Anaerobic biodegradation of phenanthrene and pyrene by sulfate-reducing cultures enriched from contaminated freshwater lake sediments

Abstract

Our current understanding of the susceptibility of hazardous polycyclic aromatic hydrocarbons (PAHs) to anaerobic microbial degradation is very limited. In the present study, we obtained phenanthrene- and pyrene-degrading strictly anaerobic sulfate-reducing enrichments using contaminated freshwater lake sediments as the source material. The highly enriched phenanthrene-degrading culture, MMKS23, was dominated (98%) by a sulfate-reducing bacterium belonging to the genus Desulfovibrio. While Desulfovibrio sp. was also predominant (79%) in the pyrene-degrading enrichment culture, MMKS44, an anoxygenic purple non-sulfur bacterium, Rhodopseudomonas sp., constituted a significant fraction (18%) of the total microbial community. Phenanthrene or pyrene biodegradation by the enrichment cultures was coupled with sulfate reduction, as evident from near stoichiometric consumption of sulfate and accumulation of sulfide. Also, there was almost complete inhibition of substrate degradation in the presence of an inhibitor of sulfate reduction, i.e., 20 mM MoO42−, in the culture medium. After 180 days of incubation, about 79.40 μM phenanthrene was degraded in the MMKS23 culture, resulting in the consumption of 806.80 μM sulfate and accumulation of 625.80 μM sulfide. Anaerobic pyrene biodegradation by the MMKS44 culture was relatively slow. About 22.30 μM of the substrate was degraded after 180 days resulting in the depletion of 239 μM sulfate and accumulation of 196.90 μM sulfide. Biodegradation of phenanthrene by the enrichment yielded a metabolite, phenanthrene-2-carboxylic acid, suggesting that carboxylation could be a widespread initial step of phenanthrene activation under sulfate-reducing conditions. Overall, this novel study demonstrates the ability of sulfate-reducing bacteria (SRB), dwelling in contaminated freshwater sediments to anaerobically biodegrade three-ringed phenanthrene and highly recalcitrant four-ringed pyrene. Our findings suggest that SRB could play a crucial role in the natural attenuation of PAHs in anoxic freshwater sediments.