Nitrogen isotope effects induced by anammox bacteria

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 47, 2013, Pages 18994-18999

  Brunner, Benjamin ^a,d   Contreras, Sergio ^a,e   Lehmann, Moritz F ^b   Matantseva, Olga ^a,f   Rollog, Mark ^b   Kalvelage, Tim ^a   Klockgether, Gabriele ^a   Lavik, Gaute ^a   Jetten, Mike S M ^c   Kartal, Boran ^c   Kuypers, Marcel M M ^a  

^a MAX PLANCK INSTITUTE FOR MARINE MICROBIOLOGY   (Germany)

^b UNIVERSITY OF BASEL   (Switzerland)

^c RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

^d AARHUS UNIVERSITY   (Denmark)

^e UNIVERSITY OF PITTSBURGH   (United States)

^f INSTITUTE OF CYTOLOGY   (Russian Federation)

Author keywords

[No Author keywords available]

Indexed keywords

AMMONIA; NITRITE; NITROGEN; OXYGEN;

ANAMMOX BACTERIUM; ARTICLE; BACTERIUM CULTURE; ENVIRONMENTAL STRESS; FRACTIONATION; NONHUMAN; OXIDATION; PRIORITY JOURNAL;

AMMONIUM COMPOUNDS; BACTERIA, ANAEROBIC; KINETICS; MODELS, BIOLOGICAL; NITROGEN ISOTOPES; OCEANS AND SEAS; SEAWATER;

EID: 84888103151     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1310488110     Document Type: Article

References (53)

1. Cline JD, Kaplan IR (1975) Isotopic fractionation of dissolved nitrate during denitrification in the eastern tropical north pacific ocean. Mar Chem 3:271-299.
2. Brandes JA, Devol AH, Yoshinari T, Jayakumar DA, Naqvi SWA (1998) Isotopic composition of nitrate in the Central Arabian Sea and Eastern Tropical North Pacific: A tracer for mixing and nitrogen cycles. Limnol Oceanogr 43:1680-1689.
3. Altabet M, Murray D, Prell W (1999) Climatically linked oscillations in Arabian Sea denitrification over the past 1 m.y.: Implications for the marine N cycle. Paleoceanography 14:732-743.
4. Brandes J, Devol A (2002) A global marine-fixed nitrogen isotopic budget: Implications for Holocene nitrogen cycling. Global Biogeochem Cycles 16(4-67-1-67-14.
5. Deutsch C, Sigman D, Thunell R, Meckler A, Haug G (2004) Isotopic constraints on glacial/interglacial changes in the oceanic nitrogen budget. Global Biogeochem Cycles, 10.1029/2003GB002189.
6. Wellman RP, Cook FD, Krouse HR (1968) Nitrogen-15: Microbiological alteration of abundance. Science 161(3838-269-270.
7. Delwiche CC, Steyn PL (1970) Nitrogen isotope fractionation in soils and microbial reactions. Environ Sci Technol 4:929-935.
8. Mariotti A, et al. (1981) Experimental determination of nitrogen kinetic isotope fractionation: Some principles; illustration for the denitrification and nitrification processes. Plant Soil 62:413-430.
9. Granger J, Sigman DM, Lehmann MF, Tortell PD (2008) Nitrogen and oxygen isotope fractionation during dissimilatory nitrate reduction by denitrifying bacteria. Limnol Oceanogr 53:2533-2545.
10. Brandes JA, Devol AH, Deutsch C (2007) New developments in the marine nitrogen cycle. Chem Rev 107(2-577-589.
11. Voss M, Dippner J, Montoya J (2001) Nitrogen isotope patterns in the oxygen-deficient waters of the Eastern Tropical North Pacific Ocean. Deep Sea Res Part I Oceanogr Res Pap 48:1905-1921.
12. Kuypers MM, et al. (2005) Massive nitrogen loss from the Benguela upwelling system through anaerobic ammonium oxidation. Proc Natl Acad Sci USA 102(18-6478-6483.
13. Thamdrup B, et al. (2006) Anaerobic ammonium oxidation in the oxygen-deficient waters off northern Chile. Limnol Oceanogr 51:2145-2156.
14. Devol AH (2003) Nitrogen cycle: Solution to a marine mystery. Nature 422(6932- 575-576.
15. Arrigo KR (2005) Marine microorganisms and global nutrient cycles. Nature 437(7057- 349-355.
16. Devol A (2003) Denitrification including Anammox. Nitrogen in the Marine Environment, eds Capone DG, Bronk DA, Mulholland M, Carpenter J (Academic, New York), 2nd Ed, pp 263-301.
17. Kartal B, Geerts W, Jetten MSM (2011) Research on Nitrification and Related Processes, Part A, Methods in Enzymology, ed Klotz MG (Academic, New York), pp 89-108. Available at http://www.sciencedirect.com/science/article/pii/ B9780123812940000043.
18. Kartal B, et al. (2011) Molecular mechanism of anaerobic ammonium oxidation. Nature 479(7371-127-130.
19. Strous M, et al. (1999) Missing lithotroph identified as new planctomycete. Nature 400(6743-446-449.
20. Tcherkez G, Farquhar GD (2006) Isotopic fractionation by plant nitrate reductase, twenty years later. Funct Plant Biol 33:531-537.
21. Yoshida N (1988) 15N-depleted N2O as a product of nitrification. Nature 335:528-529.
22. Casciotti K, Sigman D, Ward B (2003) Linking diversity and stable isotope fractionation in ammonia-oxidizing bacteria. Geomicrobiol J 20:335-353.
23. Bigeleisen J, Mayer MG (1947) Calculation of equilibrium constants for isotopic exchange reactions. J Chem Phys 15:261-267.
24. Schauble EA (2004) Applying stable isotope fractionation theory to new systems. Rev Mineral Geochem 55(1-65-111.
25. Spindel W (1954) The calculation of equilibrium constants for several exchange reactions of Nitrogen-15 between oxy compounds of nitrogen. J Chem Phys 22: 1271-1272.
26. Begun G, Fletcher W (1960) Partition function ratios for molecules containing nitrogen isotopes. J Chem Phys 33:1083-1085.
27. Casciotti KL (2009) Inverse kinetic isotope fractionation during bacterial nitrite oxidation. Geochim Cosmochim Acta 73:2061-2076.
28. Strous M, et al. (2006) Deciphering the evolution and metabolism of an anammox bacterium from a community genome. Nature 440(7085-790-794.
29. Kartal B, et al. (2013) How to make a living from anaerobic ammonium oxidation. FEMS Microbiol Rev 37(3-428-461.
30. Woebken D, Fuchs BM, Kuypers MMM, Amann R (2007) Potential interactions of particle-associated anammox bacteria with bacterial and archaeal partners in the Namibian upwelling system. Appl Environ Microbiol 73(14-4648-4657.
31. Stocker R (2012) Marine microbes see a sea of gradients. Science 338(6107-628-633.
32. Kalvelage T, et al. (2013) Nitrogen cycling driven by organic matter export in the South Pacific oxygen minimum zone. Nat Geosci 6:228-234.
33. Fry B, Ruf W, Gest H, Hayes JM (1988) Sulfur isotope effects associated with oxidation of sulfide by O2 in aqueous solution. Isot Geosci 73:205-210.
34. Lücker S, et al. (2010) A Nitrospira metagenome illuminates the physiology and evolution of globally important nitrite-oxidizing bacteria. Proc Natl Acad Sci USA 107(30-13479-13484.
35. Buchwald C, Casciotti KL (2010) Oxygen isotopic fractionation and exchange during bacterial nitrite oxidation. Limnol Oceanogr 55:1064-1074.
36. Rees CE (1973) A steady-state model for sulphur isotope fractionation in bacterial reduction processes. Geochim Cosmochim Acta 37:1141-1162.
37. Kartal B, et al. (2007) Anammox bacteria disguised as denitrifiers: Nitrate reduction to dinitrogen gas via nitrite and ammonium. Environ Microbiol 9(3-635-642.
38. Holler T, et al. (2011) Carbon and sulfur back flux during anaerobic microbial oxidation of methane and coupled sulfate reduction. Proc Natl Acad Sci USA 108(52- E1484-E1490.
39. Kritee K, et al. (2012) Reduced isotope fractionation by denitrification under conditions relevant to the ocean. Geochim Cosmochim Acta 92:243-259.
40. Bryan BA, Shearer G, Skeeters JL, Kohl DH (1983) Variable expression of the nitrogen isotope effect associated with denitrification of nitrite. J Biol Chem 258(14- 8613-8617.
41. Lehmann MF, Sigman D, Berelson W (2004) Coupling the N-15/N-14 and O-18/O-16 of nitrate as a constraint on benthic nitrogen cycling. Mar Chem 88(1-1-20.
42. Lehmann MF, et al. (2007) The distribution of nitrate 15N/14N in marine sediments and the impact of benthic nitrogen loss on the isotopic composition of oceanic nitrate. Geochim Cosmochim Acta 71:5384-5404.
43. Casciotti KL, Buchwald C, McIlvin M (2013) Implications of nitrate and nitrite isotopic measurements for the mechanisms of nitrogen cycling in the Peru oxygen deficient zone. Deep Sea Res Part I Oceanogr Res Pap 80:78-93.
44. Casciotti KL, McIlvin MR (2007) Isotopic analyses of nitrate and nitrite from reference mixtures and application to Eastern Tropical North Pacific waters. Mar Chem 107(2- 184-201.
45. Grasshoff K, Kremling K, Ehrhardt M (1999) Methods of Seawater Analysis (Wiley- VCH, Göttingen, Germany), 3rd Ed.
46. Braman RS, Hendrix SA (1989) Nanogram nitrite and nitrate determination in environmental and biological materials by vanadium (III) reduction with chemiluminescence detection. Anal Chem 61(24-2715-2718.
47. Sigman DM, et al. (1997) Natural abundance-level measurement of the nitrogen isotopic composition of oceanic nitrate: An adaptation of the ammonia diffusion method. Mar Chem 57:227-242.
48. Holmes RM, McClelland JW, Sigman DM, Fry B, Peterson BJ (1998) Measuring 15N-NH+ 4 in marine, estuarine and fresh waters: An adaptation of the ammonia diffusion method for samples with low ammonium concentrations. Mar Chem 60:235-243.
49. McIlvin MR, Altabet MA (2005) Chemical conversion of nitrate and nitrite to nitrous oxide for nitrogen and oxygen isotopic analysis in freshwater and seawater. Anal Chem 77(17-5589-5595.
50. Sigman DM, et al. (2001) A bacterial method for the nitrogen isotopic analysis of nitrate in seawater and freshwater. Anal Chem 73(17-4145-4153.
51. Granger J, Sigman DM (2009) Removal of nitrite with sulfamic acid for nitrate N and O isotope analysis with the denitrifier method. Rapid Commun Mass Spectrom 23(23- 3753-3762.
52. HoltappelsM, Lavik G, Jensen MM, KuypersMMM(2011) 15N-labeling experiments to dissect the contributions of heterotrophic denitrification and anammox to nitrogen removal in the OMZ waters of the ocean. Research on Nitrification and Related Processes, Part A, Methods in Enzymology, ed Klotz MG (Academic, New York), pp 223-251.
53. Füssel J, et al. (2012) Nitrite oxidation in the Namibian oxygen minimum zone. ISME J 6(6-1200-1209.