Direct Extracellular Electron Transfer of the Geobacter sulfurreducens Pili Relevant to Interaromatic Distances

Microorganisms can transfer electrons directly to extracellular acceptors, during which organic compounds are oxidized to carbon dioxide. One of these microbes, Geobacter sulfurreducens, is well known for the “metallic-like” conductivity of its type IV pili. However, there is no consensus on what the mechanism for electron transfer along these conductive pili is. Based on the aromatic distances and orientations of our predicted models, the mechanism of electron transfer in the Geobacter sulfurreducens (GS) pili was explored by quantum chemical calculations with Marcus theory of electron transfer reactions. Three aromatic residues from the N-terminal α-helix of the GS pilin subunit are packed together, resulting in a continuous pi-pi interaction chain. The theoretical conductance (4.69 μS/3.85 μS) of the predicted models is very similar to that in the experiments reported recently (3.40 μS). These findings offer a new concept that the GS pili belongs to a new class of proteins that can transport electrons through pi-pi interaction between aromatic residues and also provide a valuable tool for guiding further researches of these conductive pili, to investigate their roles in biogeochemical cycling, and potential applications in biomaterials, bioelectronics, and bioenergy.

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Cyclic voltammetry of biofilms of wild type and mutant Geobacter sulfurreducens on fuel cell anodes indicates possible roles of OmcB, OmcZ, type IV pili, and protons in extracellular electron transfer

Energy & Environmental Science ◽

10.1039/b816647a ◽

2009 ◽

Vol 2 (5) ◽

pp. 506 ◽

Cited By ~ 322

Author(s):

Hanno Richter ◽

Kelly P. Nevin ◽

Hongfei Jia ◽

Daniel A. Lowy ◽

Derek R. Lovley ◽

...

Keyword(s):

Electron Transfer ◽

Cyclic Voltammetry ◽

Fuel Cell ◽

Type Iv Pili ◽

Geobacter Sulfurreducens ◽

Extracellular Electron Transfer ◽

Wild Type ◽

Type Iv ◽

Fuel Cell Anodes

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Significance of a Posttranslational Modification of the PilA Protein of Geobacter sulfurreducens for Surface Attachment, Biofilm Formation, and Growth on Insoluble Extracellular Electron Acceptors

Journal of Bacteriology ◽

10.1128/jb.00716-16 ◽

2017 ◽

Vol 199 (8) ◽

Cited By ~ 11

Author(s):

Lubna V. Richter ◽

Ashley E. Franks ◽

Robert M. Weis ◽

Steven J. Sandler

Keyword(s):

Electron Transfer ◽

Amino Acid ◽

Posttranslational Modification ◽

Biofilm Formation ◽

Electron Acceptors ◽

Type Iv Pili ◽

Geobacter Sulfurreducens ◽

Surface Attachment ◽

Content Type ◽

Type Iv

ABSTRACT Geobacter sulfurreducens, an anaerobic metal-reducing bacterium, possesses type IV pili. These pili are intrinsic structural elements in biofilm formation and, together with a number of c-type cytochromes, are thought to serve as conductive nanowires enabling long-range electron transfer (ET) to metal oxides and graphite anodes. Here, we report that a posttranslational modification of a nonconserved amino acid residue within the PilA protein, the structural subunit of the type IV pili, is crucial for growth on insoluble extracellular electron acceptors. Matrix-assisted laser desorption ionization (MALDI) mass spectrometry of the secreted PilA protein revealed a posttranslational modification of tyrosine-32 with a moiety of a mass consistent with a glycerophosphate group. Mutating this tyrosine into a phenylalanine inhibited cell growth with Fe(III) oxides as the sole electron acceptor. In addition, this amino acid substitution severely diminished biofilm formation on graphite surfaces and impaired current output in microbial fuel cells. These results demonstrate that the capability to attach to insoluble electron acceptors plays a crucial role for the cells' ability to utilize them. The work suggests that glycerophosphate modification of Y32 is a key factor contributing to the surface charge of type IV pili, influencing the adhesion of Geobacter to specific surfaces. IMPORTANCE Type IV pili are bacterial appendages that function in cell adhesion, virulence, twitching motility, and long-range electron transfer (ET) from bacterial cells to insoluble extracellular electron acceptors. The mechanism and role of type IV pili for ET in Geobacter sulfurreducens is still a subject of research. In this study, we identified a posttranslational modification of the major G. sulfurreducens type IV pilin, suggested to be a glycerophosphate moiety. We show that a mutant in which the glycerophosphate-modified tyrosine-32 is replaced with a phenylalanine has reduced abilities for ET and biofilm formation compared with those of the wild type. The results show the importance of the glycerophosphate-modified tyrosine for surface attachment and electron transfer in electrode- or Fe(III)-respiring G. sulfurreducens cells.

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Phylogenetic and structural diversity of aromatically dense pili from environmental metagenomes

10.1101/668343 ◽

2019 ◽

Author(s):

M. S. Bray ◽

J. Wu ◽

C.C. Padilla ◽

F. J. Stewart ◽

D. A. Fowle ◽

...

Keyword(s):

Amino Acids ◽

Electron Transfer ◽

Microbial Respiration ◽

Aromatic Amino Acids ◽

Structural Diversity ◽

Type Iv Pili ◽

Extracellular Electron Transfer ◽

Environmental Distribution ◽

Type Iv ◽

Genes Encoding

SummaryElectroactive type IV pili, or e-pili, are used by some microbial species for extracellular electron transfer. Recent studies suggest that e-pili may be more phylogenetically and structurally diverse than previously assumed. Here, we used updated aromatic density thresholds (≥9.8% aromatic amino acids, ≤22-aa aromatic gaps, and aromatic amino acids at residues 1, 24, 27, 50 and/or 51, and 32 and/or 57) to search for putative e-pilin genes in metagenomes from diverse ecosystems with active microbial metal cycling. Environmental putative e-pilins were diverse in length and phylogeny, and included truncated e-pilins inGeobacterspp., as well as longer putative e-pilins in Fe(II)-oxidizingBetaproteobacteriaandZetaproteobacteria.Originality and SignificanceElectroactive pili (e-pili) are used by microorganisms to respire solid metals in their environment through extracellular electron transfer. Thus, e-pili enable microbes to occupy specific environmental niches. Additionally, e-pili have important potential for biotechnological applications. Currently the repertoire of known e-pili is small, and their environmental distribution is largely unknown. Using sequence analysis, we identified numerous genes encoding putative e-pili from diverse anoxic, metal-rich ecosystems. Our results expand the diversity of putative e-pili in environments where metal oxides may be important electron acceptors for microbial respiration.

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