Microbial interactions with magnetite enhance methane production from hydrocarbon biodegradation

Indigenous microbial communities in fine tailings (FT) biodegrade residual diluent hydrocarbons and support CH₄ emissions from oil sands tailings ponds and end-pit lakes. We investigated the effect of added crystalline Fe mineral magnetite on microbial metabolism of hydrocarbons in FT collected from methanogenically less and more active sites of an end-pit lake. Magnetite accelerated CH₄ production by enhancing the biodegradation of hydrocarbons, with a more prominent effect on complex/relatively recalcitrant aliphatics (C₈-C₁₁ compounds) and monoaromatics. Interestingly, 86-92 % of total magnetite added in FT remained stable even after the metabolism of labile hydrocarbons (∼45 % of total diluent hydrocarbons). This may be due to magnetite enabling mineralogical direct interspecies electron transfer (mDIET) rather than iron reduction to enhance the methanogenic biodegradation of hydrocarbons. Enrichment of Coriobacteriaceae along with Desulfosporosinus, Syntrophus, Peptococcaceae, Smithella, Methanosaeta, and Methanoregula in magnetite-supplemented FT during hydrocarbon biodegradation suggested their potential role in developing mDIET. These results suggest that magnetite, when present, accelerates methanogenesis and potentially may increase rather than suppress CH₄ emissions from FT, and also suggest the potential use of magnetite to accelerate bioremediation of other hydrocarbon-contaminated anaerobic environments.