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Title: Putative Mixotrophic Nitrifying-Denitrifying Gammaproteobacteria Implicated in Nitrogen Cycling Within the Ammonia/Oxygen Transition Zone of an Oil Sands Pit Lake

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 CO 2-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 favorsmore » 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.« less

Authors:
 [1];  [2];  [3];  [4];  [4];  [4];  [5];  [2];  [6]
  1. Univ. of Toronto, Toronto, ON (Canada); Yokohama City Univ., Yokohama (Japan)
  2. Univ. of California, Berkeley, CA (United States)
  3. Univ. of Toronto, Toronto, ON (Canada); Univ. Austral de Chile, Valdivia (Chile)
  4. Univ. of Saskatchewan, Saskatoon, SK (Canada)
  5. McMaster Univ., Hamilton, ON (Canada)
  6. Univ. of Toronto, Toronto, ON (Canada); McMaster Univ., Hamilton, ON (Canada)
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1580864
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
Frontiers in Microbiology
Additional Journal Information:
Journal Volume: 10; Journal Issue: OCT; Journal ID: ISSN 1664-302X
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; nitrifier denitrification; nitrogen cycle; oil sands; tailings deposits; shotgun metagenomics

Citation Formats

Mori, Jiro F., Chen, Lin -Xing, Jessen, Gerdhard L., Rudderham, Sarah B., McBeth, Joyce M., Lindsay, Matthew B. J., Slater, Gregory F., Banfield, Jillian F., and Warren, Lesley A. Putative Mixotrophic Nitrifying-Denitrifying Gammaproteobacteria Implicated in Nitrogen Cycling Within the Ammonia/Oxygen Transition Zone of an Oil Sands Pit Lake. United States: N. p., 2019. Web. doi:10.3389/fmicb.2019.02435.
Mori, Jiro F., Chen, Lin -Xing, Jessen, Gerdhard L., Rudderham, Sarah B., McBeth, Joyce M., Lindsay, Matthew B. J., Slater, Gregory F., Banfield, Jillian F., & Warren, Lesley A. Putative Mixotrophic Nitrifying-Denitrifying Gammaproteobacteria Implicated in Nitrogen Cycling Within the Ammonia/Oxygen Transition Zone of an Oil Sands Pit Lake. United States. doi:10.3389/fmicb.2019.02435.
Mori, Jiro F., Chen, Lin -Xing, Jessen, Gerdhard L., Rudderham, Sarah B., McBeth, Joyce M., Lindsay, Matthew B. J., Slater, Gregory F., Banfield, Jillian F., and Warren, Lesley A. Thu . "Putative Mixotrophic Nitrifying-Denitrifying Gammaproteobacteria Implicated in Nitrogen Cycling Within the Ammonia/Oxygen Transition Zone of an Oil Sands Pit Lake". United States. doi:10.3389/fmicb.2019.02435. https://www.osti.gov/servlets/purl/1580864.
@article{osti_1580864,
title = {Putative Mixotrophic Nitrifying-Denitrifying Gammaproteobacteria Implicated in Nitrogen Cycling Within the Ammonia/Oxygen Transition Zone of an Oil Sands Pit Lake},
author = {Mori, Jiro F. and Chen, Lin -Xing and Jessen, Gerdhard L. and Rudderham, Sarah B. and McBeth, Joyce M. and Lindsay, Matthew B. J. and Slater, Gregory F. and Banfield, Jillian F. and Warren, Lesley A.},
abstractNote = {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.},
doi = {10.3389/fmicb.2019.02435},
journal = {Frontiers in Microbiology},
number = OCT,
volume = 10,
place = {United States},
year = {2019},
month = {10}
}

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