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

Journal Article · · mBio (Online)
 [1];  [2];  [2];  [2];  [2];  [2];  [2];  [2];  [2]
  1. Univ. of Massachusetts, Amherst, MA (United States). Dept. of Microbiology; College of the Holy Cross, Worcester, MA (United States). Dept. of Biology; DOE/OSTI
  2. 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.

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), Journal Name: mBio (Online) Journal Issue: 2 Vol. 4; ISSN 2150-7511
Publisher:
American Society for Microbiology (ASM)Copyright Statement
Country of Publication:
United States
Language:
English

References (40)

Microbial Nanowires: A New Paradigm for Biological Electron Transfer and Bioelectronics journal May 2012
In-situ conductance measurement during electropolymerization journal January 1992
Extracellular electron transfer via microbial nanowires journal June 2005
Live wires: direct extracellular electron exchange for bioenergy and the bioremediation of energy-related contamination journal January 2011
Biochemical and genetic characterization of PpcA, a periplasmic c-type cytochrome in Geobacter sulfurreducens journal January 2003
Long-range electron transport in Geobacter sulfurreducens biofilms is redox gradient-driven journal September 2012
Product of the Pseudomonas aeruginosa gene pilD is a prepilin leader peptidase. journal April 1991
Electrosynthesis of Organic Compounds from Carbon Dioxide Is Catalyzed by a Diversity of Acetogenic Microorganisms journal March 2011
Novel Mode of Microbial Energy Metabolism: Organic Carbon Oxidation Coupled to Dissimilatory Reduction of Iron or Manganese journal January 1988
Lack of Production of Electron-Shuttling Compounds or Solubilization of Fe(III) during Reduction of Insoluble Fe(III) Oxide by Geobacter metallireducens journal May 2000
Development of a Genetic System for Geobacter sulfurreducens journal July 2001
16S ribosomal DNA amplification for phylogenetic study. journal January 1991
Potential for Direct Interspecies Electron Transfer in Methanogenic Wastewater Digester Aggregates journal August 2011
Dissimilatory Fe(III) and Mn(IV) reduction journal June 1991
Electromicrobiology journal October 2012
Interference with histidyl-tRNA synthetase by a CRISPR spacer sequence as a factor in the evolution of Pelobacter carbinolicus journal January 2010
Anode Biofilm Transcriptomics Reveals Outer Surface Components Essential for High Density Current Production in Geobacter sulfurreducens Fuel Cells journal May 2009
Real-Time Spatial Gene Expression Analysis within Current-Producing Biofilms journal May 2012
Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2−ΔΔCT Method journal December 2001
In-situ conductance measurement during electropolymerization journal January 1992
Geobacter book January 2011
Separated analysis of bulk and contact resistance of conducting polymers: Comparison of simultaneous two- and four-point measurements with impedance measurements journal October 2008
Conductivity Studies of Nanostructured TiO 2 Films Permeated with Electrolyte journal August 2004
Microtoming coupled to microarray analysis to evaluate the spatial metabolic status of Geobacter sulfurreducens biofilms journal December 2009
Tunable metallic-like conductivity in microbial nanowire networks journal August 2011
Type IV pilus structure and bacterial pathogenicity journal May 2004
Lack of cytochrome involvement in long-range electron transport through conductive biofilms and nanowires of Geobacter sulfurreducens journal January 2012
Long-range electron transport to Fe(III) oxide via pili with metallic-like conductivity journal November 2012
Microarray and genetic analysis of electron transfer to electrodes in Geobacter sulfurreducens journal October 2006
Direct Exchange of Electrons Within Aggregates of an Evolved Syntrophic Coculture of Anaerobic Bacteria journal December 2010
Alignment of the c-Type Cytochrome OmcS along Pili of Geobacter sulfurreducens journal April 2010
Biofilm and Nanowire Production Leads to Increased Current in Geobacter sulfurreducens Fuel Cells journal August 2006
Electrosynthesis of Organic Compounds from Carbon Dioxide Is Catalyzed by a Diversity of Acetogenic Microorganisms journal March 2011
Novel Mode of Microbial Energy Metabolism: Organic Carbon Oxidation Coupled to Dissimilatory Reduction of Iron or Manganese journal January 1988
Lack of Production of Electron-Shuttling Compounds or Solubilization of Fe(III) during Reduction of Insoluble Fe(III) Oxide by Geobacter metallireducens journal May 2000
Development of a Genetic System for Geobacter sulfurreducens journal July 2001
Potential for Quantifying Expression of the Geobacteraceae Citrate Synthase Gene To Assess the Activity of Geobacteraceae in the Subsurface and on Current-Harvesting Electrodes journal November 2005
16S ribosomal DNA amplification for phylogenetic study. journal January 1991
Dissimilatory Fe(III) and Mn(IV) reduction. journal January 1991
Potential for Direct Interspecies Electron Transfer in Methanogenic Wastewater Digester Aggregates journal August 2011

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