Subseafloor nitrogen transformations in diffuse hydrothermal vent fluids of the Juan de Fuca Ridge evidenced by the isotopic composition of nitrate and ammonium

Geochemistry, Geophysics, Geosystems

Volumn 13, Issue 2, 2012, Pages

  Bourbonnais, Annie ^a   Lehmann, Moritz F ^b   Butterfield, David A ^c   Juniper, S Kim ^a  

^a UNIVERSITY OF VICTORIA   (Canada)

^b UNIVERSITY OF BASEL   (Switzerland)

^c UNIVERSITY OF WASHINGTON   (United States)

Author keywords

hydrothermal vent fluids; Juan de Fuca Ridge; nitrate and ammonium isotopes; nitrogen cycle; Northeast Pacific Ocean; subsurface biosphere

Indexed keywords

AMMONIUM COMPOUNDS; ANOXIC SEDIMENTS; CARRIER MOBILITY; DENITRIFICATION; HOT SPRINGS; ISOTOPES; NITROGEN;

BACTERIAL MATS; CONCENTRATION VARIATION; DEEP OCEAN; DISSOLVED INORGANIC NITROGENS; DOMINANT PROCESS; HIGH-T; HYDROTHERMAL FLUXES; HYDROTHERMAL VENT; HYDROTHERMALLY; IN-SITU PRODUCTION; ISOTOPE DATA; ISOTOPE EFFECT; ISOTOPE RATIO; ISOTOPE VALUES; ISOTOPIC COMPOSITION; ISOTOPIC MEASUREMENT; JUAN DE FUCA RIDGE; MICROBIAL COMMUNITIES; NITRATE ASSIMILATION; NITRATE CONCENTRATION; NITRATE CONSUMPTION; NITRATE ISOTOPES; NITRATE REDUCTION; NITROGEN CYCLE; NITROGEN TRANSFORMATIONS; ORGANIC SEDIMENTS; PACIFIC OCEAN; PARTIAL NITRIFICATION; RE-OXIDATION; SEA FLOOR; SUB-SEAFLOOR; SUBSURFACE BIOSPHERE; WATER MASS;

NITRATES;

AMMONIUM; DENITRIFICATION; DISSOLVED INORGANIC NITROGEN; HYDROTHERMAL FLUID; HYDROTHERMAL VENT; ISOTOPIC COMPOSITION; ISOTOPIC RATIO; MIXING; NITRATE; NITRIFICATION; NITROGEN CYCLE; OXIDATION; SEAFLOOR; WATER MASS;

JUAN DE FUCA RIDGE; PACIFIC OCEAN; PACIFIC OCEAN (NORTHEAST);

BACTERIA (MICROORGANISMS);

EID: 84856695729     PISSN: None     EISSN: 15252027     Source Type: Journal    
DOI: 10.1029/2011GC003863     Document Type: Article

References (98)

1. Altabet, M. A. (2001), Nitrogen isotopic evidence for micronutrient control of fractional NO3- utilization in the equatorial pacific, Limnol. Oceanogr., 46(2), 368-380, doi:10.4319/ lo.2001.46.2.0368. (Pubitemid 32281612)
2. Andersson, K. K., and A. B. Hooper (1983), O2 and H 2O are each the source of one O in NO2- produced from NH3 by Nitrosomonas: 15N-NMR evidence, FEBS Lett., 164(2), 236-240, doi:10.1016/0014-5793(83)80292-0.
3. Bender, M. L. (1990), The δ18O of dissolved O 2 in seawater: A unique tracer of circulation and respiration in the deep sea, J. Geophys. Res., 95(C12), 22,243-22,252, doi:10.1029/ JC095iC12p22243.
4. Berman-Frank, I., Y. B. Chen, Y. Gerchman, G. Dismukes, and P. Falkowski (2005), Inhibition of nitrogenase by oxygen in marine cyanobacteria controls the global nitrogen and oxygen cycles, Biogeosci. Discuss., 2(2), 261-273, doi:10.5194/bgd-2-261-2005. (Pubitemid 41261670)
5. Böhlke, J. K., S. J. Mroczkowski, and T. B. Coplen (2003), Oxygen isotopes in nitrate: New reference materials for 18O: 17O: 16O measurements and observations on nitratewater equilibration, Rapid Commun. Mass Spectrom., 17(16), 1835-1846, doi:10.1002/rcm.1123. (Pubitemid 36986560)
6. Bourbonnais, A., M. F. Lehmann, J. J. Waniek, and D. E. Schulz-Bull (2009), Nitrate isotope anomalies reflect N2 fixation in the Azores Front region (subtropical NE Atlantic), J. Geophys. Res., 114, C03003, doi:10.1029/2007JC004617.
7. Braman, R. S., and S. A. Hendrix (1989), Nanogram nitrite and nitrate determination in environmental and biological materials by vanadium (III) reduction with chemiluminescence detection, Anal. Chem., 61(24), 2715-2718, doi:10.1021/ ac00199a007. (Pubitemid 20065839)
8. Brandes, J. A., and A. H. Devol (1997), Isotopic fractionation of oxygen and nitrogen in coastal marine sediments, Geochim. Cosmochim. Acta, 61(9), 1793-1801, doi:10.1016/ S0016-7037(97)00041-0.
9. Brandes, J. A., and A. H. Devol (2002), A global marine-fixed nitrogen isotopic budget: Implications for Holocene nitrogen cycling, Global Biogeochem. Cycles, 16(4), 1120, doi:10.1029/ 2001GB001856.
10. Brandes, J. A., N. Z. Boctor, G. D. Cody, B. A. Cooper, R. M. Hazen, and H. S. Yoder (1998a), Abiotic nitrogen reduction on the early Earth, Nature, 395(6700), 365-367, doi:10.1038/26450. (Pubitemid 28450682)
11. Brandes, J. A., A. H. Devol, T. Yoshinari, D. A. Jayakumar, and S. W. A. Naqvi (1998b), Isotopic composition of nitrate in the central Arabian Sea and eastern tropical North Pacific: A tracer for mixing and nitrogen cycles, Limnol. Oceanogr., 43(7), 1680-1689, doi:10.4319/lo.1998.43.7.1680. (Pubitemid 28552082)
12. Brandes, J. A., R. M. Hazen, and H. S. Yoder Jr. (2008), Inorganic nitrogen reduction and stability under simulated hydrothermal conditions, Astrobiology, 8(6), 1113-1126, doi:10.1089/ast.2007.0187.
13. Buchwald, C., and K. L. Casciotti (2010), Oxygen isotopic fractionation and exchange during bacterial nitrite oxidation, Limnol. Oceanogr., 55(3), 1064-1074, doi:10.4319/lo.2010. 55.3.1064.
14. Busigny, V., C. Laverne, and M. Bonifacie (2005), Nitrogen content and isotopic composition of oceanic crust at a superfast spreading ridge: A profile in altered basalts from ODP Site 1256, Leg 206, Geochem. Geophys. Geosyst., 6, Q12O01, doi:10.1029/2005GC001020.
15. Butterfield, D. A., I. R. Jonasson, G. J. Massoth, R. A. Feely, K. K. Roe, R. E. Embley, J. F. Holden, R. E. McDuff, M. D. Lilley, and J. R. Delaney (1997), Seafloor eruptions and evolution of hydrothermal fluid chemistry, Philos. Trans. R. Soc. London A, 355(1723), 369-386.
16. Butterfield, D. A., K. K. Roe, M. D. Lilley, J. A. Huber, J. A. Baross, R. W. Embley, and G. J. Massoth (2004), Mixing, reaction and microbial activity in the sub-seafloor revealed by temporal and spatial variation in diffuse flow vents at Axial Volcano, in The Subseafloor Biosphere at Mid-Ocean Ridges, Geophys. Monogr. Ser., vol. 144, edited by W. S. Wilcock et al., pp. 269-289, AGU, Washington, D. C., doi:10.1029/144GM17.
17. Byrne, N., M. Strous, V. Crépeau, B. Kartal, J. L. Birrien, M. Schmid, F. Lesongeur, S. Schouten, A. Jaeschke, and M. Jetten (2009), Presence and activity of anaerobic ammonium-oxidizing bacteria at deep-sea hydrothermal vents, ISME J., 3(1), 117-123, doi:10.1038/ismej.2008.72.
18. Carpenter, E. J., H. R. Harvey, B. Fry, and D. G. Capone (1997), Biogeochemical tracers of the marine cyanobacterium Trichodesmium, Deep Sea Res., Part I, 44(1), 27-38, doi:10.1016/S0967-0637(96)00091-X. (Pubitemid 27115227)
19. Carpenter, E. J., J. P. Montoya, J. Burns, M. R. Mulholland, A. Subramaniam, and D. G. Capone (1999), Extensive bloom of a N2-fixing diatom/cyanobacterial association in the tropical Atlantic Ocean, Mar. Ecol. Prog. Ser., 185, 273-283, doi:10.3354/meps185273. (Pubitemid 29429170)
20. Casciotti, K. L. (2002), Molecular and stable isotopic characterization of enzymes involved in nitrification and nitrifierdenitrification, PhD thesis, Princeton Univ., Princeton, N. J.
21. Casciotti, K. L., and M. R. McIlvin (2007), Isotopic analyses of nitrate and nitrite from reference mixtures and application to Eastern Tropical North Pacific waters, Mar. Chem., 107(2), 184-201, doi:10.1016/j.marchem.2007.06.021. (Pubitemid 47539713)
22. Casciotti, K. L., D. M. Sigman, M. G. Hastings, J. K. Böhlke, and A. Hilkert (2002), Measurement of the oxygen isotopic composition of nitrate in seawater and freshwater using the denitrifier method, Anal. Chem., 74(19), 4905-4912, doi:10.1021/ac020113w.
23. Casciotti, K. L., D. M. Sigman, and B. B. Ward (2003), Linking diversity and stable isotope fractionation in ammoniaoxidizing bacteria, Geomicrobiol. J., 20(4), 335-353, doi:10.1080/01490450303895. (Pubitemid 37156087)
24. Casciotti, K. L., J. K. Böhlke, M. R. McIlvin, S. J. Mroczkowski, and J. E. Hannon (2007), Oxygen isotopes in nitrite: Analysis, calibration, and equilibration, Anal. Chem., 79(6), 2427-2436, doi:10.1021/ac061598h. (Pubitemid 46449024)
25. Casciotti, K. L., M. McIlvin, and C. Buchwald (2010), Oxygen isotopic exchange and fractionation during bacterial ammonia oxidation, Limnol. Oceanogr., 55(2), 753-762, doi:10.4319/ lo.2009.55.2.0753.
26. Cline, J. D., and I. R. Kaplan (1975), Isotopic fractionation of dissolved nitrate during denitrification in the eastern tropical North Pacific Ocean, Mar. Chem., 3(4), 271-299, doi:10.1016/0304-4203(75)90009-2.
27. Dalsgaard, T., D. E. Canfield, J. Petersen, B. Thamdrup, and J. Acuna-González (2003), N2 production by the anammox reaction in the anoxic water column of Golfo Dulce, Costa Rica, Nature, 422(6932), 606-608, doi:10.1038/nature01526. (Pubitemid 36460411)
28. Delwiche, C. C., and P. L. Steyn (1970), Nitrogen isotope fractionation in soils and microbial reactions, Environ. Sci. Technol., 4(11), 929-935, doi:10.1021/es60046a004.
29. Dispirito, A. A., and A. B. Hooper (1986), Oxygen exchange between nitrate molecules during nitrite oxidation by Nitrobacter, J. Biol. Chem., 261(23), 10,534-10,537. (Pubitemid 17194830)
30. Dörr, M., J. Käbohrer, R. Grunert, G. Kreisel, W. A. Brand, R. A. Werner, H. Geilmann, C. Apfel, C. Robl, and W. Weigand (2003), A possible prebiotic formation of ammonia from dinitrogen on iron sulfide surfaces, Angew. Chem. Int. Ed., 42(13), 1540-1543, doi:10.1002/anie.200250371. (Pubitemid 36458520)
31. Dortch, Q. (1990), The interaction between ammonium and nitrate uptake in phytoplankton, Mar. Ecol. Prog. Ser., 61(1), 183-201, doi:10.3354/meps061183.
32. Dugdale, R. C., F. P. Wilkerson, V. E. Hogue, and A. Marchi (2007), The role of ammonium and nitrate in spring bloom development in San Francisco Bay, Estuarine Coastal Shelf Sci., 73(1-2), 17-29, doi:10.1016/j.ecss.2006.12.008. (Pubitemid 46686907)
33. Edmond, J. M., C. Measures, R. E. McDuff, L. H. Chan, R. Collier, B. Grant, L. I. Gordon, and J. B. Corliss (1979), Ridge crest hydrothermal activity and the balances of the major and minor elements in the ocean: The Galapagos data, Earth Planet. Sci. Lett., 46(1), 1-18, doi:10.1016/0012- 821X(79)90061-X.
34. Embley, R. W., K. M. Murphy, and C. G. Fox (1990), High-resolution studies of the summit of Axial Volcano, J. Geophys. Res., 95(B8), 12,785-12,812, doi:10.1029/ JB095iB08p12785.
35. Granger, J., and D. M. Sigman (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, doi:10.1002/rcm.4307.
36. Granger, J., D. M. Sigman, J. A. Needoba, and P. J. Harrison (2004), Coupled nitrogen and oxygen isotope fractionation of nitrate during assimilation by cultures of marine phytoplankton, Limnol. Oceanogr., 49(5), 1763-1773, doi:10.4319/ lo.2004.49.5.1763. (Pubitemid 39320766)
37. Granger, J., D. M. Sigman, M. G. Prokopenko, M. F. Lehmann, and P. D. Tortell (2006), A method for nitrite removal in nitrate N and O isotope analyses, Limnol. Oceanogr. Methods, 4, 205-212, doi:10.4319/lom.2006.4.205.
38. Granger, J., D. M. Sigman, M. F. Lehmann, and P. D. Tortell (2008), Nitrogen and oxygen isotope fractionation during dissimilatory nitrate reduction by denitrifying bacteria, Limnol. Oceanogr., 53(6), 2533-2545, doi:10.4319/lo.2008. 53.6.2533.
39. Hall, A. (1989), Ammonium in spilitized basalts of southwest England and its implications for the recycling of nitrogen, Geochem. J., 23, 19-23, doi:10.2343/geochemj.23.19.
40. Hamersley, M. R., G. Lavik, D. Woebken, J. E. Rattray, P. Lam, E. C. Hopmans, J. S. S. Damste, S. Krüger, M. Graco, and D. Gutiérrez (2007), Anaerobic ammonium oxidation in the Peruvian oxygen minimum zone, Limnol. Oceanogr., 52(3), 923-933, doi:10.4319/lo.2007.52.3.0923. (Pubitemid 46827143)
41. Hentschel, U., and H. Felbeck (1993), Nitrate respiration in the hydrothermal vent tubeworm Riftia pachyptila, Nature, 366, 338-340, doi:10.1038/366338a0.
42. Hoch, M. P., M. L. Fogel, and D. L. Kirchman (1992), Isotope fractionation associated with ammonium uptake by a marine bacterium, Limnol. Oceanogr., 37(7), 1447-1459, doi:10.4319/lo.1992.37.7.1447.
43. Holloway, J. M., D. K. Nordstrom, J. K. Böhlke, R. B. McCleskey, and J. W. Ball (2011), Ammonium in thermal waters of Yellowstone National Park: Processes affecting speciation and isotope fractionation, Geochim. Cosmochim. Acta, 75, 4611-4636, doi:10.1016/j.gca.2011.05.036.
44. Houlton, B. Z., D. M. Sigman, E. A. G. Schuur, and L. O. Hedin (2007), A climate-driven switch in plant nitrogen acquisition within tropical forest communities, Proc. Natl. Acad. Sci. U. S. A., 104(21), 8902-8906, doi:10.1073/ pnas.0609935104. (Pubitemid 47175409)
45. Huber, J. A., D. A. Butterfield, and J. A. Baross (2002), Temporal changes in archaeal diversity and chemistry in a midocean ridge subseafloor habitat, Appl. Environ. Microbiol., 68(4), 1585-1594, doi:10.1128/AEM.68.4.1585- 1594.2002. (Pubitemid 34279962)
46. Huber, J. A., D. A. Butterfield, and J. A. Baross (2003), Bacterial diversity in a subseafloor habitat following a deep-sea volcanic eruption, FEMS Microbiol. Ecol., 43(3), 393-409, doi:10.1111/j.1574-6941.2003.tb01080.x. (Pubitemid 36293954)
47. Jannasch, H. W., and M. J. Mottl (1985), Geomicrobiology of deep-sea hydrothermal vents, Science, 229(4715), 717-725, doi:10.1126/science.229.4715. 717.
48. Javoy, M., and F. Pineau (1991), The volatiles record of a "popping" rock from the Mid-Atlantic Ridge at 14°N: chemical and isotopic composition of gas trapped in the vesicles, Earth Planet. Sci. Lett., 107, 598-611, doi:10.1016/0012- 821X(91)90104-P.
49. Juniper, S. K., P. Martineu, J. Sarrazin, and Y. Gelinas (1995), Microbial-mineral floc associated with nascent hydrothermal activity on CoAxial Segment, Juan de Fuca Ridge, Geophys. Res. Lett., 22(2), 179-182, doi:10.1029/94GL02436.
50. Kennicutt, I. I., and R. A. Burke (1992), Stable isotope partitioning in seep and vent organisms: Chemical and ecological significance, Chem. Geol., 101(3-4), 293-310. (Pubitemid 23386289)
51. Knapp, A. N., D. M. Sigman, and F. Lipschultz (2005), N isotopic composition of dissolved organic nitrogen and nitrate at the Bermuda Atlantic Time-Series Study site, Global Biogeochem. Cycles, 19, GB1018, doi:10.1029/2004GB002320. (Pubitemid 40801469)
52. Knapp, A. N., P. J. DiFiore, C. Deutsch, D. M. Sigman, and F. Lipschultz (2008), Nitrate isotopic composition between Bermuda and Puerto Rico: Implications for N2 fixation in the Atlantic Ocean, Global Biogeochem. Cycles, 22, GB3014, doi:10.1029/2007GB003107.
53. Kumar, S., D. J. D. Nicholas, and E. H. Williams (1983), Definitive 15N NMR evidence that water serves as a source of O during nitrite oxidation by Nitrobacter agilis, FEBS Lett., 152(1), 71-74, doi:10.1016/0014- 5793(83)80484-0.
54. Kuypers, M. M. M., A. O. Sliekers, G. Lavik, M. Schmid, B. B. Jørgensen, J. G. Kuenen, J. S. S. Damsté, M. Strous, and M. S. M. Jetten (2003), Anaerobic ammonium oxidation by anammox bacteria in the Black Sea, Nature, 422(6932), 608-611, doi:10.1038/nature01472. (Pubitemid 36460412)
55. Kuypers, M. M. M., G. Lavik, D. Woebken, M. Schmid, B. M. Fuchs, R. Amann, B. B. Jørgensen, and M. S. M. Jetten (2005), Massive nitrogen loss from the Benguela upwelling system through anaerobic ammonium oxidation, Proc. Natl. Acad. Sci. U. S. A., 102(18), 6478-6483, doi:10.1073/ pnas.0502088102. (Pubitemid 40617468)
56. Lam, P., J. P. Cowen, and R. D. Jones (2004), Autotrophic ammonia oxidation in a deep-sea hydrothermal plume, FEMS Microbiol. Ecol., 47(2), 191-206, doi:10.1016/ S0168-6496(03)00256-3.
57. Lam, P., J. P. Cowen, B. N. Popp, and R. D. Jones (2008), Microbial ammonia oxidation and enhanced nitrogen cycling in the Endeavour hydrothermal plume, Geochim. Cosmochim. Acta, 72(9), 2268-2286, doi:10.1016/j.gca.2008.01. 033.
58. Lee, R. W., and J. J. Childress (1994), Assimilation of inorganic nitrogen by marine invertebrates and their chemoautotrophic and methanotrophic symbionts, Appl. Environ. Microbiol., 60(6), 1852-1858. (Pubitemid 24165829)
59. Lehmann, M. F., P. Reichert, S. M. Bernasconi, A. Barbieri, and J. A. McKenzie (2003), Modelling nitrogen and oxygen isotope fractionation during denitrification in a lacustrine redox-transition zone, Geochim. Cosmochim. Acta, 67(14), 2529-2542, doi:10.1016/S0016-7037(03)00085-1. (Pubitemid 36933364)
60. Lehmann, M. F., D. M. Sigman, and W. M. Berelson (2004), Coupling the 15N/14N and 18O/16O of nitrate as a constraint on benthic nitrogen cycling, Mar. Chem., 88(1-2), 1-20, doi:10.1016/j.marchem.2004.02.001. (Pubitemid 38700309)
61. Lehmann, M. F., D. M. Sigman, D. C. McCorkle, B. G. Brunelle, S. S. Hoffmann, M. Kienast, G. Cane, and J. Clement (2005), Origin of the deep Bering Sea nitrate deficit: Constraints from the nitrogen and oxygen isotopic composition of water column nitrate and benthic nitrate fluxes, Global Biogeochem. Cycles, 19, GB4005, doi:10.1029/ 2005GB002508.
62. Lehmann, M. F., D. M. Sigman, D. C. McCorkle, J. Granger, S. Hoffmann, G. Cane, and B. G. Brunelle (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(22), 5384-5404, doi:10.1016/j.gca.2007.07.025. (Pubitemid 350028597)
63. Lehmann, M. F., B. Barnett, Y. Gélinas, D. Gilbert, R. J. Maranger, A. Mucci, B. Sundby, and B. Thibodeau (2009), Aerobic respiration and hypoxia in the Lower St. Lawrence Estuary: Stable isotope ratios of dissolved oxygen constrain oxygen sink partitioning, Limnol. Oceanogr., 54(6), 2157-2169, doi:10.4319/lo.2009.54.6.2157.
64. Levesque, C., H. Limén, and S. K. Juniper (2005), Origin, composition and nutritional quality of particulate matter at deep-sea hydrothermal vents on Axial Volcano, NE Pacific, Mar. Ecol. Prog. Ser., 289, 43-52, doi:10.3354/ meps289043. (Pubitemid 40600473)
65. Levine, N. M., M. L. Bender, and S. C. Doney (2009), The δ18O of dissolved O2 as a tracer of mixing and respiration in the mesopelagic ocean, Global Biogeochem. Cycles, 23, GB1006, doi:10.1029/2007GB003162.
66. Lilley, M. D., D. A. Butterfield, E. J. Olson, J. E. Lupton, S. A. Macko, and R. E. McDuff (1993), Anomalous CH4 and NH4 + concentrations at an unsedimented mid-ocean-ridge hydrothermal system, Nature, 364, 45-47, doi:10.1038/ 364045a0. (Pubitemid 24429270)
67. Mariotti, A., J. C. Germon, P. Hubert, P. Kaiser, R. Letolle, A. Tardieux, and P. Tardieux (1981), Experimental determination of nitrogen kinetic isotope fractionation: Some principles; illustration for the denitrification and nitrification processes, Plant Soil, 62(3), 413-430, doi:10.1007/ BF02374138.
68. Marty, B., and F. Humbert (1997), Nitrogen and argon isotopes in oceanic basalts, Earth Planet. Sci. Lett., 152(1-4), 101-112, doi:10.1016/S0012-821X(97) 00153-2.
69. McHatton, S. C., J. P. Barry, H. W. Jannasch, and D. C. Nelson (1996), High nitrate concentrations in vacuolate, autotrophic marine Beggiatoa spp, Appl. Environ. Microbiol., 62(3), 954-958. (Pubitemid 26071464)
70. Mehta, M. P., and J. A. Baross (2006), Nitrogen fixation at 92°C by a hydrothermal vent archaeon, Science, 314(5806), 1783-1786, doi:10.1126/science. 1134772. (Pubitemid 44969091)
71. Mehta, M. P., D. A. Butterfield, and J. A. Baross (2003), Phylogenetic diversity of nitrogenase (nifH) genes in deepsea and hydrothermal vent environments of the Juan de Fuca Ridge, Appl. Environ.Microbiol., 69(2), 960-970, doi:10.1128/ AEM.69.2.960-970.2003. (Pubitemid 36204825)
72. Mehta, M. P., J. A. Huber, and J. A. Baross (2005), Incidence of novel and potentially archaeal nitrogenase genes in the deep Northeast Pacific Ocean, Environ. Microbiol., 7(10), 1525-1534, doi:10.1111/j.1462-2920.2005.00836.x. (Pubitemid 41345895)
73. Montoya, J. P., E. J. Carpenter, and D. G. Capone (2002), Nitrogen fixation and nitrogen isotope abundances in zooplankton of the oligotrophic North Atlantic, Limnol. Oceanogr., 47(6), 1617-1628, doi:10.4319/lo.2002.47.6. 1617. (Pubitemid 36016820)
74. Moyer, C. L., F. C. Dobbs, and D. M. Karl (1995), Phylogenetic diversity of the bacterial community from a microbial mat at an active, hydrothermal vent system, Loihi Seamount, Hawaii, Appl. Environ. Microbiol., 61(4), 1555-1562.
75. Paull, C. K., A. J. T. Jull, L. J. Toolin, and T. Linick (1985), Stable isotope evidence for chemosynthesis in an abyssal seep community, Nature, 317, 709-711, doi:10.1038/ 317709a0. (Pubitemid 16277780)
76. Perez-Rodriguez, I., J. Ricci, J.W. Voordeckers, V. Starovoytov, and C. Vetriani (2010), Nautilia nitratireducens sp. nov., a thermophilic, anaerobic, chemosynthetic, nitrate-ammonifying bacterium isolated from a deep-sea hydrothermal vent, Int. J. Syst. Evol. Microbiol., 60(5), 1182-1186, doi:10.1099/ ijs.0.013904-0.
77. Proctor, L. M. (1997), Nitrogen-fixing, photosynthetic, anaerobic bacteria associated with pelagic copepods, Aquat. Microb. Ecol., 12, 105-113, doi:10.3354/ame012105. (Pubitemid 127472842)
78. Rau, G. H. (1981), Low 15N/14N in hydrothermal vent animals: Ecological implications, Nature, 289, 484-485, doi:10.1038/ 289484a0.
79. Schoonen, M. A. A., and Y. Xu (2001), Nitrogen reduction under hydrothermal vent conditions: Implications for the prebiotic synthesis of CHON compounds, Astrobiology, 1(2), 133-142, doi:10.1089/153110701753198909.
80. Seyfried, W., Jr. (1987), Experimental and theoretical constraints on hydrothermal alteration processes at midocean ridges, Annu. Rev. Earth Planet. Sci., 15, 317-335, doi:10.1146/annurev.ea.15.050187.001533.
81. Sigman, D. M., and K. L. Casciotti (2001), Nitrogen isotopes in the ocean, in Encyclopedia of Ocean Sciences, edited by J. H. Steele, S. A. Thorpe, and K. K. Turekian, pp. 1884-1894, Academic, San Diego, Calif., doi:10.1006/rwos.2001.0172.
82. Sigman, D. M., M. A. Altabet, R. Michener, D. C. McCorkle, B. Fry, and R. M. Holmes (1997), Natural abundancelevel measurement of the nitrogen isotopic composition of oceanic nitrate: An adaptation of the ammonia diffusion method, Mar. Chem., 57(3-4), 227-242, doi:10.1016/S0304- 4203(97)00009-1. (Pubitemid 27369728)
83. Sigman, D. M., K. L. Casciotti, M. Andreani, C. Barford, M. Galanter, and J. K. Böhlke (2001), A bacterial method for the nitrogen isotopic analysis of nitrate in seawater and freshwater, Anal. Chem., 73(17), 4145-4153, doi:10.1021/ ac010088e. (Pubitemid 32830853)
84. Sigman, D. M., R. Robinson, A. N. Knapp, A. van Geen, D. C. McCorkle, J. A. Brandes, and R. C. Thunell (2003), Distinguishing between water column and sedimentary denitrification in the Santa Barbara Basin using the stable isotopes of nitrate, Geochem. Geophys. Geosyst., 4(5), 1040, doi:10.1029/2002GC000384.
85. Sigman, D. M., J. Granger, P. J. DiFiore, M. M. Lehmann, R. Ho, G. Cane, and A. van Geen (2005), Coupled nitrogen and oxygen isotope measurements of nitrate along the eastern North Pacific margin, Global Biogeochem. Cycles, 19, GB4022, doi:10.1029/2005GB002458. (Pubitemid 43280685)
86. Sigman, D. M., P. J. DiFiore, M. P. Hain, C. Deutsch, Y. Wang, D. M. Karl, A. N. Knapp, M. F. Lehmann, and S. Pantoja (2009), The dual isotopes of deep nitrate as a constraint on the cycle and budget of oceanic fixed nitrogen, Deep Sea Res., Part I, 56(9), 1419-1439, doi:10.1016/j. dsr.2009.04.007.
87. Thamdrup, B., and T. Dalsgaard (2002), Production of N2 through anaerobic ammonium oxidation coupled to nitrate reduction in marine sediments, Appl. Environ. Microbiol., 68(3), 1312-1318, doi:10.1128/AEM.68.3. 1312-1318.2002. (Pubitemid 34205371)
88. Tunnicliffe, V. (1991), The biology of hydrothermal vents: Ecology and evolution, Oceanogr. Mar. Biol., 29, 319-407. (Pubitemid 23403149)
89. Tunnicliffe, V., S. K. Juniper, and M. E. De Burgh (1985), The hydrothermal vent community on Axial Seamount, Juan de Fuca Ridge, Bull. Biol. Soc. Wash., 6, 453-464.
90. Van Dover, C. (2002), Trophic relationships among invertebrates at the Kairei hydrothermal vent field (Central Indian Ridge), Mar. Biol. Berlin, 141(4), 761-772, doi:10.1007/ s00227-002-0865-y. (Pubitemid 36072731)
91. Van Dover, C. L., and B. Fry (1994), Microorganisms as food resources at deep-sea hydrothermal vents, Limnol. Oceanogr., 39(1), 51-57, doi:10.4319/lo.1994.39.1.0051. (Pubitemid 2050671)
92. Vetriani, C., M. D. Speck, S. V. Ellor, R. A. Lutz, and V. Starovoytov (2004), Thermovibrio ammonificans sp. nov., a thermophilic, chemolithotrophic, nitrate-ammonifying bacterium from deep-sea hydrothermal vents, Int. J. Syst. Evol. Microbiol., 54(1), 175-181, doi:10.1099/ijs.0.02781-0. (Pubitemid 38181287)
93. Voordeckers, J. W., V. Starovoytov, and C. Vetriani (2005), Caminibacter mediatlanticus sp. nov., a thermophilic, chemolithoautotrophic, nitrate-ammonifying bacterium isolated from a deep-sea hydrothermal vent on the Mid-Atlantic Ridge, Int. J. Syst. Evol. Microbiol., 55(2), 773-779, doi:10.1099/ijs.0.63430-0. (Pubitemid 40485069)
94. Voss, M., J. W. Dippner, and J. P. Montoya (2001), Nitrogen isotope patterns in the oxygen-deficient waters of the Eastern Tropical North Pacific Ocean, Deep Sea Res., Part I, 48(8), 1905-1921, doi:10.1016/S0967-0637(00)00110- 2. (Pubitemid 32507443)
95. Wankel, S. D., C. Kendall, J. T. Pennington, F. P. Chavez, and A. Paytan (2007), Nitrification in the euphotic zone as evidenced by nitrate dual isotopic composition: Observations from Monterey Bay, California, Global Biogeochem. Cycles, 21, GB2009, doi:10.1029/2006GB002723. (Pubitemid 47323958)
96. Waser, N. A. D., P. J. Harrison, B. Nielsen, S. E. Calvert, and D. H. Turpin (1998), Nitrogen isotope fractionation during the uptake and assimilation of nitrate, nitrite, ammonium, and urea by a marine diatom, Limnol. Oceanogr., 43(2), 215-224, doi:10.4319/lo.1998.43.2.0215. (Pubitemid 28278380)
97. Yoshida, N. (1988), N-depleted N4O as a product of nitrification, Nature, 335, 528-529, doi:10.1038/335528a0.
98. Zehr, J. P., B. D. Jenkins, S. M. Short, and G. F. Steward (2003), Nitrogenase gene diversity and microbial community structure: A cross-system comparison, Environ. Microbiol., 5(7), 539-554, doi:10.1046/j.1462-2920.2003. 00451.x. (Pubitemid 36832210)