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

Vargas, Madeline; Malvankar, Nikhil S.; Tremblay, Pier-Luc; Leang, Ching; Smith, Jessica A.; Patel, Pranav; Synoeyenbos-West, Oona; Nevin, Kelly P.; Lovley, Derek R.

doi:10.1128/mbio.00105-13

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

Journal Article · Tue Mar 12 00:00:00 EDT 2013 · mBio (Online)

DOI:https://doi.org/10.1128/mbio.00105-13· OSTI ID:1626085

Vargas, Madeline ^[1]; Malvankar, Nikhil S. ^[2]; Tremblay, Pier-Luc ^[2]; Leang, Ching ^[2]; Smith, Jessica A. ^[2]; Patel, Pranav ^[2]; Synoeyenbos-West, Oona ^[2]; Nevin, Kelly P. ^[2]; Lovley, Derek R. ^[2]

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

It has been proposed that Geobacter sulfurreducens requires 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 of G. 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 which G. sulfurreducens PilA 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 multiheme c-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 of G. sulfurreducens must be conductive in order for the cells to be effective in extracellular long-range electron transport.

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Research Organization:: Univ. of Massachusetts, Amherst, MA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division

Grant/Contract Number:: SC0004114

OSTI ID:: 1626085

Journal Information:: mBio (Online), Vol. 4, Issue 2; ISSN 2150-7511

Publisher:: American Society for Microbiology (ASM)Copyright Statement

Country of Publication:: United States

Language:: English

References (30)

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
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
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
16S ribosomal DNA amplification for phylogenetic study. Weisburg, W. G.; Barns, S. M.; Pelletier, D. A. Journal of Bacteriology, Vol. 173, Issue 2 https://doi.org/10.1128/jb.173.2.697-703.1991	journal	January 1991
Dissimilatory Fe(III) and Mn(IV) reduction Lovley, D. R. Microbiological Reviews, Vol. 55, Issue 2 https://doi.org/10.1128/mr.55.2.259-287.1991	journal	June 1991
Electromicrobiology Lovley, Derek R. Annual Review of Microbiology, Vol. 66, Issue 1 https://doi.org/10.1146/annurev-micro-092611-150104	journal	October 2012
Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2−ΔΔCT Method Livak, Kenneth J.; Schmittgen, Thomas D. Methods, Vol. 25, Issue 4 https://doi.org/10.1006/meth.2001.1262	journal	December 2001
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
Microtoming coupled to microarray analysis to evaluate the spatial metabolic status of Geobacter sulfurreducens biofilms Franks, Ashley E.; Nevin, Kelly P.; Glaven, Richard H. The ISME Journal, Vol. 4, Issue 4 https://doi.org/10.1038/ismej.2009.137	journal	December 2009
Alignment of the c-Type Cytochrome OmcS along Pili of Geobacter sulfurreducens Leang, C.; Qian, X.; Mester, T. Applied and Environmental Microbiology, Vol. 76, Issue 12, p. 4080-4084 https://doi.org/10.1128/AEM.00023-10	journal	April 2010
In-situ conductance measurement during electropolymerization Kankare, Jouko; Kupila, Eeva-Liisa Journal of Electroanalytical Chemistry, Vol. 322, Issue 1-2 https://doi.org/10.1016/0022-0728(92)80074-E	journal	January 1992
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
Biochemical and genetic characterization of PpcA, a periplasmic c-type cytochrome in Geobacter sulfurreducens Lloyd, Jon R.; Leang, Ching; Myerson, Allison L. HODGES Biochemical Journal, Vol. 369, Issue 1 https://doi.org/10.1042/bj20020597	journal	January 2003
Electrosynthesis of Organic Compounds from Carbon Dioxide Is Catalyzed by a Diversity of Acetogenic Microorganisms Nevin, Kelly P.; Hensley, Sarah A.; Franks, Ashley E. Applied and Environmental Microbiology, Vol. 77, Issue 9, p. 2882-2886 https://doi.org/10.1128/AEM.02642-10	journal	March 2011
Long-range electron transport in Geobacter sulfurreducens biofilms is redox gradient-driven Snider, R. M.; Strycharz-Glaven, S. M.; Tsoi, S. D. Proceedings of the National Academy of Sciences, Vol. 109, Issue 38 https://doi.org/10.1073/pnas.1209829109	journal	September 2012
Dissimilatory Fe(III) and Mn(IV) reduction. Lovley, D. R. Microbiological Reviews, Vol. 55, Issue 2 https://doi.org/10.1128/MMBR.55.2.259-287.1991	journal	January 1991
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
Conductivity Studies of Nanostructured TiO ₂ Films Permeated with Electrolyte Greijer Agrell, Helena; Boschloo, Gerrit; Hagfeldt, Anders The Journal of Physical Chemistry B, Vol. 108, Issue 33 https://doi.org/10.1021/jp037119p	journal	August 2004
Real-Time Spatial Gene Expression Analysis within Current-Producing Biofilms Franks, Ashley E.; Glaven, Richard H.; Lovley, Derek R. ChemSusChem, Vol. 5, Issue 6 https://doi.org/10.1002/cssc.201100714	journal	May 2012
Product of the Pseudomonas aeruginosa gene pilD is a prepilin leader peptidase. Nunn, D. N.; Lory, S. Proceedings of the National Academy of Sciences, Vol. 88, Issue 8 https://doi.org/10.1073/pnas.88.8.3281	journal	April 1991
Direct Exchange of Electrons Within Aggregates of an Evolved Syntrophic Coculture of Anaerobic Bacteria Summers, Z. M.; Fogarty, H. E.; Leang, C. Science, Vol. 330, Issue 6009, p. 1413-1415 https://doi.org/10.1126/science.1196526	journal	December 2010
Novel Mode of Microbial Energy Metabolism: Organic Carbon Oxidation Coupled to Dissimilatory Reduction of Iron or Manganese Lovley, Derek R.; Phillips, Elizabeth J. P. Applied and Environmental Microbiology, Vol. 54, Issue 6 https://doi.org/10.1128/aem.54.6.1472-1480.1988	journal	January 1988
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
Potential for Direct Interspecies Electron Transfer in Methanogenic Wastewater Digester Aggregates Morita, Masahiko; Malvankar, Nikhil S.; Franks, Ashley E. mBio, Vol. 2, Issue 4 https://doi.org/10.1128/mBio.00159-11	journal	August 2011
Live wires: direct extracellular electron exchange for bioenergy and the bioremediation of energy-related contamination Lovley, Derek R. Energy & Environmental Science, Vol. 4, Issue 12 https://doi.org/10.1039/c1ee02229f	journal	January 2011
Interference with histidyl-tRNA synthetase by a CRISPR spacer sequence as a factor in the evolution of Pelobacter carbinolicus Aklujkar, Muktak; Lovley, Derek R. BMC Evolutionary Biology, Vol. 10, Issue 1 https://doi.org/10.1186/1471-2148-10-230	journal	January 2010
Separated analysis of bulk and contact resistance of conducting polymers: Comparison of simultaneous two- and four-point measurements with impedance measurements Lange, Ulrich; Mirsky, Vladimir M. Journal of Electroanalytical Chemistry, Vol. 622, Issue 2 https://doi.org/10.1016/j.jelechem.2008.06.013	journal	October 2008
Microarray and genetic analysis of electron transfer to electrodes in Geobacter sulfurreducens Holmes, Dawn E.; Chaudhuri, Swades K.; Nevin, Kelly P. Environmental Microbiology, Vol. 8, Issue 10 https://doi.org/10.1111/j.1462-2920.2006.01065.x	journal	October 2006
Lack of Production of Electron-Shuttling Compounds or Solubilization of Fe(III) during Reduction of Insoluble Fe(III) Oxide by Geobacter metallireducens Nevin, K. P.; Lovley, D. R. Applied and Environmental Microbiology, Vol. 66, Issue 5 https://doi.org/10.1128/aem.66.5.2248-2251.2000	journal	May 2000
Development of a Genetic System for Geobacter sulfurreducens Coppi, M. V.; Leang, C.; Sandler, S. J. Applied and Environmental Microbiology, Vol. 67, Issue 7, p. 3180-3187 https://doi.org/10.1128/aem.67.7.3180-3187.2001	journal	July 2001

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