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

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

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Abstract

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.IMPORTANCE Extracellular electron transfer by Geobacter species plays an important role in the biogeochemistry of soils and sediments and has a number of bioenergy applications. For example, microbial reduction of Fe(III) oxide is one of the most geo-chemically significant processes in anaerobic soils, aquatic sediments, and aquifers, and Geobacter organisms are often abundant in such environments. Geobacter sulfurreducens produces the highest current densities of any known pure culture, and close relatives are often the most abundant organisms colonizing anodes in microbial fuel cells that harvest electricity from wastewater or aquatic sediments. The finding that a strain of G. sulfurreducens that produces pili with low conductivity is limited in these extracellular electron transport functions provides further insight into these environmentally significant processes.
Original languageEnglish
Article numbere00105-13
JournalmBio
Volume4
Issue number2
ISSN2150-7511
DOIs
Publication statusPublished - 2013
Externally publishedYes

Keywords

  • long-range extracellular electron transport
  • Eubacteria Bacteria Microorganisms (Bacteria, Eubacteria, Microorganisms) - Dissimilatory Sulfate or Sulfur Reducers [06810] Geobacter sulfurreducens species strain-Aro-5
  • Facultatively Anaerobic Gram-Negative Rods Eubacteria Bacteria Microorganisms (Bacteria, Eubacteria, Microorganisms) - Enterobacteriaceae [06702] Escherichia coli species
  • aromatic amino acids
  • iron(III) oxide 1309-37-1
  • OmcS multiheme c-type cytochrome
  • PilA protein structural pilin protein
  • 02502, Cytology - General
  • 10060, Biochemistry studies - General
  • 30500, Morphology and cytology of bacteria
  • 31000, Physiology and biochemistry of bacteria
  • 32500, Tissue culture, apparatus, methods and media
  • pili
  • cell culture laboratory techniques, culturing techniques
  • Biochemistry and Molecular Biophysics
  • Cell Biology

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