Original Article

Subject Category: Integrated genomics and post-genomics approaches in microbial ecology

The ISME Journal (2012) 6, 146–157; doi:10.1038/ismej.2011.88; published online 21 July 2011

Genome-scale analysis of anaerobic benzoate and phenol metabolism in the hyperthermophilic archaeon Ferroglobus placidus

Dawn E Holmes1,2,3, Carla Risso1,3, Jessica A Smith1 and Derek R Lovley1

  1. 1Department of Microbiology, University of Massachusetts Amherst, Amherst, MA, USA
  2. 2Department of Physical and Biological Sciences, Western New England College, Springfield, MA, USA

Correspondence: DE Holmes, Department of Physical and Biological Sciences, Western New England College, 1215 Wilbraham Road, Springfield, MA 01119, USA. E-mail: dholmes@microbio.umass.edu

3These authors contributed equally to this work.

Received 21 December 2010; Revised 7 June 2011; Accepted 7 June 2011; Published online 21 July 2011.

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Abstract

Insight into the mechanisms for the anaerobic metabolism of aromatic compounds by the hyperthermophilic archaeon Ferroglobus placidus is expected to improve understanding of the degradation of aromatics in hot (>80°C) environments and to identify enzymes that might have biotechnological applications. Analysis of the F. placidus genome revealed genes predicted to encode enzymes homologous to those previously identified as having a role in benzoate and phenol metabolism in mesophilic bacteria. Surprisingly, F. placidus lacks genes for an ATP-independent class II benzoyl-CoA (coenzyme A) reductase (BCR) found in all strictly anaerobic bacteria, but has instead genes coding for a bzd-type ATP-consuming class I BCR, similar to those found in facultative bacteria. The lower portion of the benzoate degradation pathway appears to be more similar to that found in the phototroph Rhodopseudomonas palustris, than the pathway reported for all heterotrophic anaerobic benzoate degraders. Many of the genes predicted to be involved in benzoate metabolism were found in one of two gene clusters. Genes for phenol carboxylation proceeding through a phenylphosphate intermediate were identified in a single gene cluster. Analysis of transcript abundance with a whole-genome microarray and quantitative reverse transcriptase polymerase chain reaction demonstrated that most of the genes predicted to be involved in benzoate or phenol metabolism had higher transcript abundance during growth on those substrates vs growth on acetate. These results suggest that the general strategies for benzoate and phenol metabolism are highly conserved between microorganisms living in moderate and hot environments, and that anaerobic metabolism of aromatic compounds might be analyzed in a wide range of environments with similar molecular targets.

Keywords:

Archaea; benzoate; hyperthermophiles; phenol; transcriptomics