Structural Basis for Metallic-Like Conductivity in Microbial Nanowires

Malvankar, Nikhil S.; Vargas, Madeline; Nevin, Kelly; Tremblay, Pier-Luc; Evans-Lutterodt, Kenneth; Nykypanchuk, Dmytro; Martz, Eric; Tuominen, Mark T.; Lovley, Derek R.

doi:10.1128/mbio.00084-15

Title: Structural Basis for Metallic-Like Conductivity in Microbial Nanowires

Journal Article · Tue Mar 03 00:00:00 EST 2015 · mBio (Online)

DOI:https://doi.org/10.1128/mbio.00084-15· OSTI ID:1259267

Malvankar, Nikhil S. ^[1]; Vargas, Madeline ^[2]; Nevin, Kelly ^[3]; Tremblay, Pier-Luc ^[3]; Evans-Lutterodt, Kenneth ^[4]; Nykypanchuk, Dmytro ^[5]; Martz, Eric ^[3]; Tuominen, Mark T. ^[6]; Lovley, Derek R. ^[3]

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

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.

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Research Organization:: Brookhaven National Laboratory (BNL), Upton, NY (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES)

Grant/Contract Number:: AC02-98CH10886; N00014-13-1-0550; N00014-12-1-0229

OSTI ID:: 1259267

Journal Information:: mBio (Online), Vol. 6, Issue 2; ISSN 2150-7511

Publisher:: American Society for MicrobiologyCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 137 works

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References (48)

Microbial Nanowires: A New Paradigm for Biological Electron Transfer and Bioelectronics Malvankar, Nikhil S.; Lovley, Derek R. ChemSusChem, Vol. 5, Issue 6 https://doi.org/10.1002/cssc.201100733	journal	May 2012
Microbial nanowires for bioenergy applications Malvankar, Nikhil S.; Lovley, Derek R. Current Opinion in Biotechnology, Vol. 27 https://doi.org/10.1016/j.copbio.2013.12.003	journal	June 2014
Electrobiocommodities: powering microbial production of fuels and commodity chemicals from carbon dioxide with electricity Lovley, Derek R.; Nevin, Kelly P. Current Opinion in Biotechnology, Vol. 24, Issue 3 https://doi.org/10.1016/j.copbio.2013.02.012	journal	June 2013
Electron Transfer and Electronic Conduction through an Intervening Medium Edwards, Peter P.; Gray, Harry B.; Lodge, Matthew T. J. Angewandte Chemie International Edition, Vol. 47, Issue 36 https://doi.org/10.1002/anie.200703177	journal	August 2008
Tunable metallic-like conductivity in microbial nanowire networks Malvankar, Nikhil S.; Vargas, Madeline; Nevin, Kelly P. Nature Nanotechnology, Vol. 6, Issue 9 https://doi.org/10.1038/nnano.2011.119	journal	August 2011
Extracellular electron transfer via microbial nanowires Reguera, Gemma; McCarthy, Kevin D.; Mehta, Teena Nature, Vol. 435, Issue 7045, p. 1098-1101 https://doi.org/10.1038/nature03661	journal	June 2005
Direct Interspecies Electron Transfer between Geobacter metallireducens and Methanosarcina barkeri Rotaru, Amelia-Elena; Shrestha, Pravin Malla; Liu, Fanghua Applied and Environmental Microbiology, Vol. 80, Issue 15 https://doi.org/10.1128/AEM.00895-14	journal	May 2014
Biofilm conductivity is a decisive variable for high-current-density Geobacter sulfurreducens microbial fuel cells Malvankar, Nikhil S.; Tuominen, Mark T.; Lovley, Derek R. Energy & Environmental Science, Vol. 5, Issue 2 https://doi.org/10.1039/c2ee03388g	journal	January 2012
Biofilm and Nanowire Production Leads to Increased Current in Geobacter sulfurreducens Fuel Cells Reguera, G.; Nevin, K. P.; Nicoll, J. S. Applied and Environmental Microbiology, Vol. 72, Issue 11 https://doi.org/10.1128/AEM.01444-06	journal	August 2006
Anode Biofilm Transcriptomics Reveals Outer Surface Components Essential for High Density Current Production in Geobacter sulfurreducens Fuel Cells Nevin, Kelly P.; Kim, Byoung-Chan; Glaven, Richard H. PLoS ONE, Vol. 4, Issue 5 https://doi.org/10.1371/journal.pone.0005628	journal	May 2009
Seeing is believing: novel imaging techniques help clarify microbial nanowire structure and function: Resolving microbial nanowire structure and function Lovley, Derek R.; Malvankar, Nikhil S. Environmental Microbiology, Vol. 17, Issue 7 https://doi.org/10.1111/1462-2920.12708	journal	January 2015
A natural source of nanowires Qian, Fang; Li, Yat Nature Nanotechnology, Vol. 6, Issue 9 https://doi.org/10.1038/nnano.2011.148	journal	September 2011
Metallic transport in polyaniline Lee, Kwanghee; Cho, Shinuk; Heum Park, Sung Nature, Vol. 441, Issue 7089 https://doi.org/10.1038/nature04705	journal	May 2006
A Geobacter sulfurreducens Strain Expressing Pseudomonas aeruginosa Type IV Pili Localizes OmcS on Pili but Is Deficient in Fe(III) Oxide Reduction and Current Production Liu, Xing; Tremblay, Pier-Luc; Malvankar, Nikhil S. Applied and Environmental Microbiology, Vol. 80, Issue 3 https://doi.org/10.1128/AEM.02938-13	journal	December 2013
Stepping stones in the electron transport from cells to electrodes in Geobacter sulfurreducens biofilms Bonanni, Pablo Sebastián; Massazza, Diego; Busalmen, Juan Pablo Physical Chemistry Chemical Physics, Vol. 15, Issue 25 https://doi.org/10.1039/c3cp50411e	journal	January 2013
Molecular Dissection of Bacterial Nanowires Boesen, Thomas; Nielsen, Lars Peter mBio, Vol. 4, Issue 3 https://doi.org/10.1128/mBio.00270-13	journal	May 2013
Structure of the Type IVa Major Pilin from the Electrically Conductive Bacterial Nanowires of Geobacter sulfurreducens Reardon, Patrick N.; Mueller, Karl T. Journal of Biological Chemistry, Vol. 288, Issue 41 https://doi.org/10.1074/jbc.M113.498527	journal	August 2013
Molecular and Electronic Structure of the Peptide Subunit of Geobacter sulfurreducens Conductive Pili from First Principles Feliciano, Gustavo T.; da Silva, Antonio J. R.; Reguera, Gemma The Journal of Physical Chemistry A, Vol. 116, Issue 30, p. 8023-8030 https://doi.org/10.1021/jp302232p	journal	July 2012
Type IV Pilus Structure by Cryo-Electron Microscopy and Crystallography: Implications for Pilus Assembly and Functions Craig, Lisa; Volkmann, Niels; Arvai, Andrew S. Molecular Cell, Vol. 23, Issue 5, p. 651-662 https://doi.org/10.1016/j.molcel.2006.07.004	journal	September 2006
Type IV pilus structure and bacterial pathogenicity Craig, Lisa; Pique, Michael E.; Tainer, John A. Nature Reviews Microbiology, Vol. 2, Issue 5 https://doi.org/10.1038/nrmicro885	journal	May 2004
An investigation of the conductivity of peptide nanotube networks prepared by enzyme-triggered self-assembly Xu, Haixia; Das, Apurba K.; Horie, Masaki Nanoscale, Vol. 2, Issue 6 https://doi.org/10.1039/b9nr00233b	journal	January 2010
Rethinking the term “pi-stacking” Martinez, Chelsea R.; Iverson, Brent L. Chemical Science, Vol. 3, Issue 7 https://doi.org/10.1039/c2sc20045g	journal	January 2012
A critical account on π–π stacking in metal complexes with aromatic nitrogen-containing ligands † Janiak, Christoph Journal of the Chemical Society, Dalton Transactions, Issue 21 https://doi.org/10.1039/b003010o	journal	January 2000
High-resolution X-ray diffraction analyses of protein crystals Volz, H. M.; Matyi, R. J. Philosophical Transactions of the Royal Society of London. Series A: Mathematical, Physical and Engineering Sciences, Vol. 357, Issue 1761 https://doi.org/10.1098/rsta.1999.0466	journal	October 1999
Accurate rocking-curve measurements on protein crystals grown in a homogeneous magnetic field of 2.4 T Lübbert, Daniel; Meents, Alke; Weckert, Edgar Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 6 https://doi.org/10.1107/S0907444904005268	journal	May 2004
Charge-Transfer and Energy-Transfer Processes in π-Conjugated Oligomers and Polymers: A Molecular Picture Brédas, Jean-Luc; Beljonne, David; Coropceanu, Veaceslav Chemical Reviews, Vol. 104, Issue 11 https://doi.org/10.1021/cr040084k	journal	November 2004
Organic semiconductors: A theoretical characterization of the basic parameters governing charge transport Bredas, J. L.; Calbert, J. P.; da Silva Filho, D. A. Proceedings of the National Academy of Sciences, Vol. 99, Issue 9 https://doi.org/10.1073/pnas.092143399	journal	April 2002
One-Dimensional Optoelectronic Nanostructures Derived from the Aqueous Self-Assembly of π-Conjugated Oligopeptides Diegelmann, Stephen R.; Gorham, Justin M.; Tovar, John D. Journal of the American Chemical Society, Vol. 130, Issue 42 https://doi.org/10.1021/ja805491d	journal	October 2008
On-resin dimerization incorporates a diverse array of π-conjugated functionality within aqueous self-assembling peptide backbones Vadehra, Geeta S.; Wall, Brian D.; Diegelmann, Stephen R. Chemical Communications, Vol. 46, Issue 22 https://doi.org/10.1039/c0cc00301h	journal	January 2010
Lack of cytochrome involvement in long-range electron transport through conductive biofilms and nanowires of Geobacter sulfurreducens Malvankar, Nikhil S.; Tuominen, Mark T.; Lovley, Derek R. Energy & Environmental Science, Vol. 5, Issue 9 https://doi.org/10.1039/c2ee22330a	journal	January 2012
Type IV Pilin Structure and Assembly Craig, Lisa; Taylor, Ronald K.; Pique, Michael E. Molecular Cell, Vol. 11, Issue 5 https://doi.org/10.1016/S1097-2765(03)00170-9	journal	May 2003
Design of Self-Assembling Peptide Nanotubes with Delocalized Electronic States Ashkenasy, Nurit; Horne, W. Seth; Ghadiri, M. Reza Small, Vol. 2, Issue 1 https://doi.org/10.1002/smll.200500252	journal	January 2006
Stroboscopic imaging of macromolecular complexes Glaeser, Robert M. Nature Methods, Vol. 10, Issue 6 https://doi.org/10.1038/nmeth.2486	journal	May 2013
Selection of a variant of Geobacter sulfurreducens with enhanced capacity for current production in microbial fuel cells Yi, Hana; Nevin, Kelly P.; Kim, Byoung-Chan Biosensors and Bioelectronics, Vol. 24, Issue 12, p. 3498-3503 https://doi.org/10.1016/j.bios.2009.05.004	journal	August 2009
Power output and columbic efficiencies from biofilms of Geobacter sulfurreducens comparable to mixed community microbial fuel cells: High current production with a pure culture Nevin, K. P.; Richter, H.; Covalla, S. F. Environmental Microbiology, Vol. 10, Issue 10 https://doi.org/10.1111/j.1462-2920.2008.01675.x	journal	June 2008
PilX, a pilus-associated protein essential for bacterial aggregation, is a key to pilus-facilitated attachment of Neisseria meningitidis to human cells: Aggregation and pilus-facilitated adherence Hélaine, Sophie; Carbonnelle, Etienne; Prouvensier, Laure Molecular Microbiology, Vol. 55, Issue 1 https://doi.org/10.1111/j.1365-2958.2004.04372.x	journal	October 2004
Hrp pilus: An hrp-dependent bacterial surface appendage produced by Pseudomonas syringae pv. tomato DC3000 Roine, E.; Wei, W.; Yuan, J. Proceedings of the National Academy of Sciences, Vol. 94, Issue 7 https://doi.org/10.1073/pnas.94.7.3459	journal	April 1997
‘Polyaniline’: Protonic acid doping of the emeraldine form to the metallic regime Chiang, Jin-Chih; MacDiarmid, Alan G. Synthetic Metals, Vol. 13, Issue 1-3 https://doi.org/10.1016/0379-6779(86)90070-6	journal	January 1986
Bulk and interface investigations of scaffolds and tissue-engineered bones by X-ray microtomography and X-ray microdiffraction Cancedda, R.; Cedola, A.; Giuliani, A. Biomaterials, Vol. 28, Issue 15 https://doi.org/10.1016/j.biomaterials.2007.01.022	journal	May 2007
An In Situ Synchrotron Study of Zinc Anode Planarization by a Bismuth Additive Gallaway, Joshua W.; Gaikwad, Abhinav M.; Hertzberg, Benjamin Journal of The Electrochemical Society, Vol. 161, Issue 3 https://doi.org/10.1149/2.037403jes	journal	December 2013
MolProbity : all-atom structure validation for macromolecular crystallography Chen, Vincent B.; Arendall, W. Bryan; Headd, Jeffrey J. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 1 https://doi.org/10.1107/S0907444909042073	journal	December 2009
Toward the estimation of the absolute quality of individual protein structure models Benkert, Pascal; Biasini, Marco; Schwede, Torsten Bioinformatics, Vol. 27, Issue 3 https://doi.org/10.1093/bioinformatics/btq662	journal	December 2010
ConSurf 2010: calculating evolutionary conservation in sequence and structure of proteins and nucleic acids Ashkenazy, H.; Erez, E.; Martz, E. Nucleic Acids Research, Vol. 38, Issue Web Server https://doi.org/10.1093/nar/gkq399	journal	May 2010
Jmol – a paradigm shift in crystallographic visualization Hanson, Robert M. Journal of Applied Crystallography, Vol. 43, Issue 5 https://doi.org/10.1107/S0021889810030256	journal	September 2010
van der Waals Volumes and Radii Bondi, A. The Journal of Physical Chemistry, Vol. 68, Issue 3, p. 441-451 https://doi.org/10.1021/j100785a001	journal	March 1964
Exploring the gas access routes in a [NiFeSe] hydrogenase using crystals pressurized with krypton and oxygen Zacarias, Sónia; Temporão, Adriana; Carpentier, Philippe JBIC Journal of Biological Inorganic Chemistry, Vol. 25, Issue 6 https://doi.org/10.1007/s00775-020-01814-y	journal	August 2020
Charge-Transfer and Energy-Transfer Processes in ?-Conjugated Oligomers and Polymers: A Molecular Picture Bredas, Jean-Luc; Beljonne, David; Coropceanu, Veaceslav ChemInform, Vol. 36, Issue 5 https://doi.org/10.1002/chin.200505257	journal	February 2005
Structure of the Type IVa Major Pilin from the Electrically Conductive Bacterial Nanowires of Geobacter sulfurreducens Reardon, Patrick N.; Mueller, Karl T. Biological Magnetic Resonance Bank https://doi.org/10.13018/bmr19185	dataset	January 2013

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