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.

Thermally activated long range electron transport in living biofilms

2015 ◽  
Vol 17 (48) ◽  
pp. 32564-32570 ◽  
Author(s):  
Matthew D. Yates ◽  
Joel P. Golden ◽  
Jared Roy ◽  
Sarah M. Strycharz-Glaven ◽  
Stanislav Tsoi ◽  
...  
Keyword(s):  
Electron Transport ◽  
Long Range ◽  
Geobacter Sulfurreducens ◽  
Electron Hopping ◽  
Thermally Activated ◽  
Conductivity Electron ◽  
Extracellular Electron Transport ◽  
Conductive Surfaces

The rate of extracellular electron transport through living, electrode-grown Geobacter sulfurreducens biofilms decreases with decreasing temperature, consistent with incoherent redox conductivity (electron hopping) among hemes of c-type cytochromes to conductive surfaces.

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 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 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 Protein Nanowires: the Electrification of the Microbial World and Maybe Our Own

2020 ◽  
Vol 202 (20) ◽  
Author(s):  
Derek R. Lovley ◽  
Dawn E. Holmes
Keyword(s):  
Electron Transport ◽  
Long Range ◽  
Electronic Devices ◽  
Electricity Production ◽  
Microbial World ◽  
Electrically Conductive ◽  
Anaerobic Digesters ◽  
Content Type ◽  
Type Iv ◽  
Type Iv Pilin

ABSTRACT Electrically conductive protein nanowires appear to be widespread in the microbial world and are a revolutionary “green” material for the fabrication of electronic devices. Electrically conductive pili (e-pili) assembled from type IV pilin monomers have independently evolved multiple times in microbial history as have electrically conductive archaella (e-archaella) assembled from homologous archaellin monomers. A role for e-pili in long-range (micrometer) extracellular electron transport has been demonstrated in some microbes. The surprising finding of e-pili in syntrophic bacteria and the role of e-pili as conduits for direct interspecies electron transfer have necessitated a reassessment of routes for electron flux in important methanogenic environments, such as anaerobic digesters and terrestrial wetlands. Pilin monomers similar to those found in e-pili may also be a major building block of the conductive “cables” that transport electrons over centimeter distances through continuous filaments of cable bacteria consisting of a thousand cells or more. Protein nanowires harvested from microbes have many functional and sustainability advantages over traditional nanowire materials and have already yielded novel electronic devices for sustainable electricity production, neuromorphic memory, and sensing. e-pili can be mass produced with an Escherichia coli chassis, providing a ready source of material for electronics as well as for studies on the basic mechanisms for long-range electron transport along protein nanowires. Continued exploration is required to better understand the electrification of microbial communities with microbial nanowires and to expand the “green toolbox” of sustainable materials for wiring and powering the emerging “Internet of things.”

scholarly journals Aromatic Amino Acids Required for Pili Conductivity and Long-Range Extracellular Electron Transport in Geobacter sulfurreducens

mBio ◽  
2013 ◽  
Vol 4 (2) ◽  
Author(s):  
Madeline Vargas ◽  
Nikhil S. Malvankar ◽  
Pier-Luc Tremblay ◽  
Ching Leang ◽  
Jessica A. Smith ◽  
...  
Keyword(s):  
Amino Acids ◽  
Electron Transport ◽  
Long Range ◽  
Microbial Fuel Cells ◽  
Aromatic Amino Acids ◽  
Geobacter Sulfurreducens ◽  
Control Strain ◽  
Content Type ◽  
Current Production ◽  
Extracellular Electron Transport

ABSTRACTIt has been proposed thatGeobacter sulfurreducensrequires 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 ofG. 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 whichG. sulfurreducensPilA 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 multihemec-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 ofG. sulfurreducensmust be conductive in order for the cells to be effective in extracellular long-range electron transport.IMPORTANCEExtracellular electron transfer byGeobacterspecies 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, andGeobacterorganisms are often abundant in such environments.Geobacter sulfurreducensproduces 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 ofG. sulfurreducensthat produces pili with low conductivity is limited in these extracellular electron transport functions provides further insight into these environmentally significant processes.

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.

scholarly journals Structure of a cytochrome-based bacterial nanowire

2018 ◽  
Author(s):  
David J. Filman ◽  
Stephen F. Marino ◽  
Joy E. Ward ◽  
Lu Yang ◽  
Zoltán Mester ◽  
...  
Keyword(s):  
Electron Microscopy ◽  
Electron Transport ◽  
Long Range ◽  
Biological Significance ◽  
New Materials ◽  
Electrically Conductive ◽  
Cryo Electron Microscopy ◽  
Novel Structure ◽  
Bacterial Nanowires

AbstractElectrically conductive pili from Geobacter species, termed bacterial “nanowires”, are intensely studied for their biological significance and potential in the development of new materials. We have characterized a unique nanowire from conductive G. sulfurreducens pili preparations by cryo-electron microscopy composed solely of the c-type cytochrome OmcS. We present here, at 3.4 Å resolution, a novel structure of a cytochrome-based filament and discuss its possible role in long-range biological electron transport.Summary sentenceCryo-electron microscopy reveals the remarkable assembly of a c-type cytochrome into filaments comprising a heme-based bacterial nanowire.

scholarly journals Geobacter protein nanowires

2019 ◽  
Author(s):  
Derek R Lovley ◽  
David J F Walker
Keyword(s):  
Long Range ◽  
Growth Conditions ◽  
Laboratory Culture ◽  
Culture Conditions ◽  
Geobacter Sulfurreducens ◽  
Surface Proteins ◽  
Outer Cell ◽  
Electrically Conductive ◽  
Extracellular Transport

The study of electrically conductive protein nanowires in Geobacter sulfurreducens has led to new concepts for long-range electron extracellular transport, as well as the development of sustainable conductive materials and electronic devices with novel functions. Until recently, electrically conductive pili (e-pili), assembled from the PilA pilin monomer, were the only known Geobacter protein nanowires. However, filaments comprised of the multi-heme c-type cytochrome, OmcS, are present in some preparations of G. sulfurreducens outer-surface proteins. The purpose of this review is to evaluate the available evidence on the in vivo expression of e-pili and OmcS filaments and their biological function. Abundant literature demonstrates that G. sulfurreducens expresses e-pili, which are required for long-range electron transport to Fe(III) oxides and through conductive biofilms. In contrast, there is no definitive evidence yet that wild-type G. sulfurreducens express long filaments of OmcS extending from the cells, and deleting the gene for OmcS actually increases biofilm conductivity. The literature does not support the concern that many previous studies on e-pili were mistakenly studying OmcS filaments. For example, heterologous expression of the aromatic-rich pilin monomer of G. metallireducens in G. sulfurreducens increases the conductivity of individual nanowires more than 5000-fold, whereas expression of an aromatic-poor pilin reduced conductivity more than 1000-fold. This more than million-fold range in nanowire conductivity was achieved while maintaining the 3 nm diameter consistent with e-pili, not OmcS. Purification methods that eliminate all traces of OmcS yield highly conductive e-pili. Substantial evidence suggests that OmcS is often associated with the outer cell surface and intermittently localized along e-pili in vivo. Future studies of G. sulfurreducens expression of protein nanowires need to be cognizant of the importance of maintaining environmentally relevant growth conditions because artificial laboratory culture conditions can rapidly select against e-pili expression. Principles derived from the study of e-pili have enabled identification of non-cytochrome protein nanowires in diverse bacteria and archaea. A similar search for cytochrome appendages is warranted. Both e-pili and OmcS filaments offer design options for the synthesis of protein-based ‘green’ electronics, which may be the primary driving force for the study of these structures in the near future.

scholarly journals Outer Membrane c-Type Cytochromes Required for Fe(III) and Mn(IV) Oxide Reduction in Geobacter sulfurreducens

2005 ◽  
Vol 71 (12) ◽  
pp. 8634-8641 ◽  
Author(s):  
T. Mehta ◽  
M. V. Coppi ◽  
S. E. Childers ◽  
D. R. Lovley
Keyword(s):  
Electron Transfer ◽  
Molecular Mass ◽  
Outer Membrane ◽  
Outer Membrane Proteins ◽  
Nitrilotriacetic Acid ◽  
Geobacter Sulfurreducens ◽  
Oxide Reduction ◽  
Intact Cells ◽  
Ca 50

ABSTRACT The potential role of outer membrane proteins in electron transfer to insoluble Fe(III) oxides by Geobacter sulfurreducens was investigated because this organism is closely related to the Fe(III) oxide-reducing organisms that are predominant in many Fe(III)-reducing environments. Two of the most abundant proteins that were easily sheared from the outer surfaces of intact cells were c-type cytochromes. One, designated OmcS, has a molecular mass of ca. 50 kDa and is predicted to be an outer membrane hexaheme c-type cytochrome. Transcripts for omcS could be detected during growth on Fe(III) oxide, but not on soluble Fe(III) citrate. The omcS mRNA consisted primarily of a monocistronic transcript, and to a lesser extent, a longer transcript that also contained the downstream gene omcT, which is predicted to encode a second hexaheme outer membrane cytochrome with 62.6% amino acid sequence identity to OmcS. The other abundant c-type cytochrome sheared from the outer surface of G. sulfurreducens, designated OmcE, has a molecular mass of ca. 30 kDa and is predicted to be an outer membrane tetraheme c-type cytochrome. When either omcS or omcE was deleted, G. sulfurreducens could no longer reduce Fe(III) oxide but could still reduce soluble electron acceptors, including Fe(III) citrate. The mutants could reduce Fe(III) in Fe(III) oxide medium only if the Fe(III) chelator, nitrilotriacetic acid, or the electron shuttle, anthraquinone 2,6-disulfonate, was added. Expressing omcS or omcE in trans restored the capacity for Fe(III) oxide reduction. OmcT was not detected among the sheared proteins, and genetic studies indicated that G. sulfurreducens could not reduce Fe(III) oxide when omcT was expressed but OmcS was absent. In contrast, Fe(III) oxide was reduced when omcS was expressed in the absence of OmcT. These results suggest that OmcS and OmcE are involved in electron transfer to Fe(III) oxides in G. sulfurreducens. They also emphasize the importance of evaluating mechanisms for Fe(III) reduction with environmentally relevant Fe(III) oxide, rather than the more commonly utilized Fe(III) citrate, because additional electron transfer components are required for Fe(III) oxide reduction that are not required for Fe(III) citrate reduction.

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