III) citrate with a whole-genome DNA microarray revealed a significant shift in gene expression in an apparent attempt to adapt metabolism to the impaired electron transport to Fe(III). These results demonstrate that, although there are many other membrane-bound c-type cytochromes in G. sulfurreducens, increased expression of these cytochromes cannot completely compensate for the loss of OmcB. The concept that outer membrane cytochromes are promiscuous reductases that are interchangeable in function appears to be incorrect. Furthermore, the results indicate that there may be different mechanisms for electron transfer to soluble Fe(III) and insoluble Fe(III) oxides in G. sulfurreducens, which emphasizes the importance of studying electron transport to the environmentally relevant Fe(III) oxides.

scholarly journals Long-range electron transport in Geobacter sulfurreducens biofilms is redox gradient-driven

2012 ◽  
Vol 109 (38) ◽  
pp. 15467-15472 ◽  
Author(s):  
Rachel M. Snider ◽  
Sarah M. Strycharz-Glaven ◽  
Stanislav D. Tsoi ◽  
Jeffrey S. Erickson ◽  
Leonard M. Tender
Keyword(s):  
Electron Transport ◽  
Long Range ◽  
Redox Status ◽  
Electron Source ◽  
Oxidation Potential ◽  
Geobacter Sulfurreducens ◽  
The Other ◽  
Anode Surface ◽  
Extracellular Electron Transfer ◽  
Oxidation Potentials

Geobacter spp. can acquire energy by coupling intracellular oxidation of organic matter with extracellular electron transfer to an anode (an electrode poised at a metabolically oxidizing potential), forming a biofilm extending many cell lengths away from the anode surface. It has been proposed that long-range electron transport in such biofilms occurs through a network of bound redox cofactors, thought to involve extracellular matrix c-type cytochromes, as occurs for polymers containing discrete redox moieties. Here, we report measurements of electron transport in actively respiring Geobacter sulfurreducens wild type biofilms using interdigitated microelectrode arrays. Measurements when one electrode is used as an anode and the other electrode is used to monitor redox status of the biofilm 15 μm away indicate the presence of an intrabiofilm redox gradient, in which the concentration of electrons residing within the proposed redox cofactor network is higher farther from the anode surface. The magnitude of the redox gradient seems to correlate with current, which is consistent with electron transport from cells in the biofilm to the anode, where electrons effectively diffuse from areas of high to low concentration, hopping between redox cofactors. Comparison with gate measurements, when one electrode is used as an electron source and the other electrode is used as an electron drain, suggests that there are multiple types of redox cofactors in Geobacter biofilms spanning a range in oxidation potential that can engage in electron transport. The majority of these redox cofactors, however, seem to have oxidation potentials too negative to be involved in electron transport when acetate is the electron source.

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