Aquifer microbial communities are highly variable in response to thermal arsenic mobilization

Abstract

Thermal recovery technologies for in-situ bitumen extraction can result in the heating of surrounding aquifers, potentially mobilizing arsenic naturally present in the sediments to the groundwater. The relative toxicity of dissolved arsenic is related to its speciation, with As(V) being less toxic than As(III). Microorganisms have various mechanisms of arsenic resistance, including efflux and methylation. Microorganisms may also perform reduction/oxidation of As(V)/As(III) as part of their detoxification and/or metabolic pathways. We characterized the microbial communities along two aquifer transects associated with thermally mobilized arsenic near Northeastern Alberta oil sands deposits. 16S rRNA amplicons and metagenomic sequencing data of biomass from filtered groundwater indicated major changes in the dominant taxa between wells, especially those currently experiencing elevated arsenic concentrations. Annotation of arsenic-related genes indicated that efflux pumps (arsB, acr3), intracellular reduction (arsC) and methylation (arsM) genes were widespread amongst community members but comparatively few organisms encoded genes for arsenic respiratory reductases (arrA) and oxidases (arxA, aioA). While this indicates that microbes have the capacity to exacerbate arsenic toxicity by increasing the relative concentration of As(III), some populations of iron oxidizing and sulfate reducing bacteria (including novel Gallionella and Thermodesulfovibrionia populations) show potential for indirect bioremediation through formation of insoluble iron/sulfide minerals which adsorb or coprecipitate arsenic. An unusually high proportional abundance of a single Paceibacteria population that lacked arsenic resistance genes was identified in one high-arsenic well, and we discuss hypotheses for its ability to persist. Overall, this study describes how aquifer microbial communities respond to thermal and arsenic plumes, and predicts potential contributions of microbes to arsenic biogeochemical cycling under this disturbance.