Articles | Volume 21, issue 14
https://doi.org/10.5194/bg-21-3215-2024
© Author(s) 2024. This work is distributed under
the Creative Commons Attribution 4.0 License.
the Creative Commons Attribution 4.0 License.
https://doi.org/10.5194/bg-21-3215-2024
© Author(s) 2024. This work is distributed under
the Creative Commons Attribution 4.0 License.
the Creative Commons Attribution 4.0 License.
Research article
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17 Jul 2024
Research article | Highlight paper |
| 17 Jul 2024
| 17 Jul 2024
Isotopomer labeling and oxygen dependence of hybrid nitrous oxide production
Department of Earth System Science, Stanford University, Stanford, CA 94305, USA
Department of Marine Chemistry and Geochemistry, Woods Hole Oceanographic Institution, Woods Hole, MA 02543, USA
Nicole M. Travis
Department of Earth System Science, Stanford University, Stanford, CA 94305, USA
Pascale Anabelle Baya
Department of Earth System Science, Stanford University, Stanford, CA 94305, USA
Claudia Frey
Department of Environmental Science, University of Basel, Basel, Switzerland
Department of Global Ecology, Carnegie Institution for Science, Stanford, CA 94305, USA
Bess B. Ward
Department of Geosciences, Princeton University, Princeton, NJ 08544, USA
Karen L. Casciotti
Department of Earth System Science, Stanford University, Stanford, CA 94305, USA
Oceans Department, Stanford University, Stanford, CA 94305, USA
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Nitrification and nitrifiers play an important role in marine nitrogen and carbon cycles by converting ammonium to nitrite and nitrate. Nitrification could affect microbial community structure, marine productivity, and the production of nitrous oxide – a powerful greenhouse gas. We introduce the newly constructed database of nitrification and nitrifiers in the marine water column and guide future research efforts in field observations and model development of nitrification.
John C. Tracey, Andrew R. Babbin, Elizabeth Wallace, Xin Sun, Katherine L. DuRussel, Claudia Frey, Donald E. Martocello III, Tyler Tamasi, Sergey Oleynik, and Bess B. Ward
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Kai G. Schulz, Eric P. Achterberg, Javier Arístegui, Lennart T. Bach, Isabel Baños, Tim Boxhammer, Dirk Erler, Maricarmen Igarza, Verena Kalter, Andrea Ludwig, Carolin Löscher, Jana Meyer, Judith Meyer, Fabrizio Minutolo, Elisabeth von der Esch, Bess B. Ward, and Ulf Riebesell
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Upwelling of nutrient-rich deep waters to the surface make eastern boundary upwelling systems hot spots of marine productivity. This leads to subsurface oxygen depletion and the transformation of bioavailable nitrogen into inert N2. Here we quantify nitrogen loss processes following a simulated deep water upwelling. Denitrification was the dominant process, and budget calculations suggest that a significant portion of nitrogen that could be exported to depth is already lost in the surface ocean.
Amal Jayakumar and Bess B. Ward
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Diversity and community composition of nitrogen-fixing microbes in the three main oxygen minimum zones of the world ocean were investigated using nifH clone libraries. Representatives of three main clusters of nifH genes were detected. Sequences were most diverse in the surface waters. The most abundant OTUs were affiliated with Alpha- and Gammaproteobacteria. The sequences were biogeographically distinct and the dominance of a few OTUs was commonly observed in OMZs in this (and other) studies.
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Biogeosciences, 17, 5809–5828, https://doi.org/10.5194/bg-17-5809-2020, https://doi.org/10.5194/bg-17-5809-2020, 2020
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The oceans are a net source of the major greenhouse gases; however there has been little coordination of oceanic methane and nitrous oxide measurements. The scientific community has recently embarked on a series of capacity-building exercises to improve the interoperability of dissolved methane and nitrous oxide measurements. This paper derives from a workshop which discussed the challenges and opportunities for oceanic methane and nitrous oxide research in the near future.
Cited articles
Babbin, A. R., Bianchi, D., Jayakumar, A., and Ward, B. B.: Rapid nitrous oxide cycling in the suboxic ocean, Science, 348, 1127–1129, https://doi.org/10.1126/science.aaa8380, 2015.
Bianchi, D., Weber, T. S., Kiko, R., and Deutsch, C.: Global niche of marine anaerobic metabolisms expanded by particle microenvironments, Nat. Geosci., 11, 263–268, https://doi.org/10.1038/s41561-018-0081-0, 2018.
Bianchi, D., McCoy, D., and Yang, S.: Formulation, optimization, and sensitivity of NitrOMZv1.0, a biogeochemical model of the nitrogen cycle in oceanic oxygen minimum zones, Geosci. Model Dev., 16, 3581–3609, https://doi.org/10.5194/gmd-16-3581-2023, 2023.
Böhlke, J. K., Mroczkowski, S. J., and Coplen, T. B.: Oxygen isotopes in nitrate: new reference materials for 18O : 17O : 16O measurements and observations on nitrate-water equilibration, Rapid Commun. Mass Sp., 17, 1835–1846, https://doi.org/10.1002/rcm.1123, 2003.
Bourbonnais, A., Letscher, R. T., Bange, H. W., Échevin, V., Larkum, J., Mohn, J., Yoshida, N., and Altabet, M. A.: N2O production and consumption from stable isotopic and concentration data in the Peruvian coastal upwelling system, Global Biogeochem. Cy., 31, 678–698, https://doi.org/10.1002/2016GB005567, 2017.
Bourbonnais, A., Chang, B. X., Sonnerup, R. E., Doney, S. C., and Altabet, M. A.: Marine N2O cycling from high spatial resolution concentration, stable isotopic and isotopomer measurements along a meridional transect in the eastern Pacific Ocean, Front. Mar. Sci., 10, 1137064, https://doi.org/10.3389/fmars.2023.1137064, 2023.
Breitburg, D., Levin, L. A., Oschlies, A., Grégoire, M., Chavez, F. P., Conley, D. J., Garçon, V., Gilbert, D., Gutiérrez, D., Isensee, K., Jacinto, G. S., Limburg, K. E., Montes, I., Naqvi, S. W. A., Pitcher, G. C., Rabalais, N. N., Roman, M. R., Rose, K. A., Seibel, B. A., Telszewski, M., Yasuhara, M., and Zhang, J.: Declining oxygen in the global ocean and coastal waters, Science, 359, eaam7240, https://doi.org/10.1126/science.aam7240, 2018.
Brenninkmeijer, C. A. M. and Röckmann, T.: Mass spectrometry of the intramolecular nitrogen isotope distribution of environmental nitrous oxide using fragment-ion analysis, Rapid Commun. Mass Sp., 13, 2028–2033, https://doi.org/10.1002/(SICI)1097-0231(19991030)13:20<2028::AID-RCM751>3.0.CO;2-J, 1999.
Buchwald, C., Santoro, A. E., Stanley, R. H. R., and Casciotti, K. L.: Nitrogen cycling in the secondary nitrite maximum of the eastern tropical North Pacific off Costa Rica, Gloal Biogeochem. Cy., 29, 2061–2081, https://doi.org/10.1002/2015GB005187, 2015.
Busecke, J. J. M., Resplandy, L., Ditkovsky, S. J., and John, J. G.: Diverging Fates of the Pacific Ocean Oxygen Minimum Zone and Its Core in a Warming World, AGU Adv., 3, e2021AV000470, https://doi.org/10.1029/2021AV000470, 2022.
Cabré, A., Marinov, I., Bernardello, R., and Bianchi, D.: Oxygen minimum zones in the tropical Pacific across CMIP5 models: mean state differences and climate change trends, Biogeosciences, 12, 5429–5454, https://doi.org/10.5194/bg-12-5429-2015, 2015.
Carini, P., Dupont, C. L., and Santoro, A. E.: Patterns of thaumarchaeal gene expression in culture and diverse marine environments, Environ. Microbiol., 20, 2112–2124, https://doi.org/10.1111/1462-2920.14107, 2018.
Casciotti, K. L.: Nitrite isotopes as tracers of marine N cycle processes, Philos. T. R. Soc. A, 374, 20150295, https://doi.org/10.1098/rsta.2015.0295, 2016.
Casciotti, K. L., Sigman, D. M., Hastings, M. G., Böhlke, J. K., and Hilkert, A.: Measurement of the Oxygen Isotopic Composition of Nitrate in Seawater and Freshwater Using the Denitrifier Method, Anal. Chem., 74, 4905–4912, https://doi.org/10.1021/ac020113w, 2002.
Casciotti, K. L., Böhlke, J. K., McIlvin, M. R., Mroczkowski, S. J., and Hannon, J. E.: Oxygen Isotopes in Nitrite: Analysis, Calibration, and Equilibration, Anal. Chem., 79, 2427–2436, https://doi.org/10.1021/ac061598h, 2007.
Casciotti, K. L., Forbes, M., Vedamati, J., Peters, B. D., Martin, T. S., and Mordy, C. W.: Nitrous oxide cycling in the Eastern Tropical South Pacific as inferred from isotopic and isotopomeric data, Deep-Sea Res. Pt. II, 156, 155–167, https://doi.org/10.1016/j.dsr2.2018.07.014, 2018.
Codispoti, L. A. and Christensen, J. P.: Nitrification, denitrification and nitrous oxide cycling in the eastern tropical South Pacific ocean, Mar. Chem., 16, 277–300, https://doi.org/10.1016/0304-4203(85)90051-9, 1985.
Cohen, Y. and Gordon, L. I.: Nitrous oxide production in the Ocean, J. Geophys. Res.-Ocean., 84, 347–353, https://doi.org/10.1029/JC084iC01p00347, 1979.
Dalsgaard, T., Stewart, F. J., Thamdrup, B., Brabandere, L. D., Revsbech, N. P., Ulloa, O., Canfield, D. E., and DeLong, E. F.: Oxygen at Nanomolar Levels Reversibly Suppresses Process Rates and Gene Expression in Anammox and Denitrification in the Oxygen Minimum Zone off Northern Chile, mBio, 5, e01966-14, https://doi.org/10.1128/mBio.01966-14, 2014.
Farías, L., Castro-González, M., Cornejo, M., Charpentier, J., Faúndez, J., Boontanon, N., and Yoshida, N.: Denitrification and nitrous oxide cycling within the upper oxycline of the eastern tropical South Pacific oxygen minimum zone, Limnol. Oceanogr., 54, 132–144, https://doi.org/10.4319/lo.2009.54.1.0132, 2009.
Farías, L., Faúndez, J., Fernández, C., Cornejo, M., Sanhueza, S., and Carrasco, C.: Biological N2O fixation in the Eastern South Pacific Ocean and marine cyanobacterial cultures, PloS One, 8, e63956, https://doi.org/10.1371/journal.pone.0063956, 2013.
Frame, C. H. and Casciotti, K. L.: Biogeochemical controls and isotopic signatures of nitrous oxide production by a marine ammonia-oxidizing bacterium, Biogeosciences, 7, 2695–2709, https://doi.org/10.5194/bg-7-2695-2010, 2010.
Frame, C. H., Lau, E., Nolan, E. J. I., Goepfert, T. J., and Lehmann, M. F.: Acidification Enhances Hybrid N2O Production Associated with Aquatic Ammonia-Oxidizing Microorganisms, Front. Microbiol., 7, 2104, https://doi.org/10.3389/fmicb.2016.02104, 2017.
Frey, C., Bange, H. W., Achterberg, E. P., Jayakumar, A., Löscher, C. R., Arévalo-Martínez, D. L., León-Palmero, E., Sun, M., Sun, X., Xie, R. C., Oleynik, S., and Ward, B. B.: Regulation of nitrous oxide production in low-oxygen waters off the coast of Peru, Biogeosciences, 17, 2263–2287, https://doi.org/10.5194/bg-17-2263-2020, 2020.
Frey, C., Sun, X., Szemberski, L., Casciotti, K. L., Garcia-Robledo, E., Jayakumar, A., Kelly, C. L., Lehmann, M. F., and Ward, B. B.: Kinetics of nitrous oxide production from ammonia oxidation in the Eastern Tropical North Pacific, Limnol. Oceanogr., 68, 424–438, https://doi.org/10.1002/lno.12283, 2023.
Garcia, H. E. and Gordon, L. I.: Oxygen Solubility in Seawater: Better Fitting Equations, Limnol. Oceanogr., 37, 1307–1312, 1992.
Goreau, T. J., Kaplan, W. A., Wofsy, S. C., McElroy, M. B., Valois, F. W., and Watson, S. W.: Production of NO
Granger, J. and Sigman, D. M.: Removal of nitrite with sulfamic acid for nitrate N and O isotope analysis with the denitrifier method, Rapid Commun. Mass Sp., 23, 3753–3762, https://doi.org/10.1002/rcm.4307, 2009.
Grasshoff, K., Ehrhardt, M., Kremling, K., and Anderson, L. G. (Eds.): Methods of seawater analysis, 3rd, completely rev. and extended ed ed., Wiley-VCH, Weinheim, New York, 600 pp., 1999.
Hink, L., Nicol, G. W., and Prosser, J. I.: Archaea produce lower yields of N 2 O than bacteria during aerobic ammonia oxidation in soil: N 2 O production by soil ammonia oxidisers, Environ. Microbiol., 19, 4829–4837, https://doi.org/10.1111/1462-2920.13282, 2017a.
Hink, L., Lycus, P., Gubry-Rangin, C., Frostegård, Å., Nicol, G. W., Prosser, J. I., and Bakken, L. R.: Kinetics of NH3-oxidation, NO-turnover, N2O-production and electron flow during oxygen depletion in model bacterial and archaeal ammonia oxidisers, Environ. Microbiol., 19, 4882–4896, https://doi.org/10.1111/1462-2920.13914, 2017b.
Holmes, R. M., Aminot, A., Kérouel, R., Hooker, B. A., and Peterson, B. J.: A simple and precise method for measuring ammonium in marine and freshwater ecosystems, Can. J. Fish. Aquat. Sci., 56, 1801–1808, https://doi.org/10.1139/f99-128, 1999.
Ji, Q., Babbin, A. R., Jayakumar, A., Oleynik, S., and Ward, B. B.: Nitrous oxide production by nitrification and denitrification in the Eastern Tropical South Pacific oxygen minimum zone, Geophys. Res. Lett., 42, 10755–10764, https://doi.org/10.1002/2015GL066853, 2015.
Ji, Q., Buitenhuis, E., Suntharalingam, P., Sarmiento, J. L., and Ward, B. B.: Global Nitrous Oxide Production Determined by Oxygen Sensitivity of Nitrification and Denitrification, Global Biogeochem. Cy., 32, 1790–1802, https://doi.org/10.1029/2018GB005887, 2018.
Kaiser, J., Park, S., Boering, K. A., Brenninkmeijer, C. A. M., Hilkert, A., and Röckmann, T.: Mass spectrometric method for the absolute calibration of the intramolecular nitrogen isotope distribution in nitrous oxide, Anal. Bioanal. Chem., 378, 256–269, https://doi.org/10.1007/s00216-003-2233-2, 2004.
Kantnerová, K., Hattori, S., Toyoda, S., Yoshida, N., Emmenegger, L., Bernasconi, S. M., and Mohn, J.: Clumped isotope signatures of nitrous oxide formed by bacterial denitrification, Geochim. Cosmochim. Ac., 328, 120–129, https://doi.org/10.1016/j.gca.2022.05.006, 2022.
Kelly, C. L.: ckelly314/pyisotopomer: v1.0.4, Zenodo [code], https://doi.org/10.5281/zenodo.7552724, 2023.
Kelly, C. L.: ckelly314/isotopomer-soup: Second release of isotopomer-soup (v0.0.2), Zenodo [code], https://doi.org/10.5281/zenodo.11475416, 2024.
Kelly, C. L. and Casciotti, K. L.: Data in support of “Isotopomer labeling and oxygen dependence of hybrid nitrous oxide production” from the Eastern Tropical North Pacific, Stanford Digital Repository [data set], https://doi.org/10.25740/ss974md4840, 2023.
Kelly, C. L., Travis, N. M., Baya, P. A., and Casciotti, K. L.: Quantifying Nitrous Oxide Cycling Regimes in the Eastern Tropical North Pacific Ocean With Isotopomer Analysis, Global Biogeochem. Cy., 35, e2020GB006637, https://doi.org/10.1029/2020GB006637, 2021.
Kelly, C. L., Manning, C., Frey, C., Kaiser, J., Gluschankoff, N., and Casciotti, K. L.: Pyisotopomer: A Python package for obtaining intramolecular isotope ratio differences from mass spectrometric analysis of nitrous oxide isotopocules, Rapid Commun. Mass Sp., 37, e9513, https://doi.org/10.1002/rcm.9513, 2023.
Kim, K.-R. and Craig, H.: Two-isotope characterization of N2O in the Pacific Ocean and constraints on its origin in deep water, Nature, 347, 58–61, https://doi.org/10.1038/347058a0, 1990.
Kozlowski, J. A., Kits, K. D., and Stein, L. Y.: Comparison of Nitrogen Oxide Metabolism among Diverse Ammonia-Oxidizing Bacteria, Front. Microbiol., 7, 1090, https://doi.org/10.3389/fmicb.2016.01090, 2016.
Kraft, B., Jehmlich, N., Larsen, M., Bristow, L. A., Könneke, M., Thamdrup, B., and Canfield, D. E.: Oxygen and nitrogen production by an ammonia-oxidizing archaeon, Science, 375, 97–100, https://doi.org/10.1126/science.abe6733, 2022.
Kuypers, M. M. M., Marchant, H. K., and Kartal, B.: The microbial nitrogen-cycling network, Nat. Rev. Microbiol., 16, 263–276, https://doi.org/10.1038/nrmicro.2018.9, 2018.
Lancaster, K. M., Caranto, J. D., Majer, S. H., and Smith, M. A.: Alternative Bioenergy: Updates to and Challenges in Nitrification Metalloenzymology, Joule, 2, 421–441, https://doi.org/10.1016/j.joule.2018.01.018, 2018.
Lazo-Murphy, B. M., Larson, S., Staines, S., Bruck, H., McHenry, J., Bourbonnais, A., and Peng, X.: Nitrous oxide production and isotopomer composition by fungi isolated from salt marsh sediments, Front. Mar. Sci., 9, 1098508, https://doi.org/10.3389/fmars.2022.1098508, 2022.
Lipschultz, F.: Chap. 31 – Isotope Tracer Methods for Studies of the Marine Nitrogen Cycle, in: Nitrogen in the Marine Environment, 2nd Edn., edited by: Capone, D. G., Bronk, D. A., Mulholland, M. R., and Carpenter, E. J., Academic Press, San Diego, 1345–1384, https://doi.org/10.1016/B978-0-12-372522-6.00031-1, 2008.
Magyar, P. M., Orphan, V. J., and Eiler, J. M.: Measurement of rare isotopologues of nitrous oxide by high-resolution multi-collector mass spectrometry, Rapid Commun. Mass Sp., 30, 1923–1940, https://doi.org/10.1002/rcm.7671, 2016.
Martens-Habbena, W., Qin, W., Horak, R. E. A., Urakawa, H., Schauer, A. J., Moffett, J. W., Armbrust, E. V., Ingalls, A. E., Devol, A. H., and Stahl, D. A.: The production of nitric oxide by marine ammonia-oxidizing archaea and inhibition of archaeal ammonia oxidation by a nitric oxide scavenger, Environ. Microbiol., 17, 2261–2274, https://doi.org/10.1111/1462-2920.12677, 2015.
McIlvin, M. R. and Altabet, M. A.: Chemical Conversion of Nitrate and Nitrite to Nitrous Oxide for Nitrogen and Oxygen Isotopic Analysis in Freshwater and Seawater, Anal. Chem., 77, 5589–5595, https://doi.org/10.1021/ac050528s, 2005.
McIlvin, M. R. and Casciotti, K. L.: Fully automated system for stable isotopic analyses of dissolved nitrous oxide at natural abundance levels, Limnol. Oceanogr. Method., 8, 54–66, https://doi.org/10.4319/lom.2010.8.54, 2010.
McIlvin, M. R. and Casciotti, K. L.: Technical updates to the bacterial method for nitrate isotopic analyses, Anal. Chem., 83, 1850–1856, https://doi.org/10.1021/ac1028984, 2011.
Monreal, P. J., Kelly, C. L., Travis, N. M., and Casciotti, K. L.: Identifying the Sources and Drivers of Nitrous Oxide Accumulation in the Eddy-Influenced Eastern Tropical North Pacific Oxygen-Deficient Zone, Global Biogeochem. Cy., 36, e2022GB007310, https://doi.org/10.1029/2022GB007310, 2022.
Naqvi, S. W. A., Jayakumar, D. A., Narvekar, P. V., Naik, H., Sarma, V. V. S. S., D'Souza, W., Joseph, S., and George, M. D.: Increased marine production of N2O due to intensifying anoxia on the Indian continental shelf, Nature, 408, 346–349, https://doi.org/10.1038/35042551, 2000.
Nelder, J. A. and Mead, R.: A Simplex Method for Function Minimization, Comput. J., 7, 308–313, https://doi.org/10.1093/comjnl/7.4.308, 1965.
Nevison, C., Butler, J. H., and Elkins, J. W.: Global distribution of N2O and the Delta N2O-AOU yield in the subsurface ocean, Global Biogeochem. Cy., 17, 1119, https://doi.org/10.1029/2003GB002068, 2003.
NOAA/National Weather Service: Cold and Warm Episodes by Season, National Weather Service Climate Prediction Center [data set], https://origin.cpc.ncep.noaa.gov/products/analysis_monitoring/ensostuff/ONI_v5.php, last access: 20 July 2020.
Oschlies, A., Brandt, P., Stramma, L., and Schmidtko, S.: Drivers and mechanisms of ocean deoxygenation, Nat. Geosci., 11, 467–473, https://doi.org/10.1038/s41561-018-0152-2, 2018.
Peng, X. and Valentine, D. L.: Diversity and N2O Production Potential of Fungi in an Oceanic Oxygen Minimum Zone, J. Fungi, 7, 218, https://doi.org/10.3390/jof7030218, 2021.
Popp, B. N., Westley, M. B., Toyoda, S., Miwa, T., Dore, J. E., Yoshida, N., Rust, T. M., Sansone, F. J., Russ, M. E., Ostrom, N. E., and Ostrom, P. H.: Nitrogen and oxygen isotopomeric constraints on the origins and sea-to-air flux of N2O in the oligotrophic subtropical North Pacific gyre, Global Biogeochem. Cy., 16, 12-1–12-10, https://doi.org/10.1029/2001GB001806, 2002.
Rahn, T. and Wahlen, M.: A reassessment of the global isotopic budget of atmospheric nitrous oxide, Global Biogeochem. Cy., 14, 537–543, https://doi.org/10.1029/1999GB900070, 2000.
Rohe, L., Anderson, T.-H., Braker, G., Flessa, H., Giesemann, A., Lewicka-Szczebak, D., Wrage-Mönnig, N., and Well, R.: Dual isotope and isotopomer signatures of nitrous oxide from fungal denitrification – a pure culture study, Rapid Commun. Mass Sp., 28, 1893–1903, https://doi.org/10.1002/rcm.6975, 2014.
Schmidtko, S., Stramma, L., and Visbeck, M.: Decline in global oceanic oxygen content during the past five decades, Nature, 542, 335–339, https://doi.org/10.1038/nature21399, 2017.
Shoun, H., Fushinobu, S., Jiang, L., Kim, S.-W., and Wakagi, T.: Fungal denitrification and nitric oxide reductase cytochrome P450nor, Philos. Trans. Biol. Sci., 367, 1186–1194, 2012.
Si, Y., Zhu, Y., Sanders, I., Kinkel, D. B., Purdy, K. J., and Trimmer, M.: Direct biological fixation provides a freshwater sink for N2O, Nat. Commun., 14, 6775, https://doi.org/10.1038/s41467-023-42481-2, 2023.
Sigman, D. M., Casciotti, K. L., Andreani, M., Barford, C., Galanter, M., and Böhlke, J. K.: A Bacterial Method for the Nitrogen Isotopic Analysis of Nitrate in Seawater and Freshwater, Anal. Chem., 73, 4145–4153, https://doi.org/10.1021/ac010088e, 2001.
Smith, C., Nicholls, Z. R. J., Armour, K., Collins, W., Dufresne, J.-L., Frame, D., Lunt, D. J., Mauritsen, M. D., Palmer, M. D., Watanabe, M., Wild, M., and Zhang, H.: The Earth's Energy Budget, Climate Feedbacks, and Climate Sensitivity Supplementary Material, in: Climate Change 2021: The Physical Science Basis, Contribution of Working Group I to the Sixth Assessment Report of the Intergovernmental Panel on Climate Change, edited by: Masson-Delmotte, V., Zhai, P., Pirani, A., Connors, S. L., Péan, C., Berger, S., Caud, N., Chen, Y., Goldfarb, L., Gomis, M. I., Huang, M., Leitzell, K., Lonnoy, E., Matthews, J. B. R., Maycock, T. K., Waterfield, T., Yelekçi, O., Yu, R., and Zhou, B., Cambridge University Press, Cambridge, United Kingdom, ISBN: 978-1-00-915789-6, https://doi.org/10.1017/9781009157896, 2021.
Smriga, S., Ciccarese, D., and Babbin, A. R.: Denitrifying bacteria respond to and shape microscale gradients within particulate matrices, Commun. Biol., 4, 570, https://doi.org/10.1038/s42003-021-02102-4, 2021.
Stein, L. Y.: Insights into the physiology of ammonia-oxidizing microorganisms, Curr. Opin. Chem. Biol., 49, 9–15, https://doi.org/10.1016/j.cbpa.2018.09.003, 2019.
Stein, L. Y. and Yung, Y. L.: Production, Isotopic Composition, and Atmospheric Fate of Biologically Produced Nitrous Oxide, Annu. Rev. Earth Pl. Sc., 31, 329–356, https://doi.org/10.1146/annurev.earth.31.110502.080901, 2003.
Stieglmeier, M., Mooshammer, M., Kitzler, B., Wanek, W., Zechmeister-Boltenstern, S., Richter, A., and Schleper, C.: Aerobic nitrous oxide production through N-nitrosating hybrid formation in ammonia-oxidizing archaea, ISME J., 8, 1135–1146, https://doi.org/10.1038/ismej.2013.220, 2014.
Stramma, L., Johnson, G. C., Sprintall, J., and Mohrholz, V.: Expanding Oxygen-Minimum Zones in the Tropical Oceans, Science, 320, 655–658, https://doi.org/10.1126/science.1153847, 2008.
Sun, X., Ji, Q., Jayakumar, A., and Ward, B. B.: Dependence of nitrite oxidation on nitrite and oxygen in low-oxygen seawater, Geophys. Res. Lett., 44, 7883–7891, https://doi.org/10.1002/2017GL074355, 2017.
Sun, X., Jayakumar, A., Tracey, J. C., Wallace, E., Kelly, C. L., Casciotti, K. L., and Ward, B. B.: Microbial N2O consumption in and above marine N2O production hotspots, ISME J., 15, 1434–1444, https://doi.org/10.1038/s41396-020-00861-2, 2021a.
Sun, X., Frey, C., Garcia-Robledo, E., Jayakumar, A., and Ward, B. B.: Microbial niche differentiation explains nitrite oxidation in marine oxygen minimum zones, ISME J., 15, 1317–1329, https://doi.org/10.1038/s41396-020-00852-3, 2021b.
Sutka, R. L., Ostrom, N. E., Ostrom, P. H., Gandhi, H., and Breznak, J. A.: Nitrogen isotopomer site preference of N2O produced by Nitrosomonas europaea and Methylococcus capsulatus Bath, Rapid Commun. Mass Sp., 17, 738–745, https://doi.org/10.1002/rcm.968, 2003.
Sutka, R. L., Ostrom, N. E., Ostrom, P. H., Gandhi, H., and Breznak, J. A.: Nitrogen isotopomer site preference of N2O produced by Nitrosomonas europaea and Methylococcus capsulatus Bath, Rapid Commun. Mass Sp., 18, 1411–1412, https://doi.org/10.1002/rcm.1482, 2004.
Sutka, R. L., Ostrom, N. E., Ostrom, P. H., Breznak, J. A., Gandhi, H., Pitt, A. J., and Li, F.: Distinguishing Nitrous Oxide Production from Nitrification and Denitrification on the Basis of Isotopomer Abundances, Appl. Environ. Microbiol., 72, 638–644, https://doi.org/10.1128/AEM.72.1.638-644.2006, 2006.
Sutka, R. L., Adams, G. C., Ostrom, N. E., and Ostrom, P. H.: Isotopologue fractionation during N2O production by fungal denitrification, Rapid Commun. Mass Sp., 22, 3989–3996, https://doi.org/10.1002/rcm.3820, 2008.
Tian, H., Xu, R., Canadell, J. G., Thompson, R. L., Winiwarter, W., Suntharalingam, P., Davidson, E. A., Ciais, P., Jackson, R. B., Janssens-Maenhout, G., Prather, M. J., Regnier, P., Pan, N., Pan, S., Peters, G. P., Shi, H., Tubiello, F. N., Zaehle, S., Zhou, F., Arneth, A., Battaglia, G., Berthet, S., Bopp, L., Bouwman, A. F., Buitenhuis, E. T., Chang, J., Chipperfield, M. P., Dangal, S. R. S., Dlugokencky, E., Elkins, J. W., Eyre, B. D., Fu, B., Hall, B., Ito, A., Joos, F., Krummel, P. B., Landolfi, A., Laruelle, G. G., Lauerwald, R., Li, W., Lienert, S., Maavara, T., MacLeod, M., Millet, D. B., Olin, S., Patra, P. K., Prinn, R. G., Raymond, P. A., Ruiz, D. J., van der Werf, G. R., Vuichard, N., Wang, J., Weiss, R. F., Wells, K. C., Wilson, C., Yang, J., and Yao, Y.: A comprehensive quantification of global nitrous oxide sources and sinks, Nature, 586, 248–256, https://doi.org/10.1038/s41586-020-2780-0, 2020.
Toyoda, S. and Yoshida, N.: Determination of nitrogen isotopomers of nitrous oxide on a modified isotope ratio mass spectrometer, Anal. Chem., 71, 4711–4718, https://doi.org/10.1021/ac9904563, 1999.
Toyoda, S., Yoshida, N., Miwa, T., Matsui, Y., Yamagishi, H., Tsunogai, U., Nojiri, Y., and Tsurushima, N.: Production mechanism and global budget of N2O inferred from its isotopomers in the western North Pacific, Geophys. Res. Lett., 29, 7-1–7-4, https://doi.org/10.1029/2001GL014311, 2002.
Toyoda, S., Mutobe, H., Yamagishi, H., Yoshida, N., and Tanji, Y.: Fractionation of N2O isotopomers during production by denitrifier, Soil Biol. Biochem., 37, 1535–1545, https://doi.org/10.1016/j.soilbio.2005.01.009, 2005.
Toyoda, S., Yoshida, O., Yamagishi, H., Fujii, A., Yoshida, N., and Watanabe, S.: Identifying the origin of nitrous oxide dissolved in deep ocean by concentration and isotopocule analyses, Sci. Rep., 9, 1–9, https://doi.org/10.1038/s41598-019-44224-0, 2019.
Toyoda, S., Kakimoto, T., Kudo, K., Yoshida, N., Sasano, D., Kosugi, N., Ishii, M., Kameyama, S., Inagawa, M., Yoshikawa-Inoue, H., Nishino, S., Murata, A., Ishidoya, S., and Morimoto, S.: Distribution and Production Mechanisms of N2O in the Western Arctic Ocean, Global Biogeochem. Cy., 35, e2020GB006881, https://doi.org/10.1029/2020GB006881, 2021.
Toyoda, S., Terajima, K., Yoshida, N., Yoshikawa, C., Makabe, A., Hashihama, F., and Ogawa, H.: Extensive Accumulation of Nitrous Oxide in the Oxygen Minimum Zone in the Bay of Bengal, Global Biogeochem. Cy., 37, e2022GB007689, https://doi.org/10.1029/2022GB007689, 2023.
Travis, N. M., Kelly, C. L., Mulholland, M. R., and Casciotti, K. L.: Nitrite cycling in the primary nitrite maxima of the eastern tropical North Pacific, Biogeosciences, 20, 325–347, https://doi.org/10.5194/bg-20-325-2023, 2023.
Trimmer, M., Chronopoulou, P.-M., Maanoja, S. T., Upstill-Goddard, R. C., Kitidis, V., and Purdy, K. J.: Nitrous oxide as a function of oxygen and archaeal gene abundance in the North Pacific, Nat. Commun., 7, 13451–13451, https://doi.org/10.1038/ncomms13451, 2016.
Vajrala, N., Martens-Habbena, W., Sayavedra-Soto, L. A., Schauer, A., Bottomley, P. J., Stahl, D. A., and Arp, D. J.: Hydroxylamine as an intermediate in ammonia oxidation by globally abundant marine archaea, P. Natl. Acad. Sci. USA, 110, 1006–1011, 2013.
Virtanen, P., Gommers, R., Oliphant, T. E., Haberland, M., Reddy, T., Cournapeau, D., Burovski, E., Peterson, P., Weckesser, W., Bright, J., van der Walt, S. J., Brett, M., Wilson, J., Millman, K. J., Mayorov, N., Nelson, A. R. J., Jones, E., Kern, R., Larson, E., Carey, C. J., Polat, İ., Feng, Y., Moore, E. W., VanderPlas, J., Laxalde, D., Perktold, J., Cimrman, R., Henriksen, I., Quintero, E. A., Harris, C. R., Archibald, A. M., Ribeiro, A. H., Pedregosa, F., and van Mulbregt, P.: SciPy 1.0: fundamental algorithms for scientific computing in Python, Nat. Method., 17, 261–272, https://doi.org/10.1038/s41592-019-0686-2, 2020.
Wan, X. S., Sheng, H.-X., Liu, L., Shen, H., Tang, W., Zou, W., Xu, M. N., Zheng, Z., Tan, E., Chen, M., Zhang, Y., Ward, B. B., and Kao, S.-J.: Particle-associated denitrification is the primary source of N2O in oxic coastal waters, Nat. Commun., 14, 8280, https://doi.org/10.1038/s41467-023-43997-3, 2023a.
Wan, X. S., Hou, L., Kao, S.-J., Zhang, Y., Sheng, H.-X., Shen, H., Tong, S., Qin, W., and Ward, B. B.: Pathways of N2O production by marine ammonia-oxidizing archaea determined from dual-isotope labeling, P. Natl. Acad. Sci. USA, 120, e2220697120, https://doi.org/10.1073/pnas.2220697120, 2023b.
Wang, R. Z., Lonergan, Z. R., Wilbert, S. A., Eiler, J. M., and Newman, D. K.: Widespread detoxifying NO reductases impart a distinct isotopic fingerprint on N 2O under anoxia, Microbiology, bioRxiv 2023.10.13.562248, https://doi.org/10.1101/2023.10.13.562248, 2023.
Wei, J., Ibraim, E., Brüggemann, N., Vereecken, H., and Mohn, J.: First real-time isotopic characterisation of N2O from chemodenitrification, Geochim. Cosmochim. Ac., 267, 17–32, https://doi.org/10.1016/j.gca.2019.09.018, 2019.
Westley, M. B., Yamagishi, H., Popp, B. N., and Yoshida, N.: Nitrous oxide cycling in the Black Sea inferred from stable isotope and isotopomer distributions, Deep-Sea Res. Pt. II, 53, 1802–1816, https://doi.org/10.1016/j.dsr2.2006.03.012, 2006.
Wrage, N., Velthof, G. L., Van Beusichem, M. L., and Oenema, O.: Role of nitrifier denitrification in the production of nitrous oxide, Soil Biol. Biochem., 33, 1723–1732, https://doi.org/10.1016/S0038-0717(01)00096-7, 2001.
Yamagishi, H., Westley, M. B., Popp, B. N., Toyoda, S., Yoshida, N., Watanabe, S., Koba, K., and Yamanaka, Y.: Role of nitrification and denitrification on the nitrous oxide cycle in the eastern tropical North Pacific and Gulf of California, J. Geophys. Res.-Biogeo., 112, G02015, https://doi.org/10.1029/2006JG000227, 2007.
Yang, H., Gandhi, H., Ostrom, N. E., and Hegg, E. L.: Isotopic Fractionation by a Fungal P450 Nitric Oxide Reductase during the Production of N2O, Environ. Sci. Technol., 48, 10707–10715, https://doi.org/10.1021/es501912d, 2014.
Zumft, W. G.: Cell biology and molecular basis of denitrification, Microbiol. Mol. Biol. Rev., 61, 533–616, https://doi.org/10.1128/mmbr.61.4.533-616.1997, 1997.
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Short summary
Nitrous oxide, a potent greenhouse gas, accumulates in regions of the ocean that are low in dissolved oxygen. We used a novel combination of chemical tracers to determine how nitrous oxide is produced in one of these regions, the eastern tropical North Pacific Ocean. Our experiments showed that the two most important sources of nitrous oxide under low-oxygen conditions are denitrification, an anaerobic process, and a novel “hybrid” process performed by ammonia-oxidizing archaea.
Nitrous oxide, a potent greenhouse gas, accumulates in regions of the ocean that are low in...
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