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Biogeochemistry

, Volume 132, Issue 3, pp 359–372 | Cite as

Mining the isotopic complexity of nitrous oxide: a review of challenges and opportunities

  • Nathaniel E. OstromEmail author
  • Peggy H. Ostrom
Article

Abstract

Nitrous oxide (N2O) is an important focus of international greenhouse gas accounting agreements and mitigation of emissions will likely depend on understanding the mechanisms of its formation and reduction. Consequently, applications of stable isotope techniques to understand N2O cycling are proliferating and recent advances in technology are enabling (1) increases in the frequency of isotope analyses and (2) analyses not previously possible. The two isotopes of N and 3 isotopes of O combine to form a total of 12 possible isotopic molecules of N2O. Consequently, this remarkably simple molecule contains a wealth of isotopic information in the form of bulk (δ15N, δ18O), position dependent (site preference), mass independent (Δ17O) and multiply-substituted or clumped isotope compositions. With recent developments in high-mass resolution double sector instruments all 12 isotopic molecules will likely be resolved in the near future. Advances in spectroscopic instruments hold the promise of substantial increases in sample throughput; however, spectroscopic analyses require corrections due to interferences from other gases and frequent and accurate calibration. Mass spectrometric approaches require mass overlap corrections that are not uniform between research groups and interlaboratory comparisons remain imprecise. The continued lack of attention to calibration by both funding agencies and investigators can only perpetuate disagreement between laboratories in reported isotope values for N2O that, in turn, will compromise global assessments of N2O sources and sinks based on isotope ratios. This review discusses the challenges and opportunities offered by the isotopic complexity of N2O.

Keywords

Nitrous oxide Isotopomer Site preference Calibration Clumped isotopes 

Notes

Acknowledgements

This work was funded by the National Science Foundation’s (NSF) Earth Sciences Instrumentation and Facilities program (Grant #1456430), NSF’s Geobiology and Low Temperature Geochemistry program (Grant #1526926) and the Department of Energy Great Lakes Bioenergy Research Center (DOE Office of Science BER DE-FC02-07ER64494).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no additional conflicts of interest.

References

  1. Andersson KK, Hooper AB (1983) O2 and H2O are each the source of one O in NO2 Produced from NH3 by Nitrosomonas—N-15-NMR evidence. FEBS Lett 164:236–240CrossRefGoogle Scholar
  2. Angert A, Barkan E, Barnett B, Brugnoli E, Davidson EA, Fessenden J, Maneepong S, Panapitukkul N, Randerson JT, Savage K, Yakir D, Luz B (2003) Contribution of soil respiration in tropical, temperate, and boreal forests to the 18O enrichment of atmospheric O2 Glob Biogeochem. Cycle 17:1089. doi: 10.1029/2003GB002056 Google Scholar
  3. Baer DS, Paul JB, Gupta M, O’Keefe A (2002) Sensitive absorption measurements in the near-infrared region using off-axis integrated cavity output spectroscopy. Appl Phys B. doi: 10.1007/s00340-002-0971-z Google Scholar
  4. Bigeleisen J, Friedman L (1950) The infrared spectrum of N15N14O16 and N14N15O16. Some thermondynamic properties of the isotopic N2O molecules. J Chem Phys 18:1656–1659CrossRefGoogle Scholar
  5. Bohlke JK, Coplen TB (1995) Interlaboratory comparison of reference materials for nitrogen-isotope-ratio measurements. In: IAEA (ed) Reference and intercomparison materials for stable isotopes of light elements. IAEA, Vienna, pp 51–66Google Scholar
  6. Bowling DR, Sargent SD, Tanner BD, Ehleringer JR (2003) Tunable diode laser absorption spectroscopy for stable isotope studies of ecosystem–atmosphere CO2 exchange. Agric For Meteorol 118:1–19CrossRefGoogle Scholar
  7. Bowling DR, Burns SP, Conway TJ, Monson RK, White JWC (2005) Extensive observations of CO2 carbon isotope content in and above a high-elevation subalpine forest. Global Biogeochem Cycles 19 GB3023, doi: 10.1029/2004GB002394
  8. Brand WA, Coplen TB (2012) Stable isotope deltas: tiny, yet robust signatures in nature. Isot Environ Health Stud 48:393–409CrossRefGoogle Scholar
  9. Brand WA, Coplen TB, Vogl J, Rosner M, Prohaska T (2014) Assessment of international reference materials for isotope-ratio analysis (IUPAC Technical Report). Pure Appl Chem 86:425–467CrossRefGoogle Scholar
  10. Breider F, Yoshikawa C, Abe H, Toyoda S, Yoshida N (2015) Origin and fluxes of nitrous oxide along a latitudinal transect in western North Pacific: controls and regional significance. Global Biogeochem Cycles 29:1014–1027CrossRefGoogle Scholar
  11. Brenninkmeijer CAM, Röckmann T (1999) Mass spectrometry of the intramolecular nitrogen isotope distribution of environmental nitrous oxide using fragment-ion analysis. Rapid Commun Mass Spectrom 13:2028–2033CrossRefGoogle Scholar
  12. Chen H, Williams D, Walker JT, Shi W (2016) Probing the biological source of N2O emissions by quantum cascade laser-based 15N isotopocule analysis. Soil Biol Biochem 100:175–181CrossRefGoogle Scholar
  13. Cliff SS, Brenninkmeijer CAM, Thiemens MH (1999) First measurement of the O-18/O-16 and O-17/O-16 ratios in stratospheric nitrous oxide: a mass-independent anomaly. J Geophys Res-Atmos. 104:16171–16175CrossRefGoogle Scholar
  14. Coplen TB (2011) Guidelines and recommended terms for expression of stable-isotope-ratio and gas-ratio measurement results. Rapid Commun Mass Spectrom 25:2538–2560CrossRefGoogle Scholar
  15. Diaz RJ, Rosenberg R (2008) Spreading dead zones and consequences for marine ecosystems. Science 321:926–929CrossRefGoogle Scholar
  16. Diaz RJ, Rosenberg R (2011) Introduction to environmental and economic consequences of hypoxia. Water Resour Dev 27:71–82CrossRefGoogle Scholar
  17. Dua RD, Bhandari B, Nicholas DJD (1979) Stable isotope studies on the oxidation of ammonia to hydroxylamine by Nitrosomonas europaea. FEBS Lett 106:401–404CrossRefGoogle Scholar
  18. Dyckmans J, Lewicka-Szczebak D, Szwec L, Langel R, Well R (2015) Comparison of methods to determine triple oxygen isotope composition of N2O. Rapid Commun Mass Spectromy 29:1991–1996CrossRefGoogle Scholar
  19. Eiler JM (2007) “Clumped-isotope” geochemistry—The study of naturally-occurring, multiply-substituted isotopologues. Earth Planet Sci Lett 262:309–327CrossRefGoogle Scholar
  20. Eiler JM, Clog M, Magyar P, Piasecki A, Sessions A, Stolper D, Deerberg M, Schlueter HJ, Schwieters J (2013) A high-resolution gas-source isotope ratio mass spectrometer. Int J Mass Spectrom 335:45–56CrossRefGoogle Scholar
  21. Erler DV, Duncan TM, Murray R, Maher DT, Santos IR, Gatland JR, Mangion P, Eyre BD (2015) Applying cavity ring-down spectroscopy for the measurement of dissolved nitrous oxide concentrations and bulk nitrogen isotopic composition in aquatic systems: correcting for interferences and field application. Limnol Oceanogr Methods 13:391–401CrossRefGoogle Scholar
  22. Esler MB, Griffith DW, Turatti F, Wilson SR, Rahn T, Zhang H (2000) N2O concentration and flux measurements and complete isotopic analysis by FTIR spectroscopy. Chemosphere 2:445–454Google Scholar
  23. Forster P, Ramaswamy V, Artaxo P, Berntsen T, Betts R, Fahey DW, Haywood J, Lean J, Lowe DC, Myhre G, Nganga J., Prinn R., Raga, G, Schultz M., Van Dorland, R (2007) Changes in atmospheric constituents and in radiative forcing. Chapter 2. In: Solomon, S., D. Qin, M. Manning, Z. Chen, M. Marquis, K.B. Averyt, M.Tignor and H.L. Miller (eds.), Climate Change 2007: The Physical Science Basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, United Kingdom and New York, NY, USAGoogle Scholar
  24. Frame C, Casciotti K (2010) Biogeochemical controls and isotopic signatures of nitrous oxide production by a marine ammonia-oxidizing bacterium. Biogeosci Discuss 7:3019–3059CrossRefGoogle Scholar
  25. Friedman L, Bigeleisen J (1950) Oxygen and nitrogen isotope effects in the decomposition of ammonium nitrate. J Chem Phys 18:1325–1331CrossRefGoogle Scholar
  26. Fujii A, Toyoda S, Yoshida O, Watanabe S, Sasaki KI, Yoshida N (2013) Distribution of nitrous oxide dissolved in water masses in the eastern subtropical North Pacific and its origin inferred from isotopomer analysis. J Oceanogr 69:147–157CrossRefGoogle Scholar
  27. Griffith DW, Parkes SD, Haverd V, Paton-Walsh C, Wilson SR (2009) Absolute calibration of the intramolecular site preference of 15N fractionation in tropospheric N2O by FT-IR spectroscopy. Anal Chem 81:2227–2234CrossRefGoogle Scholar
  28. Guo W, Eiler JM (2007) Temperatures of aqueous alteration and evidence for methane generation on the parent bodies of the CM chondrites. Geochim Cosmochim Acta 71:5565–5575CrossRefGoogle Scholar
  29. Harris E, Nelson DD, Olszewski W, Zahniser M, Potter KE, McManus BJ, Whitehall A, Prinn RG, Ono S (2014) Development of a spectroscopic technique for continuous online monitoring of oxygen and site-specific nitrogen isotopic composition of atmospheric nitrous oxide. Anal Chem 86:1726–1734CrossRefGoogle Scholar
  30. Heil J, Wolf B, Bruggermann N, Emmenegger L, Tuzson B, Vereecken H, Mohn J (2014) Site-specific 15N isotopic signatures of abiotically produced N2O. Geochim Cosmochim Acta 139:72–82CrossRefGoogle Scholar
  31. Heil J, Liu S, Vereecken H, Brüggemann N (2015) Abiotic nitrous oxide production from hydroxylamine in soils and their dependence on soil properties. Soil Biol Biochem 84:107–115CrossRefGoogle Scholar
  32. Jinuntuya-Nortman M, Sutka RL, Ostrom PH, Gandhi H, Ostrom NE (2008) Isotopologue fractionation during microbial reduction of N2O within soil mesocosms as a function of water-filled pore space. Soil Biol Biochem 40:2273–2280CrossRefGoogle Scholar
  33. Jung MY, Well R, Min D, Giesemann A, Park SJ, Kim JG, Kim SJ, Rhee SK (2014) Isotopic signatures of N2O produced by ammonia-oxidizing archaea from soils. ISME J 8:1115–1125CrossRefGoogle Scholar
  34. Kaiser J, Rockmann T (2005) Absence of isotope exchange in the reaction of N2O + O(1D) and the global Δ17O budget of nitrous oxide. Geophys Res Lett. doi: 10.1029/2005GL023199 Google Scholar
  35. Kaiser J, Röckmann T (2008) Correction of mass spectrometric isotope ratio measurements for isobaric isotopologues of O2, CO, CO2, N2O and SO2. Rapid Commun Mass Spectrom 22:3997–4008CrossRefGoogle Scholar
  36. Kaiser J, Park S, Boering KA, Brenninkmeijer CAM, Hilkert A, Rockmann T (2004) Mass spectrometric method for the absolute calibration of the intramolecular nitrogen isotope distribution in nitrous oxide. Anal Bioanal Chem 378:256–269CrossRefGoogle Scholar
  37. Kong X, Duan Y, Schramm A, Eriksen J, Holmstrup M, Larsen T, Bol R, Petersen SO (2017) Mitigating N2O emissions from clover residues by 3,4-dimethylpyrazole phosphate (DMPP) without adverse effects on the earthworm Lumbricus terrestris. Soil Biol Biochem 104:95–107CrossRefGoogle Scholar
  38. Köster JR, Well R, Tuzson B, Bol R, Dittert K, Giesemann A, Emmenegger L, Manninen A, Cárdenas L, Mohn J (2012) Novel laser spectroscopic technique for continuous analysis of N2O isotopomers–application and intercomparison with isotope ratio mass spectrometry. Rapid Commun Mass Spectrom 27:216–222CrossRefGoogle Scholar
  39. Köster JR, Well R, Dittert K, Giesemann A, Lewicka-Szczebak D, Mühling KH, Herrmann A, Lammel J, Senbayram M (2013) Soil denitrification potential and its influence on N2O reduction and N2O isotopomer ratios. Rapid Commun Mass Spectrom 27:2363–2373CrossRefGoogle Scholar
  40. Kumar S, Nicholas DJD, Williams EH (1983) Definitive 15N-NMR evidence that water serves as a source of O during nitrite oxidation by Nitrobacter agilis. FEBS Lett 152:71–74CrossRefGoogle Scholar
  41. Lammerzahl P, Rockmann T, Brenninkmeijer CAM, Krankowsky D, Mauersberger K (2002) Oxygen isotope composition of stratospheric carbon dioxide. Geophys Res Lett. doi: 10.1029/2001GL014343 Google Scholar
  42. Maeda K, Spor A, Edel-Hermann V, Heraud C, Breuil MC, Bizouard F, Toyoda S, Yoshida N, Steinberg C, Philippot L (2015) N2O production, a widespread trait in fungi. Sci Rep. doi: 10.1038/srep09697 Google Scholar
  43. Mak JE, Brenninkmeijer CAM (1994) Compressed air sample technology for isotopic analysis of atmospheric carbon monoxide. J Atmos Ocean Technol 11(2):425–431CrossRefGoogle Scholar
  44. Mander Ü, Maddison M, Soosaar K, Koger H, Teemusk A, Truu J, Well R, Sebilo M (2015) The impact of a pulsing water table on wastewater purification and greenhouse gas emission in a horizontal subsurface flow constructed wetland. Ecol Eng 80:69–78CrossRefGoogle Scholar
  45. Maygar P, Orphan VJ, Eiler JM (2016) Measurement of rare isotopologues of nitrous oxide by high-resolution multi-collector mass spectrometry. Rapid Commun Mass Spectrom 30:1923–1940CrossRefGoogle Scholar
  46. Meijer H, Li W (1998) The use of electrolysis for accurate δ17O and δ18O isotope measurements in water. Isot Environ Health Stud 34:349–369CrossRefGoogle Scholar
  47. Michalski G, Bhattacharya SK, Mase DF (2012) Oxygen isotope dynamics of atmospheric nitrate and its precursor molecules. In: Baskaran M (ed) Handbook of environmental isotope geochemistry. Springer, Berlin, pp 613–635CrossRefGoogle Scholar
  48. Miller MF (2002) Isotopic fractionation and the quantification of 17O anomalies in the oxygen three-isotope system: an appraisal and geochemical significance. Geochim Cosmochim Acta 66:1881–1889CrossRefGoogle Scholar
  49. Mohn J, Guggenheim C, Tuzson B, Vollmer MK, Toyoda S, Yoshida N, Emmenegger L (2010) A liquic nitrogen-free preconcentration unit for measurements of ambient N2O isotopomers by QCLAS. Atmos Meas Tech 3:609–618CrossRefGoogle Scholar
  50. Mohn J, Tuzson B, Manninen A, Yoshida N, Toyoda S, Brand WA, Emmenegger L (2012) Site selective real-time measurements of atmospheric N2O isotopomers by laser spectroscopy. Atmos Meas Tech Discuss 5:813–838CrossRefGoogle Scholar
  51. Mohn J, Wolf B, Toyoda S, Lin C-T, Liang M-C, Bruggermann N, Wissel H, Steiker AE, Dyckmans J, Szwec L, Ostrom NE, Casciotti KL, Forbes M, Giesemann A, Well R, Doucett RR, Yarnes CT, Ridley AR, Kaiser J, Yoshida N (2014) Interlaboratory assessment of nitrous oxide isotopomer analysis by isotope ratio mass spectrometry. Rapid Commun Mass Spectrom 28:1995–2007CrossRefGoogle Scholar
  52. Mohn J, Gutjahr W, Toyoda S, Yoshida N, Brand WA, Harris E, Ibraim E, Geilmann H, Schleppi P, Kuhn T, Lehmann MF, Decock C, Werner RA (2016) Reassessment of the NH4NO3 thermal decomposition technique for calibration of the N2O isotopic composition. Rapid Commun Mass Spectrom 30:2487–2496CrossRefGoogle Scholar
  53. Murray AE, Kenig F, Fritsen CH, McKay CP, Cawley KM, Edward R, Kuhn E, McKnight DM, Ostrom NE, Peng V, Ponce A, Priscu JC, Samarkin V, Townsend AT, Wagh P, Young SA, Yung PT, Doran PT (2012) Microbial life at −13 °C in the brine of an ice-sealed Antarctic lake. Proc Natl Acad Sci 109:20626–20631CrossRefGoogle Scholar
  54. Naqvi SWA, Bange HW, Farías L, Monteiro PMS, Scranton MI, Zhang J (2010) Marine hypoxia/anoxia as a source of CH4 and N2O. Biogeosciences 7:2159–2190CrossRefGoogle Scholar
  55. Ono S, Wang DT, Gruen DS, Sherwood Lollar B, Zahniser MS, McManus BJ, Nelson DD (2014) Measurement of a doubly substituted methane isotopologue, 13CH3D, by tunable infrared laser direct absorption spectroscopy. Anal Chem 86:6487–6494CrossRefGoogle Scholar
  56. Ostrom NE, Ostrom PH (2012) The isotopomers of nitrous oxide: analytical considerations and application to resolution of microbial production pathways. In: Baskaran M (ed) Handbook of environmental isotope geochemistry. Springer, New York, pp 453–476CrossRefGoogle Scholar
  57. Ostrom NE, Russ ME, Popp B, Rust TM, Karl DM (2000) Mechanisms of N2O production in the subtropical North Pacific based on determinations of the isotopic abundances of N2O and O2. Chemosphere Glob Chang Sci 2:281–290CrossRefGoogle Scholar
  58. Ostrom NE, Gandhi H, Trubl G, Murray AE (2016) Chemodenitrification in the cryoecosystem of Lake Vida, Victoria Valley, Antarctica. Geobiology 14:575–587CrossRefGoogle Scholar
  59. Pataki DE, Bowling DR, Ehleringer JR, Zobitz JM (2006) High resolution atmospheric monitoring of urban carbon dioxide sources. Geophys Res Lett. doi: 10.1029/2003JD003865 Google Scholar
  60. Ravishankara AR, Daniel JS, Portmann RW (2009) Nitrous oxide (N2O): the dominant ozone-depleting substance emitted in the 21st century. Science 326:123–125CrossRefGoogle Scholar
  61. Richardson WS, Wilson EB Jr (1950) The infrared spectrum of N15N14O and force constants of nitrous oxide. J Chem Phys 18:694–696CrossRefGoogle Scholar
  62. Röckmann T, Kaiser J, Brenninkmeijer CA, Brand WA (2003) Gas chromatography/isotope-ratio mass spectrometry method for high-precision position-dependent 15N and 18O measurements of atmospheric nitrous oxide. Rapid Commun Mass Spectrom 17:1897–1908CrossRefGoogle Scholar
  63. Rohe L, Anderson TH, Braker G, Flessa H, Giesemann A, Lewicka-Szczebak D, Wrage-Mönnig N, Well R (2014) Dual isotope and isotopomer signatures of nitrous oxide from fungal denitrification–a pure culture study. Rapid Commun Mass Spectrom 28:1893–1903CrossRefGoogle Scholar
  64. Salk KR, Ostrom PH, Biddanda BA, Weinke AD, Kendall ST, Ostrom NE (2016) Ecosystem metabolism and greenhouse gas production in a mesotrophic northern temperate lake experiencing seasonal hypoxia. Biogeochemistry 131:303–319CrossRefGoogle Scholar
  65. Samarkin VA, Madigan MT, Bowles MW, Casciotti KL, Priscu JC, McKay CP, Joye SB (2010) Abiotic nitrous oxide emission from the hypersaline Don Juan Pond in Antarctica. Nat Geosci 3:341–344CrossRefGoogle Scholar
  66. Santoro AE, Buchwald C, McIlvin MR, Casciotti KL (2011) Isotopic signature of N2O produced by marine ammonia-oxidizing archaea. Science 333:1282–1285CrossRefGoogle Scholar
  67. Savarino J, Morin S (2012) The N, O, S isotopes of oxy-anions in ice cores and polar environments. In: Baskaran M (ed) Handbook of environmental isotope geochemistry. Springer, Berlin, pp 835–864CrossRefGoogle Scholar
  68. Schmidt JA, Johnson MS (2015) Clumped isotope perturbation in tropospheric nitrous oxide from stratospheric photolysis. Geophys Res Lett 42:3546–3552CrossRefGoogle Scholar
  69. Senbayram M, Chen R, Budai A, Bakken L, Dittert K (2012) N2O emission and the N2O/(N2O + N2) product ratio of denitrification as controlled by available carbon substrates and nitrate concentrations. Agric Ecosyst Environ 147:4–12CrossRefGoogle Scholar
  70. Smemo KA, Ostrom NE, Opdyke MR, Ostrom PH, Bohm S, Robertson GP (2011) Improving process-based estimates of N2O emissions from soil using temporally extensive chamber techniques and stable isotopes. Nutr Cycl Agroecosyst 91:145–154CrossRefGoogle Scholar
  71. Snider D, Thompson K, Wagner-Riddle C, Spoelstra J, Dunfield K (2015a) Molecular techniques and stable isotope ratios at natural abundance give complementary inferences about N2O production pathways in an agricultural soil following a rainfall event. Soil Biol Biochem 88:197–213CrossRefGoogle Scholar
  72. Snider DM, Venkiteswaran JJ, Schiff SL, Spoelstra J (2015b) From the ground up: global nitrous oxide sources are constrained by stable isotope values. PLoS ONE. 10(3):e0118954CrossRefGoogle Scholar
  73. Soto DX, Koehler G, Hobson KA (2015) Combining denitrifying bacteria and laser spectroscopy for isotopic analyses (δ15N, δ18O) of dissolved nitrate. Anal Chem 87:7000–7005CrossRefGoogle Scholar
  74. Stein LY, Yung YL (2003) Production, isotopic composition, and atmospheric fate of biologically produced nitrous oxide. Ann Rev Earth Planet Sci 31:329–356CrossRefGoogle Scholar
  75. Stolper DA, Sessions AL, Ferreira AA, Neto ES, Schimmelmann A, Shusta SS, Valentine DL, Eiler JM (2014) Combined 13 C-D and D–D clumping in methane: methods and preliminary results. Geochim Cosmochim Acta 126:169–191CrossRefGoogle Scholar
  76. Sutka RL, Ostrom NE, Ostrom PH, Gandhi H, Breznak JA (2003) Nitrogen isotopomer site preference of N2O produced by Nitrosomonas europaea and Methylococcus capsulatus Bath. Rapid Commun Mass Spectrom 17:738–745CrossRefGoogle Scholar
  77. Sutka RL, Ostrom NE, Ostrom PH, Breznak JA, Gandhi H, Pitt AJ, Li F (2006) Distinguishing nitrous oxide production from nitrification and denitrification on the basis of isotopomer abundances. Appl Environ Microbiol 72:638–644CrossRefGoogle Scholar
  78. Sutka RL, Adams GC, Ostrom NE, Ostrom PH (2008) Isotopologue fractionation during N2O production by fungal denitrification. Rapid Commun Mass Spectrom 22:3989–3996CrossRefGoogle Scholar
  79. Thiemens MH (2006) History and applications of mass-independent isotope effects. Annu Rev Earth Planet Sci 34:217–262CrossRefGoogle Scholar
  80. Toyoda S, Yoshida N (1999) Determination of nitrogen isotopomers of nitrous oxide on a modified isotope ratio mass spectrometer. Anal Chem 71:4711–4718CrossRefGoogle Scholar
  81. Toyoda S, Mutobe H, Yamagishi H, Yoshida N, Tanji Y (2005) Fractionation of N2O isotopomers during production by denitrifier. Soil Biol Biochem 37:1535–1545CrossRefGoogle Scholar
  82. Toyoda S, Iwai H, Koba K, Yoshida N (2009) Isotopomeric analysis of N2O dissolved in a river in the Tokyo metropolitan area. Rapid Commun Mass Spectrom 23:809–821CrossRefGoogle Scholar
  83. Toyoda S, Suzuki Y, Hattori S, Yamada K, Fujii A, Yoshida N, Kouno R, Murayama K, Shiomi H (2010) Isotopomer analysis of production and consumption mechanisms of N2O and CH4 in an advanced wastewater treatment system. Environ Sci Technol 45:917–922CrossRefGoogle Scholar
  84. Trolier M, White JWC, Tans PP, Masarie KA, Gemery PA (1996) Monitoring the isotopic composition of atmospheric CO2: measurements from the NOAA global air sampling network. J Geophys Res 101(D20):25897–25916CrossRefGoogle Scholar
  85. Turatti F, Griffith DW, Wilson SR, Esler MB, Rahn T, Zhang H, Blake GA (2000) Positionally dependent 15N fractionation factors in the UV photolysis of N2O determined by high resolution FTIR spectroscopy. Geophys Res Lett 27:2489–2492CrossRefGoogle Scholar
  86. Waechter H, Mohn J, Tuzson B, Emmenegger L, Sigrist MW (2008) Determination of N2O isotopomers with quantum cascade laser based absorption spectroscopy. Opt Express 16:9239–9244CrossRefGoogle Scholar
  87. Wahlen M, Yoshinari T (1985) Oxygen isotope ratios in N2O from different environments. Nature 313:780–782CrossRefGoogle Scholar
  88. Well R, Kurganova I, de Gerenyu VL, Flessa H (2006) Isotopomer signatures of soil-emitted N2O under different moisture conditions—a microcosm study with arable loess soil. Soil Biol Biochem 38:2923–2933CrossRefGoogle Scholar
  89. Well R, Flessa H, Xing L, Ju XT, Romheld V (2008) Isotopologue ratios of N2O emitted from microcosms with NH4 + fertilized arable soils under conditions favoring nitrification. Soil Biol Biochem 40:2416–2426CrossRefGoogle Scholar
  90. Well R, Eschenbach W, Flessa H, von der Heide C, Weymann D (2012) Are dual isotope and isotopomer ratios of N2O useful indicators for N2O turnover during denitrification in nitrate-contaminated aquifers? Geochim Cosmochim Acta 90:265–282CrossRefGoogle Scholar
  91. Westley MB, Popp BN, Rust TM (2007) The calibration of the intramolecular nitrogen isotope distribution in nitrous oxide measured by isotope ratio mass spectrometry. Rapid Commun Mass Spectrom 21:391–405CrossRefGoogle Scholar
  92. Wrage N, Velthof GL, Van Beusichem ML, Oenema O (2001) Role of nitrifier denitrification in the production of nitrous oxide. Soil Biol Biochem 33:1723–1732CrossRefGoogle Scholar
  93. Wunderlin P, Mohn J, Joss A, Emmenegger L, Siegrist H (2012) Mechanisms of N2O production in biological wastewater treatment under nitrifying and denitrifying conditions. Water Res 46:1027–1037CrossRefGoogle Scholar
  94. Wunderlin P, Lehmann MF, Siegrist H, Tuzson B, Joss A, Emmenegger L, Mohn J (2013) Isotope signatures of N2O in a mixed microbial population system: constraints on N2O producing pathways in wastewater treatment. Environ Sci Technol 47:1339–1348CrossRefGoogle Scholar
  95. Yamamoto A, Uchida Y, Akiyama H, Nakajima Y (2014) Continuous and unattended measurements of the site preference of nitrous oxide emitted from an agricultural soil using quantum cascade laser spectrometry with intercomparison with isotope ratio mass spectrometry. Rapid Commun Mass Spectrom 28:1444–1452CrossRefGoogle Scholar
  96. Yamazaki T, Hozuki T, Arai K, Toyoda S, Koba K, Fujiwara T, Yoshida N (2014) Isotopomeric characterization of nitrous oxide produced by reaction of enzymes extracted from nitrifying and denitrifying bacteria. Biogeosciences 11:2679–2689CrossRefGoogle Scholar
  97. Yang H, Gandhi H, Ostrom NE, Hegg EL (2014a) Isotopic fractionation by a fungal P450 nitric oxide reductase during production of N2O. Environ Sci Technol 48:10707–10715CrossRefGoogle Scholar
  98. Yang WH, McDowell AC, Brooks PD, Silver WL (2014b) New high precision approach for measuring 15N–N2 gas fluxes from terrestrial ecosystems. Soil Biol Biochem 69:234–241CrossRefGoogle Scholar
  99. Yeung LY (2016) Combinatorial effects on clumped isotopes and their significance in biogeochemistry. Geochim Cosmochim Acta 172:22–38CrossRefGoogle Scholar
  100. Yoshida N, Matsuo S (1983) Nitrogen isotope ratio of atmospheric N2O as a key to the global cycle of N2O. Geochem J 17:231–399CrossRefGoogle Scholar
  101. Yoshida N, Toyoda S (2000) Constraining the atmospheric N2O budget from intramolecular site preference in N2O isotopomers. Nature 405:330–334CrossRefGoogle Scholar
  102. Yoshida N, Hattori A, Saino T, Matsuo S, Wada E (1984) 15N/14N ratio of dissolved N2O in the eastern tropical Pacific Ocean. Nature 307:442–444CrossRefGoogle Scholar
  103. Yoshida N, Morimoto H, Hirano M, Koike I, Matsuo S, Wada E, Saino T, Hattori A (1989) Nitrification rates and 15N abundances of N2O and NO3 in the western North Pacific. Nature 342:895–897CrossRefGoogle Scholar
  104. Yoshinari T, Wahlen M (1985) Oxygen isotope ratios in N2O from nitrification at a wastewater treatment facility. Nature 317:349–350CrossRefGoogle Scholar
  105. Young ED, Galy A, Nagahara H (2002) Kinetic and equilibrium mass-dependent isotope fractionation laws in nature and their geochemical and cosmochemical significance. Geochim Cosmochim Acta 66:1095–1104CrossRefGoogle Scholar
  106. Young ED, Rumble D, Freedman P, Mills M (2016) A large-radius high-mass-resolution multiple-collector isotope ratio mass spectrometer for analysis of rare isotopologues of O2, N2, CH4 and other gases. Int J Mass Spectrom 401:1–10CrossRefGoogle Scholar
  107. Zhu-Barker X, Cavazos AR, Ostrom NE, Horwath WR, Glass JB (2015) The importance of abiotic reactions for nitrous oxide production. Biogeochemistry 126:251–267CrossRefGoogle Scholar

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© Springer International Publishing Switzerland 2017

Authors and Affiliations

  1. 1.Department of Integrative Biology, Ecology and Evolutionary Biology and Behavior Program, and DOE Great Lakes Bioenergy Research CenterMichigan State UniversityEast LansingUSA

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