Anaerobic biodegradation of anthracene by oral Firmicutes isolates from smokers and its potential pathway

Abstract

Exposure to polycyclic aromatic hydrocarbons (PAHs) from tobacco smoke has been linked to many negative health effects. Studies on the biodegradation of PAHs by human microbiota and detailed pathways for their anaerobic biodegradation are scarce despite their importance in getting rid of these toxic compounds. In a previous study for our group, we determined the ability of oral bacterial isolates in the anaerobic biodegradation of anthracene as a model of PAHs. Three isolates with the highest anthracene degradation ability were selected for the present study which include Limosilactobacillus fermentum, Veillonella parvula, and Streptococcus anginosus. In this study, we aimed at exploring and elucidating the anthracene anaerobic biodegradation pathways in selected Firmicutes oral isolates. Metabolites throughout the pathway were detected by gas chromatography coupled with mass spectroscopy (GC-MS) using anthracene as sole source of carbon. After incubation for 3 days, anthracene was undetected in the supernatant of L. fermentum and V. parvula, while a residual of 3% of anthracene was detected in presence of S. anginosus. Results revealed that anaerobic biodegradation by L. fermentum and V. parvula started with hydroxylation and dehydrogenation producing 9,10- anthraquinone and ended up with simpler structures such as catechol, while S. anginosus hydroxylation for anthracene resulted in the production of 1,2-anthracenediol and ended up with catechol and phthalic acid. The biodegradation of anthracene by oral bacteria could convert it to other toxic metabolites such as anthraquinone and catechol which were reported to have potential carcinogenic effects. Moreover, fatty acids detected as biodegradation metabolites could be one of the causes of smokers’ heart-related diseases. Thus, this study explored oral metabolites resulting from smoking under anaerobic conditions towards elucidating the role of oral microbiota in health and disease states.