Anammox, denitrification and fixed-nitrogen removal in sediments from the Lower St. Lawrence Estuary

Biogeosciences

Volumn 9, Issue 11, 2012, Pages 4309-4321

  Crowe, S A ^a   Canfield, D E ^a   Mucci, A ^b   Sundby, B ^b   Maranger, R ^c  

^a UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^b MCGILL UNIVERSITY   (Canada)

^c UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

AMMONIUM; DENITRIFICATION; HYPOXIA; NITRATE; POLLUTANT REMOVAL; SEDIMENT CORE; SLURRY;

CANADA; QUEBEC [CANADA]; SAINT LAWRENCE ESTUARY;

EID: 84881518781     PISSN: 17264170     EISSN: 17264189     Source Type: Journal    
DOI: 10.5194/bg-9-4309-2012     Document Type: Article

References (64)

1. Anschutz, P., Sundby, B., Lefrancois, L., Luther, G. W., and Mucci, A.: Interactions between metal oxides and species of nitrogen and iodine in bioturbated marine sediments, Geochim. Cosmochim. Ac., 64, 2751-2763, 2000.
2. Boudreau, B. P.: Diagenetic models and their implementation, Springer-Verlag, New York, 414 pp., 1996.
3. Braman, R. S. and Hendrix, S. A.: Nanogram nitrite and nitrate determination in environmental and biological-materials by vanadium( III) reduction with chemi-luminescence detection, Anal. Chem., 61, 2715-2718, 1989. (Pubitemid 20065839)
4. Breitburg, D. L., Hondorp, D. W., Davias, L. A., and Diaz, R. J.: Hypoxia, nitrogen, and fisheries: Integrating effects across local and global landscapes, Ann. Rev. Mar. Sci., 1, 329-349, doi:10.1146/annurev.marine.010908. 163754, 2009.
5. Canfield, D. E., Kristensen, E., and Thamdrup, B.: Aquatic geomicrobiology, in: Advances in marine biology, edited by: Southward, A., Craig, J., Young, P. A. T., Lee, M., and Fuiman, A., Elsevier, San Diego, 640 pp., 2005.
6. Canfield, D. E., Glazer, A. N., and Falkowski, P. G.: The evolution and future of earth's nitrogen cycle, Science, 330, 192-196, doi:10.1126/science. 1186120, 2010.
7. Capone, D. G., Bronk, D. A., Mulholland, M. R., and Carpenter, E. J.: Nitrogen in the marine environment, 2nd Ed., Academic Press, Burlington, 1729 pp., 2008.
8. Clement, J. C., Shrestha, J., Ehrenfeld, J. G., and Jaffe, P. R.: Ammonium oxidation coupled to dissimilatory reduction of iron under anaerobic conditions in wetland soils, Soil Biol. Biochem., 37, 2323-2328, doi:10.1016/j.soilbio.2005.03.027, 2005. (Pubitemid 41757561)
9. Cloern, J. E.: Our evolving conceptual model of the coastal eutrophication problem, Mar. Ecol.-Prog. Ser., 210, 223-253, 2001. (Pubitemid 32164184)
10. Codispoti, L. A., Brandes, J. A., Christensen, J. P., Devol, A. H., Naqvi, S. W. A., Paerl, H. W., and Yoshinari, T.: The oceanic fixed nitrogen and nitrous oxide budgets: Moving targets as we enter the anthropocene?, Scientia Marina, 65, 85-105, 2001. (Pubitemid 33102466)
11. Dalsgaard, T. and Thamdrup, B.: Factors controlling anaerobic ammonium oxidation with nitrite in marine sediments, Appl. Environ. Microbiol., 68, 3802-3808, 2002. (Pubitemid 34836688)
12. Dalsgaard, T., Thamdrup, B., and Canfield, D. E.: Anaerobic ammonium oxidation (anammox) in the marine environment, Res. Microbiol., 156, 457-464, doi:10.1016/j.resmic.2005.01.011, 2005. (Pubitemid 40615411)
13. Dong, L. F., Sobey, M. N., Smith, C. J., Rusmana, I., Phillips, W., Stott, A., Osborn, M., and Nedwell, D. B.: Dissimilatory reduction of nitrate to ammonium, not denitrification or anammox, dominates benthic nitrate reduction in tropical estuaries, Limnol. Oceanogr., 56, 279-291, 2011.
14. Edenborn, H. M., Mucci, A., Belzile, N., Lebel, J., Silverberg, N., and Sundby, B.: A glove box for the fine-scale subsampling of sediment box cores, Sedimentology, 33, 147-150, 1986.
15. Francis, C. A., Beman, J. M., and Kuypers, M. M. M.: New processes and players in the nitrogen cycle: The microbial ecology of anaerobic and archaeal ammonia oxidation, ISME Journal, 1, 19-27, doi:10.1038/ismej.2007.8, 2007. (Pubitemid 46717128)
16. Gilbert, D., Sundby, B., Gobeil, C., Mucci, A., and Tremblay, G. H.: A seventy-two-year record of diminishing deep-water oxygen in the st. Lawrence estuary: The northwest atlantic connection, Limnol. Oceanogr., 50, 1654-1666, 2005. (Pubitemid 41356445)
17. Gilbert, D., Chabot, D., Archambault, P., Rondeau, B., and H́ebert, S.: Appauvrissement en oxyg̀ene dans les eaux profondes du saint-laurent marin: Causes possibles et impacts ́ecologiques, Naturaliste Canadien, 131, 67-75, 2007.
18. Gobeil, C.: Biogeochemistry and chemical contamination in the St. Lawrence estuary, in: Estuaries, edited by: Wangersky, P. J., Springer-Verlag, Berlin Heidelberg, 121-147, 2006.
19. Grasshoff, K., Kremling, K., and Ehrhardt M.: Methods of seawater analysis, 3rd Ed., Wiley-VCH, 1999.
20. Hall, G. H.: Measurement of nitrification rates in lake sediments: comparison of the nitrification inhibitors nitrapyrin and allylthiourea, Microb. Ecol., 10, 25-36, 1984.
21. Hall, P. O. and Aller, R. C.: Rapid, small-volume, flow-injection analysis for P CO2 and NH+ 4 in marine and fresh-waters, Limnol. Oceanogr., 37, 1113-1119, 1992. (Pubitemid 23382725)
22. Hulth, S., Aller, R. C., and Gilbert, F.: Coupled anoxic nitrification manganese reduction in marine sediments, Geochim. Cosmochim. Ac., 63, 49-66, 1999. (Pubitemid 29380951)
23. Jensen, M. M., Kuypers, M. M. M., Lavik, G., and Thamdrup, B.: Rates and regulation of anaerobic ammonium oxidation and denitrification in the Black Sea, Limnol. Oceanogr., 53, 23-36, 2008. (Pubitemid 351186007)
24. Kana, T. M., Dakrangelo, C., Oldham, J. B., Bennett, G. E., and Cornwell, J. C.: Membrane inlet mass spectrometer for rapid high-precision determination of N2, O2, and Ar in environmental water samples, Anal. Chem., 66, 4166-4170, 1994. (Pubitemid 124006359)
25. Katsev, S., Chaillou, G., Sundby, B., and Mucci, A.: Effects of progressive oxygen depletion on sediment diagenesis and fluxes: A model for the Lower St. Lawrence River Estuary, Limnol. Oceanogr., 52, 2555-2568, 2007. (Pubitemid 350205808)
26. Klewicki, J. K. and Morgan, J. J.: Kinetic behavior of Mn(III) complexes of pyrophosphate, EDTA, and citrate, Environ. Sci. Technol., 32, 2916-2922, 1998. (Pubitemid 28475654)
27. Konig, I., Drodt, M., Suess, E., and Trautwein, A. X.: Iron reduction through the tan-green color transition in deep-sea sediments, Geochim. Cosmochim. Ac., 61, 1679-1683, 1997.
28. Kostka, J. E., Luther, G. W., and Nealson, K. H.: Chemical and biological reduction of Mn(III)-pyrophsophate complexes-potential importance of dissolved Mn(III) as an environmental oxidant Geochim. Cosmochim. Ac., 59, 885-894, 1995.
29. Kuypers, M. M. M., Lavik, G., Woebken, D., Schmid, M., Fuchs, B. M., Amann, R., Jorgensen, B. B., and Jetten, M. S. M.: Massive nitrogen loss from the benguela upwelling system through anaerobic ammonium oxidation, P. Natl. Acad. Sci. USA, 102, 6478-6483, doi:10.1073/pnas.0502088102, 2005. (Pubitemid 40617468)
30. Loring, D. H. and Nota, D. J. G.: Occurrence and significance of iron, manganese, and titanium in glacial marine sediments from the Estuary of the St. Lawrence River, J. Fish. Res. Board Can., 25, 2327-2347, 1968.
31. Luther, G. W., Sundby, B., Lewis, B. L., Brendel, P. J., and Silverberg, N.: Interactions of manganese with the nitrogen cycle: Alternative pathways to dinitrogen, Geochim. Cosmochim. Ac., 61, 4043-4052, 1997.
32. Luther, G. W., Brendel, P. J., Lewis, B. L., Sundby, B., Lefrancois, L., Silverberg, N., and Nuzzio, D. B.: Simultaneous measurement of O2, Mn, Fe, I, and S(II) in marine pore waters with a solid-state voltammetric microelectrode, Limnol. Oceanogr., 43, 325-333, 1998. (Pubitemid 28278390)
33. Lyle, M.: The brown-green color transition in marine sediments: A marker of the Fe (III)-Fe(II) redox boundary, Limnol. Oceanogr., 28, 1026-1033, 1983.
34. Madison, A., Tebo, B., and Luther, G. W.: Simultaneous determination of soluble manganese(III), manganese(II) and total manganese in natural (pore) waters, Talanta, 84, 374-381, 2011.
35. Magen, C., Mucci, A., and Sundby, B.: Reduction rates of sedimentary Mn and Fe oxides: An incubation experiment with Arctic Ocean sediments, Aquat. Geochem., 17, 629-643, 2011.
36. Meyer, R. L., Risgaard-Petersen, N., and Allen, D. E.: Correlation between anammox activity and microscale distribution of nitrite in a subtropical mangrove sediment, Appl. Environ. Microbiol., 71, 6142-6149, doi:10.1128/aem.71.10.6142-6149.2005, 2005. (Pubitemid 41456912)
37. Mucci, A., Sundby, B., Gehlen, M., Arakaki, T., Zhong, S., and Silverberg, N.: The fate of carbon in continental shelf sediments of eastern canada: A case study, Deep-Sea Res. Pt. II, 47, 733-760, 2000. (Pubitemid 30063411)
38. Nicholls, J. C. and Trimmer, M.: Widespread occurrence of the anammox reaction in estuarine sediments, Aquat. Microb. Ecol., 55, 105-113, doi:10.3354/ame01285, 2009.
39. Nielsen, L. P., Risgaard-Petersen, N., Fossing, H., Christensen, P. B., and Sayama, M.: Electric currents couple spatially separated biogeochemical processes in marine sediment, Nature, 463, 1071-1074, doi:10.1038/nature08790, 2010.
40. Nota, D. J. G. and Loring, D. H.: Recent depositional conditions in the St. Lawrence River and Gulf-a reconnaissance survey, Mar. Geol., 2, 198-235, doi:10.1016/0025-3227(64)90040-4, 1964.
41. Park, W., Nam, Y. K., Lee, M. J., and Kim, T. H.: Anaerobic ammonia-oxidation coupled with Fe3+ reduction by an anaerobic culture from a piggery wastewater acclimated to NH+ 4/Fe3+ medium, Biotechnol. Bioproc. E., 14, 680-685, doi:10.1007/s12257-009-0026-y, 2009.
42. Poulton, S. W. and Canfield, D. E.: Development of a sequential extraction procedure for iron: Implications for iron partitioning in continentally derived particulates, Chem. Geol., 214, 209-221, 2005. (Pubitemid 40140813)
43. Reeburgh, W. S.: An improved interstitial water sampler, Limnol. Oceanogr., 12, 163-165, 1967.
44. Rich, J. J., Dale, O. R., Song, B., and Ward, B. B.: Anaerobic ammonium oxidation (anammox) in chesapeake bay sediments, Microb. Ecol., 55, 311-320, doi:10.1007/s00248-007-9277-3, 2008. (Pubitemid 351171471)
45. Risgaard-Petersen, N., Nielsen, L. P., Rysgaard, S., Dalsgaard, T., and Meyer, R. L.: Application of the isotope pairing technique in sediments where anammox and denitrification coexist, Limnol. Oceanogr. Meth., 1, 63-73, 2003.
46. Risgaard-Petersen, N., Meyer, R. L., and Revsbech, N. P.: Denitrification and anaerobic ammonium oxidation in sediments: Effects of microphytobenthos and NO? 3 , Aquat. Microb. Ecol., 40, 67-76, 2005. (Pubitemid 41128846)
47. Rysgaard, S. and Risgaard-Petersen, N.: A sensitive method for determining nitrogen-15 isotope in urea, Mar. Biol., 128, 1493-1502, 1997.
48. Rysgaard, S., Glud, R. N., Risgaard-Petersen, N., and Dalsgaard, T.: Denitrification and anammox activity in arctic marine sediments, Limnol. Oceanogr., 49, 1493-1502, 2004. (Pubitemid 39320744)
49. Saucier, F. J., Roy, F., Gilbert, D., Pellerin, P., and Ritchie, H.: Modeling the formation and circulation processes of water masses and sea ice in the Gulf of St. Lawrence, Canada, J. Geophys. Res.-Oceans, 108, 3269, doi:10.1029/2000JC000686, 2003.
50. Schrum, H. N., Spivack, A. J., Kastner, M., and D'Hondt, S.: Sulfate-reducing ammonium oxidation: A thermodynamically feasible metabolic pathway in subseafloor sediment, Geology, 37, 939-942, doi:10.1130/g30238a.1, 2009.
51. Shaw, J., Gareau, P., and Courtney, R. C.: Palaeogeography of Atlantic Canada 13-0 kyr, Quaternary Sci. Rev., 21, 1861-1878, doi:10.1016/s0277-3791(02) 00004-5, 2002.
52. Shrestha, J., Rich, J. J., Ehrenfeld, J. G., and Jaffe, P. R.: Oxidation of ammonium to nitrite under iron-reducing conditions in wetland soils laboratory, field demonstrations, and push-pull rate determination, Soil Sci., 174, 156-164, doi:10.1097/SS.0b013e3181988fbf, 2009.
53. Thamdrup, B. and Dalsgaard, T.: The fate of ammonium in anoxic manganese oxide-rich marine sediment, Geochim. Cosmochim. Ac., 64, 4157-4164, 2000. (Pubitemid 32169479)
54. Thamdrup, B. and Dalsgaard, T.: Production of N2 through anaerobic ammonium oxidation coupled to nitrate reduction in marine sediments, Appl. Environ. Microbiol., 68, 1312-1318, 2002. (Pubitemid 34205371)
55. Thamdrup, B. and Dalsgaard, T.: Nitrogen cycling in sediments, in: Microbial ecology of the oceans, 2nd Ed., edited by: Kirchman, D. L., John Wiley & Sons Inc., 2008.
56. Thibodeau, B., de Vernal, A., and Mucci, A.: Enhanced primary productivity, organic carbon fluxes and the development of hy-poxic bottom waters in the Lower St. Lawrence Estuary, Eastern Canada: Micropaleontological and geochemical evidence, Mar. Geol., 231, 37-50, 2006.
57. Thibodeau, B., Lehmann, M. F., Kowarzyk, J., Mucci, A., Gelinas, Y., Gilbert, D., Maranger, R., and Alkhati, M.: Benthic nutrient fluxes along the Laurentian channel: Impacts on the N budget of the St. Lawrence marine system, Estuar. Coast. Shelf Sci., 90, 195-205, doi:10.1016/j.ecss.2010.08.015, 2010.
58. Trimmer, M. and Nicholls, J. C.: Production of nitrogen gas via anammox and denitrification in intact sediment cores along a continental shelf to slope transect in the North Atlantic, Limnol. Oceanogr., 54, 577-589, 2009.
59. Trimmer, M., Nicholls, J. C., and Deflandre, B.: Anaerobic ammonium oxidation measured in sediments along the thames estuary, United Kingdom, Appl. Environ. Microbiol., 69, 6447-6454, doi:10.1128/aem.69.11.6447-6454.2003, 2003. (Pubitemid 37420176)
60. Trimmer, M., Nicholls, J. C., Morley, N., Davies, C. A., and Aldridge, J.: Biphasic behavior of anammox regulated by nitrite and nitrate in an estuarine sediment, Appl. Environ. Microbiol., 71, 1923-1930, doi:10.1128/aem.71.4.1923-1930.2005, 2005. (Pubitemid 40546113)
61. Trimmer, M., Risgaard-Petersen, N., Nicholls, J. C., and Engstrom, P.: Direct measurement of anaerobic ammonium oxidation (anammox) and denitrification in intact sediment cores, Mar. Ecol.-Prog. Ser., 326, 37-47, 2006. (Pubitemid 46026123)
62. Trouwborst, R. E., Clement, B. G., Tebo, B. M., Glazer, B. T., and Luther, G. W.: Soluble Mn(III) in suboxic zones, Science, 313, 1955-1957, 2006. (Pubitemid 44498001)
63. Wang, F. H., Juniper, S. K., Pelegri, S. P., and Macko, S. A.: Denitrification in sediments of the Laurentian trough, St. Lawrence Estuary, Quebec, Canada, Estuar. Coast. Shelf Sci., 57, 515-522, doi:10.1016/s0272- 7714(02)00396-7, 2003. (Pubitemid 36922244)
64. Zumft, W. G.: Cell biology and molecular basis of denitrification, Microbiol. Mol. Biol. R., 61, 533-616, 1997. (Pubitemid 28006959)