Eukaryotic assimilatory nitrate reductase fractionates N and O isotopes with a ratio near unity

Environmental Science and Technology

Volumn 46, Issue 11, 2012, Pages 5727-5735

  Karsh, Kristen L ^a,b,c,d   Granger, Julie ^a,e   Kritee, K ^a,f   Sigman, Daniel M ^a  

^a PRINCETON UNIVERSITY   (United States)

^b UNIVERSITY OF TASMANIA   (Australia)

^c UNIVERSITY OF TASMANIA   (Australia)

^d CSIRO   (Australia)

^e UNIVERSITY OF CONNECTICUT   (United States)

^f ENVIRONMENTAL DEFENSE FUND   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ASPERGILLUS NIGER; BOND RUPTURE; CELL HOMOGENATE; INTRACELLULAR REDUCTION; ISOTOPE EFFECT; ISOTOPE FRACTIONATION; ISOTOPE RATIO; ISOTOPE SIGNATURES; MARINE DIATOMS; NATURAL ABUNDANCE; NITRATE ASSIMILATION; NITRATE REDUCTASE; NITRATE REDUCTION; NITRATE-N; POTENTIAL CONSTRAINTS; RELIABLE MEASUREMENT; TRANSITION STATE;

ASPERGILLUS; CARRIER MOBILITY; CELL CULTURE; ENZYME ACTIVITY; NITRATES;

ISOTOPES;

NITRATE REDUCTASE; NITROGEN; OXYGEN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE;

DIATOM; ENZYME ACTIVITY; FUNGUS; ISOTOPIC FRACTIONATION; MARINE ECOSYSTEM; NITROGEN ISOTOPE; OXYGEN ISOTOPE; PHYTOPLANKTON; TAXONOMY;

ARTICLE; ASPERGILLUS NIGER; CELL FREE SYSTEM; DIATOM; FRACTIONATION; ISOTOPE ANALYSIS; MOLECULAR MECHANICS; NONHUMAN; REDUCTION; THALASSIOSIRA WEISSFLOGII;

ASPERGILLUS NIGER; BIOCATALYSIS; CHEMICAL FRACTIONATION; DIATOMS; ELECTRONS; ENZYME ASSAYS; EUKARYOTIC CELLS; NAD; NADP; NITRATES; NITRITE REDUCTASE (NAD(P)H); NITROGEN; NITROGEN ISOTOPES; OXYGEN; OXYGEN ISOTOPES;

ASPERGILLUS NIGER; EUKARYOTA; FUNGI; NITZSCHIA ALBA; THALASSIOSIRA WEISSFLOGII;

EID: 84861850382     PISSN: 0013936X     EISSN: 15205851     Source Type: Journal    
DOI: 10.1021/es204593q     Document Type: Article

References (55)

1. Canfield, D. E.; Glazer, A. N.; Falkowski, P. G. The evolution and future of Earth's nitrogen cycle. Science 2010, 330 (192), 192-196.
2. Gruber, N.; Galloway, J. N. An Earth-system perspective of the global nitrogen cycle. Nature 2008, 45, 293-296.
3. Sigman, D. M.; Granger, J.; DiFiore, P. J.; Lehmann, M. M.; Ho, R.; Cane, G.; van Geen, A. Coupled nitrogen and oxygen isotope measurements of nitrate along the eastern North Pacific margin. Global Biogeochem. Cycle 2005, 19 (4), DOI 10.1029/2005gb002458.
4. Casciotti, K. L.; Sigman, D. M.; Hastings, M. G.; Böhlke, J. K.; Hilkert, A. Measurement of the oxygen isotopic composition of nitrate in seawater and freshwater using the denitrifier method. Anal. Chem. 2002, 74 (19), 4905-4912.
5. Granger, J.; Sigman, D. M.; Lehmann, M. F.; Tortell, P. D. Nitrogen and oxygen isotope fractionation during dissimilatory nitrate reduction by denitrifying bacteria. Limnol. Oceanogr. 2008, 53 (6), 2533-2545.
6. Granger, J.; Sigman, D. M.; Needoba, J. A.; Harrison, P. J. Coupled nitrogen and oxygen isotope fractionation of nitrate during assimilation by cultures of marine phytoplankton. Limnol. Oceanogr. 2004, 49 (5), 1763-1773. (Pubitemid 39320766)
7. DiFiore, P. J.; Sigman, D. M.; Dunbar, R. B. Upper ocean nitrogen fluxes in the Polar Antarctic Zone: Constraints from the nitrogen and oxygen isotopes of nitrate. Geochem. Geophys. Geosyst. 2009, 10 (11), DOI 10.1029/2009gc002468.
8. Lehmann, M. F.; Sigman, D. M.; Berelson, W. M. Coupling the N-15/N-14 and O-18/O-16 of nitrate as a constraint on benthic nitrogen cycling. Mar. Chem. 2004, 88 (1-2), 1-20. (Pubitemid 38700309)
9. Granger, J.; Prokopenko, M. G.; Sigman, D. M.; Mordy, C. W.; Morse, Z. M.; Morales, L. V.; Sambrotto, R. N.; Plessen, B. Coupled nitrification- denitrification in sediment of the eastern Bering Sea shelf waters. J. Geophys. Res. 2011, 116 (C11006), DOI 10.1029/ 2010jc006751.
10. Wankel, S. D.; Kendall, C.; Pennington, J. T.; Chavez, F. P.; Paytan, A. Nitrification in the euphotic zone as evidenced by nitrate dual isotopic composition: Observations from Monterey Bay, California. Global Biogeochem. Cycle 2007, 21 (2), DOI 10.1029/ 2006gb002723.
11. Brookshire, E. N. J.; Hedin, L. O.; Newbold, J. D.; Sigman, D. M.; Jackson, J. K. Sustained losses of bioavailable nitrogen from montane tropical forests. Nat. Geosci. 2012, 5, 123-126.
12. Clough, T. J.; Buckthought, L. E.; Casciotti, K. L.; Kelliher, F. M.; Jones, P. K. Nitrous oxide dynamics in a braided river system, New Zealand. J. Environ. Quality 2011, 40 (5), 1532-1541.
13. Kendall, C.; Elliott, E. M.; Wankel, S. D. Tracing Anthropogenic Inputs of Nitrogen to Ecosystems. In Stable Isotopes in Ecology and Environmental Science, 2nd ed.; Michener, R., Lajtha, K., Eds.; Blackwell Publishing Ltd: Malden, 2007; pp 375-449.
14. Granger, J.; Sigman, D. M.; Rohde, M. M.; Maldonado, M. T.; Tortell, P. D. N and O isotope effects during nitrate assimilation by unicellular prokaryotic and eukaryotic plankton cultures. Geochim. Cosmochim. Acta 2010, 74 (3), 1030-1040.
15. DiFiore, P. J.; Sigman, D. M.; Trull, T. W.; Lourey, M. J.; Karsh, K.; Cane, G.; Ho, R. Nitrogen isotope constraints on subantarctic biogeochemistry. J. Geophys. Res.-Oceans 2006, 111 (C8), DOI 10.1029/2005jc003216.
16. Sigman, D. M.; Altabet, M. A.; McCorkle, D. C.; Francois, R.; Fischer, G. The delta N-15 of nitrate in the Southern Ocean: Consumption of nitrate in surface waters. Global Biogeochem. Cycle 1999, 13 (4), 1149-1166. (Pubitemid 34002206)
17. 2concentrations during the last glacial period. Nature 1997, 389 (6654), 929-935.
18. Robinson, R. S.; Sigman, D. M.; DiFiore, P. J.; Rohde, M. M.; Mashiotta, T. A.; Lea, D. W. Diatom-bound N-15/N-14: New support for enhanced nutrient consumption in the ice age subantarctic. Paleoceanography 2005, 20 (3), DOI 10.1029/2004pa001114.
19. Needoba, J. A.; Waser, N. A.; Harrison, P. J.; Calvert, S. E. Nitrogen isotope fractionation in 12 species of marine phytoplankton during growth on nitrate. Mar. Ecol.-Prog. Ser. 2003, 255, 81-91. (Pubitemid 36872404)
20. Shearer, G.; Schneider, J. D.; Kohl, D. H. Separating the efflux and influx components of net nitrate uptake by Synechococcus R2 under steady-sate conditions. J. Gen. Microbiol. 1991, 137, 1179-1184.
21. Wada, E.; Hattori, A. Nitrogen isotope effects in the assimilation of inorganic nitrogenous compounds by marine diatoms. Geomicrobiol. J. 1978, 1 (1), 85-101.
22. Needoba, J. A.; Sigman, D. M.; Harrison, P. J. The mechanism of isotope fractionation during algal nitrate assimilation as illuminated by the N-15/N-14 of intracellular nitrate. J. Phycol. 2004, 40 (3), 517-522. (Pubitemid 38740380)
23. 3- by Pearl Millet. Plant Physiol. 1982, 69 (4), 880-884.
24. O'Leary, M. H. Determination of heavy atom isotope effects on enzyme-catalyzed reactions. Methods Enzymol. 1980, 64, 83-104.
25. Solomonson, L. P.; Barber, M. J. Assimilatory nitrate reductase - Functional properties and regulation. Annu. Rev. Plant Physiol. Plant Molec. Biol. 1990, 41, 225-253. (Pubitemid 120024683)
26. Berges, J. A.; Harrison, P. J. Nitrate reductase-activity quantitatively predicts the rate of nitrate incorporation under steady-state light limitation - A revised assay and characterization of the enzyme in 3 species of marine-phytoplankton. Limnol. Oceanogr. 1995, 40 (1), 82-93.
27. Ledgard, S. F.; Woo, K. C.; Bergersen, F. J. Isotopic fractionation during reduction of nitrate and nitrite by extracts of spinach leaves. Austral. J. Plant Physiol. 1985, 12 (6), 631-640.
28. Olleros-Izard, T. Kinetische isotopeneffekte der arginase und nitratreduktase reaktion: Ein betrag zur aufklärung der entsprechenden reaktionmechanismen. PhD Thesis, Technischen Universität München: Freising-Weihenstephan, 1983.
29. Schmidt, H. L.; Medina, R. Possibilities and scope of the double isotope effect method in the elucidation of mechanisms of enzyme catalyzed-reactions. Isotopenpraxis 1991, 27 (1), 1-4.
30. Tcherkez, G.; Farquhar, G. D. Isotopic fractionation by plant nitrate reductase, twenty years later. Funct. Plant Biol. 2006, 33 (6), 531-537. (Pubitemid 43854197)
31. McIlvin, M. R.; Altabet, M. A. Chemical conversion of nitrate and nitrite to nitrous oxide for nitrogen and oxygen isotopic analysis in freshwater and seawater. Anal. Chem. 2005, 77 (17), 5589-5595. (Pubitemid 41266054)
32. Sigman, D. M.; Casciotti, K. L.; Andreani, M.; Barford, C.; Galanter, M.; Bohlke, J. K. A bacterial method for the nitrogen isotopic analysis of nitrate in seawater and freshwater. Anal. Chem. 2001, 73 (17), 4145-4153. (Pubitemid 32830853)
33. Karsh, K. L. unpublished data.
34. Stolz, J. F.; Basu, P. Evolution of nitrate reductase: Molecular and structural variations on a common function. ChemBioChem 2002, 3 (2-3), 198-206. (Pubitemid 36004495)
35. Garside, C. A chemiluminescent technique for the determination of nanomolar concentrations of nitrate and nitrite in seawater. Mar. Chem. 1982, 11, 159-167.
36. Granger, J.; Sigman, D. M. Removal of nitrite with sulfamic acid for nitrate N and O isotope analysis with the denitrifier method. Rapid Commun. Mass Spectrom. 2009, 23 (23), 3753-3762.
37. Braman, R. S.; Hendrix, S. A. Nanogram nitrite and nitrate determination in environmental and biological-materials by vanadium- (III) reduction with chemi-luminescence detection. Anal. Chem. 1989, 61 (24), 2715-2718. (Pubitemid 20065839)
38. Gonfiantini, R.; Stichler, W.; Rosanski, K. Standards and intercomparison materials distributed by the IAEA for stable isotope measurements. In Reference and Intercomparison Materials for Stable Isotopes of Light Elements; International Atomic Energy Agency: Vienna, Austria, 1995.
39. Böhlke, J. K.; Mroczkowski, S. J.; Coplen, T. B. Oxygen isotopes in nitrate: New reference materials for O-18: O-17: O-16 measurements and observations on nitrate-water equilibration. Rapid Commun. Mass Spectrom. 2003, 17 (16), 1835-1846. (Pubitemid 36986560)
40. Sigman, D. M.; DiFiore, P. J.; Hain, M. P.; Deutsch, C.; Wang, Y.; Karl, D. M.; Knapp, A. N.; Lehmann, M. F.; Pantoja, S. The dual isotopes of deep nitrate as a constraint on the cycle and budget of oceanic fixed nitrogen. Deep-Sea Res. Part I-Oceanogr. Res. Pap. 2009, 56 (9), 1419-1439.
41. Mariotti, A.; Germon, J. C.; Hubert, P.; Kaiser, P.; Letolle, R.; Tardieux, A.; Tardieux, P. Experimental determination of nitrogen kinetic isotope fractionation: Some principles; illustration for the denitrification and nitrification processes. Plant Soil 1981, 62, 413-430.
42. Trull, T. W.; Davies, D.; Casciotti, K. Insights into nutrient assimilation and export in naturally iron-fertilized waters of the Southern Ocean from nitrogen, carbon and oxygen isotopes. Deep-Sea Res. Part II-Top. Stud. Oceanogr. 2008, 55 (5-7), 820-840.
43. Revesz, K.; Bohlke, J. K. Comparison of O-delta 18 measurements in nitrate by different combustion techniques. Anal. Chem. 2002, 74 (20), 5410-5413.
44. Campbell, W. H. Nitrate reductase structure, function and regulation: Bridging the gap between biochemistry and physiology. Annu. Rev. Plant Physiol. Plant Molec. Biol. 1999, 50, 277-303. (Pubitemid 129491964)
45. Farquhar, G. D.; O'Leary, M. H.; Berry, J. A. On the relationship between carbon isotope discrimination and the intercellular carbon dioxide concentration in leaves. Austral. J. Plant Physiol. 1982, 9, 121-137. (Pubitemid 13280643)
46. Barbier, G. G.; Campbell, W. H. Viscosity effects on eukaryotic nitrate reductase activity. J. Biol. Chem. 2005, 280 (28), 26049-26054. (Pubitemid 41022196)
47. Kay, C. J.; Barber, M. J. Assimilatory nitrate reductase from Chlorella: Effect of ionic strength and pH on catalytic activity. J. Biol. Chem. 1986, 261 (30), 14125-14129.
48. Skipper, L.; Campbell, W. H.; Mertens, J. A.; Lowe, D. J. Pre-steady- state kinetic analysis of recombinant arabidopsis NADP: Nitrate reductase-rate-limiting processes in catalysis. J. Biol. Chem. 2001, 276 (29), 26995-27002.
49. Campbell, W. H. Structure and function of eukaryotic NAD(P)H: Nitrate reductase. Cell. Mol. Life Sci. 2001, 58 (2), 194-204. (Pubitemid 32217351)
50. Yoneyama, T.; Ito, O.; Engelaar, W. M. H. G. Uptake, metabolism and distribution of nitrogen in crop plants traced by enriched and natural 15N: Progress over the last 30 years. Phytochem. Rev. 2003, 2, 121-132. (Pubitemid 39012598)
51. Howard, W. D.; Solomonson, L. P. Kinetic mechanism of assimilatory NADH-nitrate reductase from Chlorella. J. Biol. Chem. 1981, 256 (24), 2725-2730.
52. McDonald, D. W.; Coddington, A. Properties of assimilatory nitrate reductase from Aspergillus Nidulans. Eur. J. Biochem. 1974, 46 (1), 169-178.
53. Cook, P. F. Kinetic and regulatory mechanisms of enzymes from isotope effects. In Enzyme Mechanism from Isotope Effects; Cook, P. F., Ed.; CRC Press: Boca Raton, FL, 1991; pp 203-230.
54. Hille, R.; Nishino, T.; Bittner, F. Molybdenum enzymes in higher organisms. Coord. Chem. Rev. 2011, 255, 1179-1205.
55. Amberger, A.; Schmidt, H. L. The natural isotope content of nitrate as an indicator of its origin. Geochim. Cosmochim. Acta 1987, 51 (10), 2699-2705.