Microbial metabolic strategies for overcoming low-oxygen in naturalized freshwater reservoirs surrounding the Athabasca Oil Sands: A proxy for End-Pit Lakes?

Highlights: • Seeking to provide much needed insight into large landscape reclamation end-point objectives • Insights into natural microbial metabolism in the Athabasca Oil Sands region • In-situ geochemical and gene expression surveys to understand active biogeochemistry • Hydrocarbon impact on microbial metabolism and sediment geochemistry under sub-oxic conditions -- Abstract: The success and sustainability of aquatic ecosystems are driven by the complex, cooperative metabolism of microbes. Ecological engineering strategies often strive to harness this syntrophic synergy of microbial metabolism for the reclamation of contaminated environments worldwide. Currently, there is a significant knowledge gap in our understanding of how the natural microbial ecology overcomes thermodynamic limitations in recovering contaminated environments. Here, we used in-situ metatranscriptomics and associated metataxonomic analyses on sediments collected from naturalized freshwater man-made reservoirs within the Athabasca Oil Sands region of Alberta, Canada. These reservoirs are unique since they are untouched by industrial mining processes and serve as representative endpoints for model landscape reconstruction. Results indicate that a microbial syntrophic cooperation has been established represented by the oxygenic and anoxygenic phototrophs, sustained through the efficient use of novel cellular mechanistic adaptations tailored to these unique thermodynamic conditions. Specifically, chemotaxis transcripts (cheY & MCPs-methyl-accepting chemotaxis proteins) were highly expressed, suggesting a highly active microbial response to gradients in environmental stimuli, resulting indirectly from hydrocarbon compound alteration. A high expression of photosynthetic activity, likely sustaining nutrient delivery to the similarly highly expressed methanogenic community acting in syntrophy during the breakdown of organics. Overall the more diversified functionality within sub-oxic sample locations indicates an ability to maintain efficient metabolism under thermodynamic constraints. This is the first study to holistically identify and characterize these types of in-situ, metabolic processes and address their thermodynamic feasibility within a global context for large landscape reconstruction. These characterizations of regional, natural landscapes surrounding the oil sands mining operation are severely lacking, but truly provide invaluable insight into end-point goals and targets for reclamation procedures.