Oil in subsurface reservoirs is biodegraded by resident microbial communities. Water-mediated, anaerobic conversion of hydrocarbons to methane and CO2, catalyzed by syntrophic bacteria and methanogenic archaea, is thought to be one of the dominant processes. We compared 160 microbial community compositions in ten hydrocarbon resource environments (HREs) and sequenced twelve metagenomes to characterize their metabolic potential. Although anaerobic communities were common, cores from oil sands and coal beds had unexpectedly high proportions of aerobic hydrocarbon-degrading bacteria. Likewise, most metagenomes had high proportions of genes for enzymes involved in aerobic hydrocarbon metabolism. Hence, although HREs may have been strictly anaerobic and typically methanogenic for much of their history, this may not hold today for coal beds and for the Alberta oil sands, one of the largest remaining oil reservoirs in the world. This finding may influence strategies to recover energy or chemicals from these HREs by in situ microbial processes.

Oil sands are surface exposed in river valley outcrops in northeastern Alberta, where flat slabs (tablets) of weathered, bitumensaturated sandstone can be retrieved from outcrop cliffs or from riverbeds. Although the average yearly surface temperature of this region is low (0.7°C), we found that the temperatures of the exposed surfaces of outcrop cliffs reached 55 to 60°C on sunny summer days, with daily maxima being 27 to 31°C. Analysis of the cooccurrence of taxa derived from pyrosequencing of 16S/18S rRNA genes indicated that an aerobic microbial network of fungi and hydrocarbon-, methane-, or acetate-oxidizing heterotrophic bacteria was present in all cliff tablets. Metagenomic analyses indicated an elevated presence of fungal cytochrome P450 monooxygenases in these samples. This network was distinct from the heterotrophic community found in riverbeds, which included fewer fungi. A subset of cliff tablets had a network of anaerobic and/or thermophilic taxa, including methanogens, Firmicutes, and Thermotogae, in the center. Long-term aerobic incubation of outcrop samples at 55°C gave a thermophilic microbial community. Analysis of residual bitumen with a Fourier transform ion cyclotron resonance mass spectrometer indicated that aerobic degradation proceeded at 55°C but not at 4°C. Little anaerobic degradation was observed. These results indicate that bitumen degradation on outcrop surfaces is a largely aerobic process with a minor anaerobic contribution and is catalyzed by a consortium of bacteria and fungi. Bitumen degradation is stimulated by periodic high temperatures on outcrop cliffs, which cause significant decreases in bitumen viscosity.T he world's largest oil sands deposit, located in western Canada, is contained in Lower Cretaceous sandstone formations in the Western Canadian Sedimentary Basin at depths of 0 to 800 m below the surface (mbs) (1, 2). Surface oil sands deposits are found in river valley outcrops (Fig. 1), where they are further changed by oxidative biodegradation and weathering.Oil sands hydrocarbon formed 84 million to 55 million years ago in tide-controlled river and estuarine sediment source rock, from where it migrated upwards and eastwards to accumulate at the northeastern margins of the basin centered around Fort McMurray, Alberta, Canada (2-4). The oil became severely biodegraded during this journey and following its placement at low depth and low temperature in the Athabasca, Cold Lake, and Peace River oil sands deposits that exist today. Biodegradation of low-molecular-weight components caused the oil to become more viscous, with the viscosity ranging from 1 cP for initially formed nondegraded light oil to 10 6 cP for heavily biodegraded, eastern Athabasca oil sands bitumen, which is currently in place (5-11). Bitumen is therefore depleted of low-molecular-weight aliphatic and aromatic hydrocarbons and enriched in polyaromatic hydrocarbons (PAHs), including alkylnaphthalenes or alkylphenanthrenes, as well as in naphthenic acids (NAs), resins, and asphaltenes (12)(13)(14). The ...