Email updates

Keep up to date with the latest news and content from BMC Genomics and BioMed Central.

Open Access Research article

Genomic and microarray analysis of aromatics degradation in Geobacter metallireducens and comparison to a Geobacter isolate from a contaminated field site

Jessica E Butler1*, Qiang He3, Kelly P Nevin1, Zhili He2, Jizhong Zhou2 and Derek R Lovley1

Author Affiliations

1 Department of Microbiology, University of Massachusetts, Amherst, MA 01003, USA

2 Environmental Science Division, Oak Ridge National Laboratory, Oak Ridge, TN 37831, USA

3 Department of Civil and Environmental Engineering, University of Tennessee, Knoxville, TN 37996, USA

For all author emails, please log on.

BMC Genomics 2007, 8:180  doi:10.1186/1471-2164-8-180

Published: 19 June 2007

Abstract

Background

Groundwater and subsurface environments contaminated with aromatic compounds can be remediated in situ by Geobacter species that couple oxidation of these compounds to reduction of Fe(III)-oxides. Geobacter metallireducens metabolizes many aromatic compounds, but the enzymes involved are not well known.

Results

The complete G. metallireducens genome contained a 300 kb island predicted to encode enzymes for the degradation of phenol, p-cresol, 4-hydroxybenzaldehyde, 4-hydroxybenzoate, benzyl alcohol, benzaldehyde, and benzoate. Toluene degradation genes were encoded in a separate region. None of these genes was found in closely related species that cannot degrade aromatic compounds. Abundant transposons and phage-like genes in the island suggest mobility, but nucleotide composition and lack of synteny with other species do not suggest a recent transfer. The inferred degradation pathways are similar to those in species that anaerobically oxidize aromatic compounds with nitrate as an electron acceptor. In these pathways the aromatic compounds are converted to benzoyl-CoA and then to 3-hydroxypimelyl-CoA. However, in G. metallireducens there were no genes for the energetically-expensive dearomatizing enzyme. Whole-genome changes in transcript levels were identified in cells oxidizing benzoate. These supported the predicted pathway, identified induced fatty-acid oxidation genes, and identified an apparent shift in the TCA cycle to a putative ATP-yielding succinyl-CoA synthase. Paralogs to several genes in the pathway were also induced, as were several putative molybdo-proteins. Comparison of the aromatics degradation pathway genes to the genome of an isolate from a contaminated field site showed very similar content, and suggested this strain degrades many of the same compounds. This strain also lacked a classical dearomatizing enzyme, but contained two copies of an eight-gene cluster encoding redox proteins that was 30-fold induced during benzoate oxidation.

Conclusion

G. metallireducens appears to convert aromatic compounds to benzoyl-CoA, then to acetyl-CoA via fatty acid oxidation, and then to carbon dioxide via the TCA cycle. The enzyme responsible for dearomatizing the aromatic ring may be novel, and energetic investments at this step may be offset by a change in succinate metabolism. Analysis of a field isolate suggests that the pathways inferred for G. metallireducens may be applicable to modeling in situ bioremediation.