Differential gene expression in response to phenol and catechol reveals different metabolic activities for the degradation of aromatic compounds in Bacillus subtilis

Environ Microbiol. 2006 Aug;8(8):1408-27. doi: 10.1111/j.1462-2920.2006.01034.x.

Abstract

Aromatic organic compounds that are present in the environment can have toxic effects or provide carbon sources for bacteria. We report here the global response of Bacillus subtilis 168 to phenol and catechol using proteome and transcriptome analyses. Phenol induced the HrcA, sigmaB and CtsR heat-shock regulons as well as the Spx disulfide stress regulon. Catechol caused the activation of the HrcA and CtsR heat-shock regulons and a thiol-specific oxidative stress response involving the Spx, PerR and FurR regulons but no induction of the sigmaB regulon. The most surprising result was that several catabolite-controlled genes are derepressed by catechol, even if glucose is taken up under these conditions. This derepression of the carbon catabolite control was dependent on the glucose concentration in the medium, as glucose excess increased the derepression of the CcpA-dependent lichenin utilization licBCAH operon and the ribose metabolism rbsRKDACB operon by catechol. Growth and viability experiments with catechol as sole carbon source suggested that B. subtilis is not able to utilize catechol as a carbon-energy source. In addition, the microarray results revealed the very strong induction of the yfiDE operon by catechol of which the yfiE gene shares similarities to glyoxalases/bleomycin resistance proteins/extradiol dioxygenases. Using recombinant His6-YfiE(Bs) we demonstrate that YfiE shows catechol-2,3-dioxygenase activity in the presence of catechol as the metabolite 2-hydroxymuconic semialdehyde was measured. Furthermore, both genes of the yfiDE operon are essential for the growth and viability of B. subtilis in the presence of catechol. Thus, our studies revealed that the catechol-2,3-dioxygenase YfiE is the key enzyme of a meta cleavage pathway in B. subtilis involved in the catabolism of catechol.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Bacillus subtilis / drug effects
  • Bacillus subtilis / metabolism*
  • Bacillus subtilis / physiology
  • Biodegradation, Environmental
  • Blotting, Northern
  • Catechols / metabolism*
  • Catechols / toxicity
  • Colony Count, Microbial
  • Electrophoresis, Gel, Two-Dimensional / methods
  • Gene Expression Regulation, Bacterial / genetics*
  • Gene Expression Regulation, Bacterial / physiology
  • Heat-Shock Response
  • Mass Spectrometry / methods
  • Microbial Sensitivity Tests / methods
  • Oxygenases / physiology
  • Phenol / metabolism*
  • Phenol / toxicity
  • Regulon / genetics*
  • Sulfur Isotopes / metabolism

Substances

  • Catechols
  • Sulfur Isotopes
  • Phenol
  • Oxygenases
  • extradiol dioxygenase
  • catechol