Periplasmic electron transfer via the c-type cytochromes MtrA and FccA of Shewanella oneidensis MR-1

Appl Environ Microbiol. 2009 Dec;75(24):7789-96. doi: 10.1128/AEM.01834-09. Epub 2009 Oct 16.

Abstract

Dissimilatory microbial reduction of insoluble Fe(III) oxides is a geochemically and ecologically important process which involves the transfer of cellular, respiratory electrons from the cytoplasmic membrane to insoluble, extracellular, mineral-phase electron acceptors. In this paper evidence is provided for the function of the periplasmic fumarate reductase FccA and the decaheme c-type cytochrome MtrA in periplasmic electron transfer reactions in the gammaproteobacterium Shewanella oneidensis. Both proteins are abundant in the periplasm of ferric citrate-reducing S. oneidensis cells. In vitro fumarate reductase FccA and c-type cytochrome MtrA were reduced by the cytoplasmic membrane-bound protein CymA. Electron transfer between CymA and MtrA was 1.4-fold faster than the CymA-catalyzed reduction of FccA. Further experiments showing a bidirectional electron transfer between FccA and MtrA provided evidence for an electron transfer network in the periplasmic space of S. oneidensis. Hence, FccA could function in both the electron transport to fumarate and via MtrA to mineral-phase Fe(III). Growth experiments with a DeltafccA deletion mutant suggest a role of FccA as a transient electron storage protein.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Bacterial Outer Membrane Proteins / genetics
  • Bacterial Outer Membrane Proteins / isolation & purification
  • Bacterial Outer Membrane Proteins / metabolism*
  • Cytochrome c Group / genetics
  • Cytochrome c Group / metabolism*
  • Electron Transport*
  • Escherichia coli / genetics
  • Escherichia coli / metabolism
  • Ferric Compounds / metabolism
  • Fumarates / metabolism
  • Gene Expression Regulation, Bacterial
  • Oxidation-Reduction
  • Periplasm / genetics
  • Periplasm / metabolism*
  • Shewanella / genetics
  • Shewanella / metabolism*
  • Succinate Dehydrogenase / genetics
  • Succinate Dehydrogenase / isolation & purification
  • Succinate Dehydrogenase / metabolism*

Substances

  • Bacterial Outer Membrane Proteins
  • Cytochrome c Group
  • Ferric Compounds
  • Fumarates
  • ferric oxide
  • ferric citrate
  • cytochrome c(3)
  • Succinate Dehydrogenase