Subsurface biogeochemical cycling of nitrogen in the actively serpentinizing Samail Ophiolite, Oman
Nitrogen (N) is an essential element for life. N compounds such as ammonium (NH4+) may act as electron donors, while nitrate (NO3-) and nitrite (NO2-) may serve as electron acceptors to support energy metabolism. However, little is known regarding the availability and forms of N in subsurface ecosys...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2023-04-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fmicb.2023.1139633/full |
| _version_ | 1797843308804833280 |
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| author | Kaitlin R. Rempfert Daniel B. Nothaft Emily A. Kraus Ciara K. Asamoto R. Dave Evans John R. Spear John R. Spear Juerg M. Matter Sebastian H. Kopf Alexis S. Templeton |
| author_facet | Kaitlin R. Rempfert Daniel B. Nothaft Emily A. Kraus Ciara K. Asamoto R. Dave Evans John R. Spear John R. Spear Juerg M. Matter Sebastian H. Kopf Alexis S. Templeton |
| author_sort | Kaitlin R. Rempfert |
| collection | DOAJ |
| description | Nitrogen (N) is an essential element for life. N compounds such as ammonium (NH4+) may act as electron donors, while nitrate (NO3-) and nitrite (NO2-) may serve as electron acceptors to support energy metabolism. However, little is known regarding the availability and forms of N in subsurface ecosystems, particularly in serpentinite-hosted settings where hydrogen (H2) generated through water–rock reactions promotes habitable conditions for microbial life. Here, we analyzed N and oxygen (O) isotope composition to investigate the source, abundance, and cycling of N species within the Samail Ophiolite of Oman. The dominant dissolved N species was dependent on the fluid type, with Mg2+-HCO3- type fluids comprised mostly of NO3-, and Ca2+-OH− fluids comprised primarily of ammonia (NH3). We infer that fixed N is introduced to the serpentinite aquifer as NO3-. High concentrations of NO3- (>100 μM) with a relict meteoric oxygen isotopic composition (δ18O ~ 22‰, Δ17O ~ 6‰) were observed in shallow aquifer fluids, indicative of NO3- sourced from atmospheric deposition (rainwater NO3-: δ18O of 53.7‰, Δ17O of 16.8‰) mixed with NO3- produced in situ through nitrification (estimated endmember δ18O and Δ17O of ~0‰). Conversely, highly reacted hyperalkaline fluids had high concentrations of NH3 (>100 μM) with little NO3- detectable. We interpret that NH3 in hyperalkaline fluids is a product of NO3- reduction. The proportionality of the O and N isotope fractionation (18ε / 15ε) measured in Samail Ophiolite NO3- was close to unity (18ε / 15ε ~ 1), which is consistent with dissimilatory NO3- reduction with a membrane-bound reductase (NarG); however, abiotic reduction processes may also be occurring. The presence of genes commonly involved in N reduction processes (narG, napA, nrfA) in the metagenomes of biomass sourced from aquifer fluids supports potential biological involvement in the consumption of NO3-. Production of NH4+ as the end-product of NO3- reduction via dissimilatory nitrate reduction to ammonium (DNRA) could retain N in the subsurface and fuel nitrification in the oxygenated near surface. Elevated bioavailable N in all sampled fluids indicates that N is not likely limiting as a nutrient in serpentinites of the Samail Ophiolite. |
| first_indexed | 2024-04-09T17:03:03Z |
| format | Article |
| id | doaj.art-64bfd3fd46474ed284fd01720035f527 |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-04-09T17:03:03Z |
| publishDate | 2023-04-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Microbiology |
| spelling | doaj.art-64bfd3fd46474ed284fd01720035f5272023-04-21T04:19:12ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2023-04-011410.3389/fmicb.2023.11396331139633Subsurface biogeochemical cycling of nitrogen in the actively serpentinizing Samail Ophiolite, OmanKaitlin R. Rempfert0Daniel B. Nothaft1Emily A. Kraus2Ciara K. Asamoto3R. Dave Evans4John R. Spear5John R. Spear6Juerg M. Matter7Sebastian H. Kopf8Alexis S. Templeton9Department of Geological Sciences, University of Colorado, Boulder, CO, United StatesDepartment of Geological Sciences, University of Colorado, Boulder, CO, United StatesDepartment of Civil and Environmental Engineering, Colorado School of Mines, Golden, CO, United StatesDepartment of Geological Sciences, University of Colorado, Boulder, CO, United StatesSchool of Biological Sciences, Washington State University, Pullman, WA, United StatesDepartment of Civil and Environmental Engineering, Colorado School of Mines, Golden, CO, United StatesQuantitative Biosciences and Engineering, Colorado School of Mines, Golden, CO, United StatesNational Oceanography Centre, University of Southampton, Southampton, United KingdomDepartment of Geological Sciences, University of Colorado, Boulder, CO, United StatesDepartment of Geological Sciences, University of Colorado, Boulder, CO, United StatesNitrogen (N) is an essential element for life. N compounds such as ammonium (NH4+) may act as electron donors, while nitrate (NO3-) and nitrite (NO2-) may serve as electron acceptors to support energy metabolism. However, little is known regarding the availability and forms of N in subsurface ecosystems, particularly in serpentinite-hosted settings where hydrogen (H2) generated through water–rock reactions promotes habitable conditions for microbial life. Here, we analyzed N and oxygen (O) isotope composition to investigate the source, abundance, and cycling of N species within the Samail Ophiolite of Oman. The dominant dissolved N species was dependent on the fluid type, with Mg2+-HCO3- type fluids comprised mostly of NO3-, and Ca2+-OH− fluids comprised primarily of ammonia (NH3). We infer that fixed N is introduced to the serpentinite aquifer as NO3-. High concentrations of NO3- (>100 μM) with a relict meteoric oxygen isotopic composition (δ18O ~ 22‰, Δ17O ~ 6‰) were observed in shallow aquifer fluids, indicative of NO3- sourced from atmospheric deposition (rainwater NO3-: δ18O of 53.7‰, Δ17O of 16.8‰) mixed with NO3- produced in situ through nitrification (estimated endmember δ18O and Δ17O of ~0‰). Conversely, highly reacted hyperalkaline fluids had high concentrations of NH3 (>100 μM) with little NO3- detectable. We interpret that NH3 in hyperalkaline fluids is a product of NO3- reduction. The proportionality of the O and N isotope fractionation (18ε / 15ε) measured in Samail Ophiolite NO3- was close to unity (18ε / 15ε ~ 1), which is consistent with dissimilatory NO3- reduction with a membrane-bound reductase (NarG); however, abiotic reduction processes may also be occurring. The presence of genes commonly involved in N reduction processes (narG, napA, nrfA) in the metagenomes of biomass sourced from aquifer fluids supports potential biological involvement in the consumption of NO3-. Production of NH4+ as the end-product of NO3- reduction via dissimilatory nitrate reduction to ammonium (DNRA) could retain N in the subsurface and fuel nitrification in the oxygenated near surface. Elevated bioavailable N in all sampled fluids indicates that N is not likely limiting as a nutrient in serpentinites of the Samail Ophiolite.https://www.frontiersin.org/articles/10.3389/fmicb.2023.1139633/fullserpentinizationwater–rock interactiondeep subsurface biospherenitratenitrogen isotopesnitrogen |
| spellingShingle | Kaitlin R. Rempfert Daniel B. Nothaft Emily A. Kraus Ciara K. Asamoto R. Dave Evans John R. Spear John R. Spear Juerg M. Matter Sebastian H. Kopf Alexis S. Templeton Subsurface biogeochemical cycling of nitrogen in the actively serpentinizing Samail Ophiolite, Oman Frontiers in Microbiology serpentinization water–rock interaction deep subsurface biosphere nitrate nitrogen isotopes nitrogen |
| title | Subsurface biogeochemical cycling of nitrogen in the actively serpentinizing Samail Ophiolite, Oman |
| title_full | Subsurface biogeochemical cycling of nitrogen in the actively serpentinizing Samail Ophiolite, Oman |
| title_fullStr | Subsurface biogeochemical cycling of nitrogen in the actively serpentinizing Samail Ophiolite, Oman |
| title_full_unstemmed | Subsurface biogeochemical cycling of nitrogen in the actively serpentinizing Samail Ophiolite, Oman |
| title_short | Subsurface biogeochemical cycling of nitrogen in the actively serpentinizing Samail Ophiolite, Oman |
| title_sort | subsurface biogeochemical cycling of nitrogen in the actively serpentinizing samail ophiolite oman |
| topic | serpentinization water–rock interaction deep subsurface biosphere nitrate nitrogen isotopes nitrogen |
| url | https://www.frontiersin.org/articles/10.3389/fmicb.2023.1139633/full |
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