Degradation of benzene by the heavy-metal resistant bacteriumCupriavidus metalliduransCH34 reveals its catabolic potential for aromatic compounds

Abstract

AbstractBenzene, toluene, ethylbenzene and the three xylene isomers are monoaromatic contaminants widely distributed on polluted sites. Some microorganisms have developed mechanisms to degrade these compounds, but their aerobic and anaerobic degradation is inhibited in presence of heavy metals, such as mercury or lead. In this report, the degradation of benzene and other aromatic compounds catalyzed by the metal resistant bacteriumCupriavidus metalliduransCH34 was characterized. A metabolic reconstruction of aromatic catabolic pathways was performed based on bioinformatics analyses. Functionality of the predicted pathways was confirmed by growing strain CH34 on benzene, toluene,o-xylene,p-cymene, 3-hydroxybenzoate, 4-hydroxybenzoate, 3-hydroxyphenylacetate, 4-hydroxyphenylacetate, homogentisate, catechol, naphthalene, and 2-aminophenol as sole carbon and energy sources. Benzene catabolic pathway was further characterized. Results showed that firstly benzene is transformed into phenol and, thereafter, into catechol. Benzene is degraded under aerobic conditions via a combined pathway catalyzed by three Bacterial Multicomponent Monooxygenases: a toluene-2-monoxygenase (TomA012345), a toluene-4-monooxygenase (TmoABCDEF) and a phenol-2-hydroxylase (PhyZABCDE). A catechol-2,3-dioxygenase (TomB) expressed at early exponential phase cleaves the catechol ring inmeta-position; anortho-cleavage of catechol is accomplished by a catechol-1,2-dioxygenase (CatA) at late exponential phase instead. This study additionally shows thatC. metalliduransCH34 is capable of degrading benzene in presence of heavy metals, such as Hg(II) or Pb(II). This capability of degrading aromatic compounds in presence of heavy metals is rather unusual among environmental bacteria; therefore,C. metalliduransCH34 seems to be a promising candidate for developing novel bioremediation process for multi-contaminated environments.HIGHLIGHTSThe strainCupriavidus metalliduransCH34 is capable to degrade benzene aerobicallyBenzene oxydation is mediated by bacterial multicomponent monoxygenasesStrain CH34 is able to grow using a broad range of aromatic compounds as sole carbon and energy sourceBenzene degradation occurs even in presence of heavy metals such as mercury and lead