Putative Mixotrophic Nitrifying-Denitrifying Gammaproteobacteria Implicated in Nitrogen Cycling Within the Ammonia/Oxygen Transition Zone of an Oil Sands Pit Lake
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, re...
| Main Authors: | , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2019-10-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/article/10.3389/fmicb.2019.02435/full |
| _version_ | 1818197921234944000 |
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| author | Jiro F. Mori Lin-Xing Chen Gerdhard L. Jessen Sarah B. Rudderham Joyce M. McBeth Matthew B. J. Lindsay Gregory F. Slater Jillian F. Banfield Lesley A. Warren Lesley A. Warren |
| author_facet | Jiro F. Mori Lin-Xing Chen Gerdhard L. Jessen Sarah B. Rudderham Joyce M. McBeth Matthew B. J. Lindsay Gregory F. Slater Jillian F. Banfield Lesley A. Warren Lesley A. Warren |
| author_sort | Jiro F. Mori |
| collection | DOAJ |
| description | 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. |
| first_indexed | 2024-12-12T01:57:39Z |
| format | Article |
| id | doaj.art-8190ce22611c498f9faae35c74a8eb2b |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-12-12T01:57:39Z |
| publishDate | 2019-10-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Microbiology |
| spelling | doaj.art-8190ce22611c498f9faae35c74a8eb2b2022-12-22T00:42:18ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2019-10-011010.3389/fmicb.2019.02435486850Putative Mixotrophic Nitrifying-Denitrifying Gammaproteobacteria Implicated in Nitrogen Cycling Within the Ammonia/Oxygen Transition Zone of an Oil Sands Pit LakeJiro F. Mori0Lin-Xing Chen1Gerdhard L. Jessen2Sarah B. Rudderham3Joyce M. McBeth4Matthew B. J. Lindsay5Gregory F. Slater6Jillian F. Banfield7Lesley A. Warren8Lesley A. Warren9Department of Civil and Mineral Engineering, University of Toronto, Toronto, ON, CanadaDepartment of Earth and Planetary Sciences, University of California, Berkeley, Berkeley, CA, United StatesDepartment of Civil and Mineral Engineering, University of Toronto, Toronto, ON, CanadaDepartment of Geological Sciences, University of Saskatchewan, Saskatoon, SK, CanadaDepartment of Geological Sciences, University of Saskatchewan, Saskatoon, SK, CanadaDepartment of Geological Sciences, University of Saskatchewan, Saskatoon, SK, CanadaSchool of Geography and Earth Science, McMaster University, Hamilton, ON, CanadaDepartment of Earth and Planetary Sciences, University of California, Berkeley, Berkeley, CA, United StatesDepartment of Civil and Mineral Engineering, University of Toronto, Toronto, ON, CanadaSchool of Geography and Earth Science, McMaster University, Hamilton, ON, CanadaAnthropogenically-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.https://www.frontiersin.org/article/10.3389/fmicb.2019.02435/fullnitrifier denitrificationnitrogen cycleoil sandstailings depositsshotgun metagenomics |
| spellingShingle | Jiro F. Mori Lin-Xing Chen Gerdhard L. Jessen Sarah B. Rudderham Joyce M. McBeth Matthew B. J. Lindsay Gregory F. Slater Jillian F. Banfield Lesley A. Warren Lesley A. Warren Putative Mixotrophic Nitrifying-Denitrifying Gammaproteobacteria Implicated in Nitrogen Cycling Within the Ammonia/Oxygen Transition Zone of an Oil Sands Pit Lake Frontiers in Microbiology nitrifier denitrification nitrogen cycle oil sands tailings deposits shotgun metagenomics |
| title | Putative Mixotrophic Nitrifying-Denitrifying Gammaproteobacteria Implicated in Nitrogen Cycling Within the Ammonia/Oxygen Transition Zone of an Oil Sands Pit Lake |
| title_full | Putative Mixotrophic Nitrifying-Denitrifying Gammaproteobacteria Implicated in Nitrogen Cycling Within the Ammonia/Oxygen Transition Zone of an Oil Sands Pit Lake |
| title_fullStr | Putative Mixotrophic Nitrifying-Denitrifying Gammaproteobacteria Implicated in Nitrogen Cycling Within the Ammonia/Oxygen Transition Zone of an Oil Sands Pit Lake |
| title_full_unstemmed | Putative Mixotrophic Nitrifying-Denitrifying Gammaproteobacteria Implicated in Nitrogen Cycling Within the Ammonia/Oxygen Transition Zone of an Oil Sands Pit Lake |
| title_short | Putative Mixotrophic Nitrifying-Denitrifying Gammaproteobacteria Implicated in Nitrogen Cycling Within the Ammonia/Oxygen Transition Zone of an Oil Sands Pit Lake |
| title_sort | putative mixotrophic nitrifying denitrifying gammaproteobacteria implicated in nitrogen cycling within the ammonia oxygen transition zone of an oil sands pit lake |
| topic | nitrifier denitrification nitrogen cycle oil sands tailings deposits shotgun metagenomics |
| url | https://www.frontiersin.org/article/10.3389/fmicb.2019.02435/full |
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