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 The Archaellum ofMethanospirillum hungateiIs Electrically Conductive

mBio ◽  
2019 ◽  
Vol 10 (2) ◽  
Author(s):  
David J. F. Walker ◽  
Eric Martz ◽  
Dawn E. Holmes ◽  
Zimu Zhou ◽  
Stephen S. Nonnenmann ◽  
...  
Keyword(s):  
Electron Transfer ◽  
Long Range ◽  
Electronic Materials ◽  
Protein Structures ◽  
Surface Protein ◽  
Major Advance ◽  
Electrically Conductive ◽  
Anaerobic Digesters ◽  
Content Type ◽  
Potential Applications

ABSTRACTMicrobially produced electrically conductive protein filaments are of interest because they can function as conduits for long-range biological electron transfer. They also show promise as sustainably produced electronic materials. Until now, microbially produced conductive protein filaments have been reported only for bacteria. We report here that the archaellum ofMethanospirillum hungateiis electrically conductive. This is the first demonstration that electrically conductive protein filaments have evolved inArchaea. Furthermore, the structure of theM. hungateiarchaellum was previously determined (N. Poweleit, P. Ge, H. N. Nguyen, R. R. O. Loo, et al., Nat Microbiol 2:16222, 2016,https://doi.org/10.1038/nmicrobiol.2016.222). Thus, the archaellum ofM. hungateiis the first microbially produced electrically conductive protein filament for which a structure is known. We analyzed the previously published structure and identified a core of tightly packed phenylalanines that is one likely route for electron conductance. The availability of theM. hungateiarchaellum structure is expected to substantially advance mechanistic evaluation of long-range electron transport in microbially produced electrically conductive filaments and to aid in the design of “green” electronic materials that can be microbially produced with renewable feedstocks.IMPORTANCEMicrobially produced electrically conductive protein filaments are a revolutionary, sustainably produced, electronic material with broad potential applications. The design of new protein nanowires based on the knownM. hungateiarchaellum structure could be a major advance over the current empirical design of synthetic protein nanowires from electrically conductive bacterial pili. An understanding of the diversity of outer-surface protein structures capable of electron transfer is important for developing models for microbial electrical communication with other cells and minerals in natural anaerobic environments. Extracellular electron exchange is also essential in engineered environments such as bioelectrochemical devices and anaerobic digesters converting wastes to methane. The finding that the archaellum ofM. hungateiis electrically conductive suggests that some archaea might be able to make long-range electrical connections with their external environment.

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.

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 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 Molecular Dissection of Bacterial Nanowires

mBio ◽  
2013 ◽  
Vol 4 (3) ◽  
Author(s):  
Thomas Boesen ◽  
Lars Peter Nielsen
Keyword(s):  
Conclusive Evidence ◽  
Geobacter Sulfurreducens ◽  
Electron Conduction ◽  
Content Type ◽  
Type Iv ◽  
Pilin Subunit ◽  
Type Iv Pilin ◽  
Final Electron ◽  
Conductive Properties ◽  
Final Electron Acceptor

ABSTRACTThe discovery of bacterial conductive structures, termed nanowires, has intrigued scientists for almost a decade. Nanowires enable bacteria to transfer electrons over micrometer distances to extracellular electron acceptors such as insoluble metal oxides or electrodes. Nanowires are pilus based and inGeobacter sulfurreducensare composed of the type IV pilin subunit PilA. Multihemec-type cytochromes have been shown to attach to nanowire pili. Two hypotheses have been proposed for electron conduction in nanowires. The first (termed the metal-like conductivity or MLC hypothesis) claims that the pilus itself has the electron-conductive properties and the attached cytochromes mediate transfer to the final electron acceptor, whereas the second hypothesis (termed the superexchange conductivity or SEC hypothesis) suggests that electrons are “hopping” between heme groups in cytochromes closely aligned with the pilus as a scaffold. In their recent article inmBio, Vargas et al. [M. Vargas, N. S. Malvankar, P.-L. Tremblay, C. Leang, J. A. Smith, P. Patel, O. Snoeyenbos-West, K. P. Nevin, and D. R. Lovley, mBio 4(2):e00210-13, 2013] address this ambiguity through an analysis of strain Aro-5, aG. sulfurreducensPilA mutant lacking aromatic residues in the nonconserved portion of PilA. These residues were suspected of involvement in electron transport according to the MLC hypothesis. TheG. sulfurreducensmutant had reduced conductive properties, lending important support to the MLC hypothesis. The data also highlight the need for further and more conclusive evidence for one or the other hypothesis.

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 The Archaellum of Methanospirillum hungatei is Electrically Conductive

2018 ◽  
Author(s):  
David J.F. Walker ◽  
Eric Martz ◽  
Dawn E. Holmes ◽  
Zimu Zhou ◽  
Stephen S. Nonnenmann ◽  
...  
Keyword(s):  
Electron Transport ◽  
Long Range ◽  
Electrically Conductive ◽  
Methanospirillum Hungatei

Here we report that the archaellum of Methanospirillum hungatei is electrically conductive. Our analysis of the previously published archaellum structure suggests that a core of tightly packed phenylalanines is one likely route for electron conductance. This is the first demonstration that electrically conductive protein filaments (e-PFs) have evolved in Archaea and is the first e-PF for which a structure is known, facilitating mechanistic evaluation of long-range electron transport in e-PFs.

scholarly journals Relatedness of type IV pilin PilA amongst geographically diverse Moraxella bovoculi isolated from cattle with infectious bovine keratoconjunctivitis

2021 ◽  
Author(s):  
John A. Angelos ◽  
Kristin A. Clothier ◽  
Regina L. Agulto ◽  
Boguslav Mandzyuk ◽  
Morten Tryland
Keyword(s):  
Amino Acid ◽  
Type Species ◽  
Amino Acid Sequences ◽  
Similar Degree ◽  
Content Type ◽  
Infectious Bovine Keratoconjunctivitis ◽  
Link Type ◽  
Type Iv ◽  
Type Iv Pilin ◽  
Moraxella Bovoculi

Introduction. Moraxella bovoculi is frequently isolated from the eyes of cattle with infectious bovine keratoconjunctivitis (IBK; pinkeye). As with M. bovis, which has been causally linked to IBK, M. bovoculi expresses an RTX (repeats in the structural toxin) cytotoxin that is related to M. bovis cytotoxin. Pilin, another pathogenic factor in M. bovis , is required for corneal attachment. Seven antigenically distinct pilin serogroups have been described in M. bovis . Hypothesis/Gap Statement. Multiple different serogroups exist amongst type IV pilin encoded by M. bovis , however, it is not known whether M. bovoculi exhibits a similar degree of diversity in type IV pilin that it encodes. Aim. This study was done to characterize a structural pilin (PilA) encoded by M. bovoculi isolated from cases of IBK to determine if diversity exists amongst PilA sequences. Methodology. Ninety-four isolates of M. bovoculi collected between 2002 and 2017 from 23 counties throughout California and from five counties in four other Western states were evaluated. Results. DNA sequencing and determination of deduced amino acid sequences revealed ten (designated groups A through J) unique PilA sequences that were ~96.1–99.3 % identical. Pilin groups A and C matched previously reported putative PilA sequences from M. bovoculi isolated from IBK-affected cattle in the USA (Virginia, Nebraska, and Kansas) and Asia (Kazakhstan). The ten pilin sequences identified were only ~74–76 % identical to deduced amino acid sequences of putative pilin proteins identified from the previously reported whole-genome sequences of M. bovoculi derived from deep nasopharyngeal swabs of IBK-asymptomatic cattle. Conclusions. Compared to the diversity reported between structural pilin proteins amongst different serogroups of M. bovis , M. bovoculi PilA from geographically diverse isolates derived from IBK-affected cattle are more conserved.

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 Expression of a Clostridium perfringens Type IV Pilin by Neisseria gonorrhoeae Mediates Adherence to Muscle Cells

2011 ◽  
Vol 79 (8) ◽  
pp. 3096-3105 ◽  
Author(s):  
Katherine Rodgers ◽  
Cindy Grove Arvidson ◽  
Stephen Melville
Keyword(s):  
Neisseria Gonorrhoeae ◽  
Clostridium Perfringens ◽  
Klebsiella Oxytoca ◽  
Wild Type ◽  
Unique Type ◽  
Gram Negative ◽  
Content Type ◽  
Type Iv ◽  
Type Iv Pilin

ABSTRACTClostridium perfringensis an anaerobic, Gram-positive bacterium that causes a range of diseases in humans, including lethal gas gangrene. We have recently shown that strains ofC. perfringensmove across the surface of agar plates by a unique type IV pilus (TFP)-mediated social motility that had not been previously described. Based on sequence homology to pilins in Gram-negative bacteria,C. perfringensappears to have two pilin subunits, PilA1 and PilA2. Structural prediction analysis indicated PilA1 is similar to the pseudopilin found inKlebsiella oxytoca, while PilA2 is more similar to true pilins found in the Gram-negative pathogensPseudomonas aeruginosaandNeisseria gonorrhoeae. Strains ofN. gonorrhoeaethat were genetically deficient in the native pilin, PilE, but supplemented with inducible expression of PilA1 and PilA2 ofC. perfringenswere constructed. Genetic competence, wild-type twitching motility, and attachment to human urogenital epithelial cells were not restored by expression of either pilin. However, attachment to mouse and rat myoblast (muscle) cell lines was observed with theN. gonorrhoeaestrain expressing PilA2. Significantly, wild-typeC. perfringenscells adhered to mouse myoblasts under anaerobic conditions, and adherence was 10-fold lower in apilTmutant that lacked functional TFP. These findings implicateC. perfringensTFP in the ability ofC. perfringensto adhere to and move along muscle fibersin vivo, which may provide a therapeutic approach to limiting this rapidly spreading and highly lethal infection.

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