Structural Basis for Metallic-Like Conductivity in Microbial Nanowires
Abstract
Direct measurement of multiple physical properties of Geobacter sulfurreducens pili have demonstrated that they possess metallic-like conductivity, but several studies have suggested that metallic-like conductivity is unlikely based on the structures of the G. sulfurreducens pilus predicted from homology models. In order to further evaluate this discrepancy, pili were examined with synchrotron X-ray microdiffraction and rocking-curve X-ray diffraction. Both techniques revealed a periodic 3.2-Å spacing in conductive, wild-type G. sulfurreducens pili that was missing in the nonconductive pili of strain Aro5, which lack key aromatic acids required for conductivity. The intensity of the 3.2-Å peak increased 100-fold when the pH was shifted from 10.5 to 2, corresponding with a previously reported 100-fold increase in pilus conductivity with this pH change. These results suggest a clear structure-function correlation for metallic-like conductivity that can be attributed to overlapping π-orbitals of aromatic amino acids. A homology model of the G. sulfurreducens pilus was constructed with a Pseudomonas aeruginosa pilus model as a template as an alternative to previous models, which were based on a Neisseria gonorrhoeae pilus structure. This alternative model predicted that aromatic amino acids in G. sulfurreducens pili are packed within 3 to 4 Å, consistent with the experimental results. Thus,more »
- Authors:
-
- Univ. of Massachusetts, Amherst, MA (United States). Dept. of Physics; Univ. of Massachusetts, Amherst, MA (United States). Dept. of Microbiology
- Univ. of Massachusetts, Amherst, MA (United States). Dept. of Microbiology; College of the Holy Cross Worcester, MA (United States). Dept. of Biology
- Univ. of Massachusetts, Amherst, MA (United States). Dept. of Microbiology
- Brookhaven National Lab. (BNL), Upton, NY (United States). Photon Sciences Directorate
- Brookhaven National Lab. (BNL), Upton, NY (United States). Center for Functional Nanomaterials (CFN)
- Univ. of Massachusetts, Amherst, MA (United States). Dept. of Physics
- Publication Date:
- Research Org.:
- Brookhaven National Laboratory (BNL), Upton, NY (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES)
- OSTI Identifier:
- 1259267
- Grant/Contract Number:
- AC02-98CH10886; N00014-13-1-0550; N00014-12-1-0229
- Resource Type:
- Journal Article: Accepted Manuscript
- Journal Name:
- mBio (Online)
- Additional Journal Information:
- Journal Volume: 6; Journal Issue: 2; Journal ID: ISSN 2150-7511
- Publisher:
- American Society for Microbiology
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 36 MATERIALS SCIENCE
Citation Formats
Malvankar, Nikhil S., Vargas, Madeline, Nevin, Kelly, Tremblay, Pier-Luc, Evans-Lutterodt, Kenneth, Nykypanchuk, Dmytro, Martz, Eric, Tuominen, Mark T., and Lovley, Derek R. Structural Basis for Metallic-Like Conductivity in Microbial Nanowires. United States: N. p., 2015.
Web. doi:10.1128/mbio.00084-15.
Malvankar, Nikhil S., Vargas, Madeline, Nevin, Kelly, Tremblay, Pier-Luc, Evans-Lutterodt, Kenneth, Nykypanchuk, Dmytro, Martz, Eric, Tuominen, Mark T., & Lovley, Derek R. Structural Basis for Metallic-Like Conductivity in Microbial Nanowires. United States. https://doi.org/10.1128/mbio.00084-15
Malvankar, Nikhil S., Vargas, Madeline, Nevin, Kelly, Tremblay, Pier-Luc, Evans-Lutterodt, Kenneth, Nykypanchuk, Dmytro, Martz, Eric, Tuominen, Mark T., and Lovley, Derek R. 2015.
"Structural Basis for Metallic-Like Conductivity in Microbial Nanowires". United States. https://doi.org/10.1128/mbio.00084-15. https://www.osti.gov/servlets/purl/1259267.
@article{osti_1259267,
title = {Structural Basis for Metallic-Like Conductivity in Microbial Nanowires},
author = {Malvankar, Nikhil S. and Vargas, Madeline and Nevin, Kelly and Tremblay, Pier-Luc and Evans-Lutterodt, Kenneth and Nykypanchuk, Dmytro and Martz, Eric and Tuominen, Mark T. and Lovley, Derek R.},
abstractNote = {Direct measurement of multiple physical properties of Geobacter sulfurreducens pili have demonstrated that they possess metallic-like conductivity, but several studies have suggested that metallic-like conductivity is unlikely based on the structures of the G. sulfurreducens pilus predicted from homology models. In order to further evaluate this discrepancy, pili were examined with synchrotron X-ray microdiffraction and rocking-curve X-ray diffraction. Both techniques revealed a periodic 3.2-Å spacing in conductive, wild-type G. sulfurreducens pili that was missing in the nonconductive pili of strain Aro5, which lack key aromatic acids required for conductivity. The intensity of the 3.2-Å peak increased 100-fold when the pH was shifted from 10.5 to 2, corresponding with a previously reported 100-fold increase in pilus conductivity with this pH change. These results suggest a clear structure-function correlation for metallic-like conductivity that can be attributed to overlapping π-orbitals of aromatic amino acids. A homology model of the G. sulfurreducens pilus was constructed with a Pseudomonas aeruginosa pilus model as a template as an alternative to previous models, which were based on a Neisseria gonorrhoeae pilus structure. This alternative model predicted that aromatic amino acids in G. sulfurreducens pili are packed within 3 to 4 Å, consistent with the experimental results. Thus, the predictions of homology modeling are highly sensitive to assumptions inherent in the model construction. Finally, the experimental results reported here further support the concept that the pili of G. sulfurreducens represent a novel class of electronically functional proteins in which aromatic amino acids promote long-distance electron transport.},
doi = {10.1128/mbio.00084-15},
url = {https://www.osti.gov/biblio/1259267},
journal = {mBio (Online)},
issn = {2150-7511},
number = 2,
volume = 6,
place = {United States},
year = {Tue Mar 03 00:00:00 EST 2015},
month = {Tue Mar 03 00:00:00 EST 2015}
}
Web of Science
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Microbial electron transport and energy conservation – the foundation for optimizing bioelectrochemical systems
journal, June 2015
- Kracke, Frauke; Vassilev, Igor; Krömer, Jens O.
- Frontiers in Microbiology, Vol. 6
Comparative Analysis of Type IV Pilin in Desulfuromonadales
journal, December 2016
- Shu, Chuanjun; Xiao, Ke; Yan, Qin
- Frontiers in Microbiology, Vol. 7
Anodic and Cathodic Extracellular Electron Transfer by the Filamentous Bacterium Ardenticatena maritima 110S
journal, February 2018
- Kawaichi, Satoshi; Yamada, Tetsuya; Umezawa, Akio
- Frontiers in Microbiology, Vol. 9
Stimulatory Effect of Magnetite Nanoparticles on a Highly Enriched Butyrate-Oxidizing Consortium
journal, July 2018
- Fu, Li; Song, Tianze; Zhang, Wei
- Frontiers in Microbiology, Vol. 9
Thermophiles; or, the Modern Prometheus: The Importance of Extreme Microorganisms for Understanding and Applying Extracellular Electron Transfer
journal, April 2019
- Lusk, Bradley G.
- Frontiers in Microbiology, Vol. 10
Geobacter Protein Nanowires
journal, September 2019
- Lovley, Derek R.; Walker, David J. F.
- Frontiers in Microbiology, Vol. 10
Predicting and Interpreting the Structure of Type IV Pilus of Electricigens by Molecular Dynamics Simulations
journal, August 2017
- Shu, Chuanjun; Xiao, Ke; Cao, Changchang
- Molecules, Vol. 22, Issue 8