Anaerobic oxidation of benzene by the hyperthermophilic archaeon Ferroglobus placidus

Appl Environ Microbiol. 2011 Sep;77(17):5926-33. doi: 10.1128/AEM.05452-11. Epub 2011 Jul 8.

Abstract

Anaerobic benzene oxidation coupled to the reduction of Fe(III) was studied in Ferroglobus placidus in order to learn more about how such a stable molecule could be metabolized under strict anaerobic conditions. F. placidus conserved energy to support growth at 85°C in a medium with benzene provided as the sole electron donor and Fe(III) as the sole electron acceptor. The stoichiometry of benzene loss and Fe(III) reduction, as well as the conversion of [(14)C]benzene to [(14)C]carbon dioxide, was consistent with complete oxidation of benzene to carbon dioxide with electron transfer to Fe(III). Benzoate, but not phenol or toluene, accumulated at low levels during benzene metabolism, and [(14)C]benzoate was produced from [(14)C]benzene. Analysis of gene transcript levels revealed increased expression of genes encoding enzymes for anaerobic benzoate degradation during growth on benzene versus growth on acetate, but genes involved in phenol degradation were not upregulated during growth on benzene. A gene for a putative carboxylase that was more highly expressed in benzene- than in benzoate-grown cells was identified. These results suggest that benzene is carboxylated to benzoate and that phenol is not an important intermediate in the benzene metabolism of F. placidus. This is the first demonstration of a microorganism in pure culture that can grow on benzene under strict anaerobic conditions and for which there is strong evidence for degradation of benzene via clearly defined anaerobic metabolic pathways. Thus, F. placidus provides a much-needed pure culture model for further studies on the anaerobic activation of benzene in microorganisms.

Publication types

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

MeSH terms

  • Anaerobiosis
  • Archaeoglobales / metabolism*
  • Benzene / metabolism*
  • Carbon Radioisotopes / metabolism
  • Ferric Compounds / metabolism
  • Gene Expression Profiling
  • Hot Temperature
  • Isotope Labeling
  • Oxidation-Reduction

Substances

  • Carbon Radioisotopes
  • Ferric Compounds
  • Benzene