Abstract
Polycyclic aromatic hydrocarbons (PAH) such as naphthalene are widespread, recalcitrant pollutants in anoxic and methanogenic environments. A mechanism catalyzing PAH activation under methanogenic conditions has yet to be discovered, and the microbial communities coordinating their metabolism are largely unknown. This is primarily due to the difficulty of cultivating PAH degraders, requiring lengthy incubations to yield sufficient biomass for biochemical analysis. Here, we sought to characterize a new methanogenic naphthalene-degrading enrichment culture using DNA-based stable isotope probing (SIP) and metagenomic analyses. 16S rRNA gene sequencing of fractionated DNA pinpointed an unclassified Clostridiaceae species as a putative naphthalene degrader after two months of SIP incubation. This finding was supported by metabolite and metagenomic evidence of genes predicted to encode for enzymes facilitating naphthalene carboxylic acid CoA-thioesterification and degradation of an unknown arylcarboxyl-CoA structure. Our findings also suggest a possible but unknown role for Desulfuromonadales in naphthalene degradation. This is the first reported functional evidence of PAH biodegradation by a methanogenic consortium, and we envision that this approach could be used to assess carbon flow through other slow growing enrichment cultures and environmental samples.
Highlights
Polycyclic aromatic hydrocarbons (PAH) are ubiquitous environmental pollutants generated during the incomplete combustion of organic materials, and from natural seepage of petroleum or coal deposits, accidental fuel releases, and volcanic activities [1]
We aimed to identify key microorganisms and reactions responsible for the initial degradation steps of the PAH naphthalene by a new methanogenic naphthalene-degrading enrichment culture using a variety of molecular ecology toolbox approaches including DNA-stable isotope probing (SIP) and metagenomic analyses
Naphthalene was not initially reported to be susceptible to methanogenic degradation by this culture, but enhanced methane production and naphthalene loss was verified by gas chromatography more than a year after the original publication date [38]. The results of this present study revealed that members of the Clostridiaceae, and possibly Desulfuromonadales, are involved in naphthalene degradation by NDC under methanogenic conditions, as these phylotypes became labeled during incubations with isotopically heavy naphthalene and/or harbored genes known to be involved in anaerobic naphthalene metabolism
Summary
Polycyclic aromatic hydrocarbons (PAH) are ubiquitous environmental pollutants generated during the incomplete combustion of organic materials (e.g., fossil fuels, refined fuel products, and wood), and from natural seepage of petroleum or coal deposits, accidental fuel releases, and volcanic activities [1]. Due to their high hydrophobicity, PAHs tend to partition and deposit in sedimentary environments, but water-soluble components (e.g., 2-to 3-ringed PAHs) are capable of migrating through anoxic groundwater systems [2]. There is no evidence to date demonstrating that ≥ 4-ringed PAHs can be metabolized anaerobically as a sole carbon source, though co-metabolic PAH degradation is possible [6,7]
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