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Original Research ARTICLE Provisionally accepted The full-text will be published soon. Notify me

Front. Microbiol. | doi: 10.3389/fmicb.2019.02435

Putative mixotrophic nitrifying-denitrifying Gammaproteobacteria implicated in nitrogen cycling within the ammonia/oxygen transition zone of an oil sands pit lake

  • 1Department of Civil and Mineral Engineering, Faculty of Applied Science & Engineering, University of Toronto, Canada
  • 2Graduate School of Nanobiosciences, Yokohama City University, Japan
  • 3Department of Earth and Planetary Science, University of California Berkeley, United States
  • 4Institute of Marine and Limnological Sciences, Faculty of Sciences, Universidad Austral de Chile, Chile
  • 5Department of Geological Sciences, College of Arts & Science, University of Saskatchewan, Canada
  • 6School of Geography and Earth Science, Faculty of Science, McMaster University, Canada

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 (approx. 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.

Keywords: Nitrifier denitrification, oil sands, Tailings deposits, Shotgun metagenomics, Nitrogen Cycle

Received: 24 Jul 2019; Accepted: 09 Oct 2019.

Copyright: © 2019 Mori, Chen, Jessen, Rudderham, McBeth, Lindsay, Slater, Banfield and Warren. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

* Correspondence: Prof. Lesley A. Warren, Department of Civil and Mineral Engineering, Faculty of Applied Science & Engineering, University of Toronto, Toronto, Canada, lesley.warren@utoronto.ca