Abstract
Anthropogenically-impacted environments offer the opportunity to discover novel microbial species and metabolisms, which may be undetectable in natural systems. Here, a combined metagenomic and geochemical study in Base Mine Lake, Alberta, Canada, which is the only oil sands end pit lake to date, revealed that nitrification was performed by members from Nitrosomonadaceae, Chloroflexi and unclassified Gammaproteobacteria “MBAE14.” While Nitrosomonadaceae and Chloroflexi groups were relatively abundant in the upper oxygenated zones, MBAE14 dominated the hypoxic hypolimnetic zones (approximately 30% of total microbial communities); MBAE14 was not detected in the underlying anoxic tailings. Replication rate analyses indicate that MBAE14 grew in metalimnetic and hypolimnetic water cap regions, most actively at the metalimnetic, ammonia/oxygen transition zone consistent with it putatively conducting nitrification. Detailed genomic analyses of MBAE14 evidenced both ammonia oxidation and denitrification into dinitrogen capabilities. However, the absence of known CO2-fixation genes suggests a heterotrophic denitrifying metabolism. Functional marker genes of ammonia oxidation (amo and hao) in the MBAE14 genome are homologous with those conserved in autotrophic nitrifiers, but not with those of known heterotrophic nitrifiers. We propose that this novel MBAE14 inhabits the specific ammonia-rich, oxygen and labile organic matter-limited conditions occurring in Base Mine Lake which selectively favors mixotrophic coupled nitrifier denitrification metabolism. Our results highlight the opportunities to better constrain biogeochemical cycles from the application of metagenomics to engineered systems associated with extractive resource sectors.
Highlights
The biogeochemical nitrogen cycle involves many microbiallycatalyzed forward and reverse redox reactions that interconvert nitrate, nitrite, ammonia, nitric acid, nitrous oxide, and dinitrogen species
The highest level of dissolved aqueous methane concentration (∼70 μM) in the water cap was detected at the lower hypolimnetic zone
Nitrite and ammonia were detectable throughout the water cap in both years, which were with higher concentrations in 2015 compared to 2016
Summary
The biogeochemical nitrogen cycle involves many microbiallycatalyzed forward and reverse redox reactions that interconvert nitrate, nitrite, ammonia, nitric acid, nitrous oxide, and dinitrogen species. Previous culture-independent surveys indicate the ubiquitous existence of aerobic nitrifiers in natural environments, they rarely dominate communities, and often face competition for ammonia and oxygen with heterotrophs (Geets et al, 2006). They do succeed in ammonium-rich, aerated, and organic matter-limited conditions found in engineered systems such as wastewater treatment systems (Dionisi et al, 2002; Kuypers et al, 2018). The specific targeting of anthropogenic, ammonia-rich environments may reveal novel nitrifying players that may be present in natural environments as members of the rare biosphere
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