Alternative pathways for removal of nitrogen from the sea. Nils Risgaard-Petersen, National Environmental Research Institute, Denmark
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1 Alternative pathways for removal of nitrogen from the sea Nils RisgaardPetersen, National Environmental Research Institute, Denmark
2 NH 4 NH 4 NO 2 NO 3 NO 2 N 2 O N 2
3 NH 4 NH 4 NO 2 NO 3 NO 2 N 2 O N 2
4 The classical benthic nitrogen cycle Oxic NH 4 Ammonia oxidation NO 3 Nitrite oxidation Anoxic Org C Nitrate reduction DNRA Denitrification NH 4 N 2 Anammox
5 The Anammox process: NH 4 >N 2 2 H 2 Historic: Process suggested :Hamm & Thomoson 1941 NH 4 deficit in oxygen minimum zones anaerobic oxidation of NH4: Richards 1965 Disappearance of NH 4 from fluidized bed reactor: Mulder 1995 Reaction identified in wastewater sluged: Van de Graff 1997 Bacteria responsible for the reaction identified: Schmid 2 First direct evidence for existence of the process in marine sediments: Thamdrup and Dalsgaard 22.
6 Experimental evidence for anammox: Incubations of sediment slurries with 15 Nisotopes NH 4 29 N 2 RF1 3 N 2 Nothing happens! nmol cm NH 4 14 NO NH 4 15 NO Time (hours) 15 NH N 2 2*H 2 (anammox) 15 NH N 2 (anammox) 15 NO 3 15 NO 3 3 N 2 (denitrification) Data from Randers Fjord, DK
7 Anammox is ubiquitous in the marine environment
8 Depth (mm) 5 1 NO 3 NH In sediments Anammox occurs below the oxic/anoxic interface NO NH 4 Randers Fjord
9 Which processes are responsible for the supply of to the ANAMMOX reaction? Oxic NH 4 Ammonia oxidation Nitrite oxidation NO 3 Anoxic ANAMMOX NH 4 Nitrate reduction Org C Denitrification N 2 N 2 Anammox
10 Inference of process rates from microprofiles Depth (mm) NO 3 NO calculation of Nitrate profile Depth (mm) NO 3 7 NO NO 3 modeling Depth(mm) Oxic Anoxic NO 3 7 NO Production (nmol NO x cm 2 s 1 ) NO 3 NO 3 1 Depth (mm) Ammonia oxidation Nitrite reduction Nitrite oxidation Nitrate reduction Rate (nmol cm 3 s 1 ) Meyer et al 25
11 The principal Nitrite source for anammox is Anaerobic Nitrate Reduction Example from Logan River Australia. Units: nmol cm 2 h 1 Oxic NH NO 3 Ammonia oxidation Nitrite oxidation Anoxic ANAMMOX NH Nitrate reduction Org C Denitrification N 2 N 2 Anammox
12 Anammox Station Depth (mm) NO RF NO 3 Depth (mm) NO anammox station NO 3 9 Light NO 3 Depth (mm) NO RF7 Dark May NO 3 Deep profiles of NOx NO2 present in anoxic zone most of the year Relative low Denitrification capacity Relative low O2 consumption Relative low Cmineralization Shallow profiles of NOx Relative High Denitrification capacity Relative High O2 consumption Relative High Cmineralization Ho: High Org C load favours hetrotropic denitrification on the expense of Anammox.
13 The contribution of anammox to benthic N 2 production decreases with increasing sediment reactivity, because heterotrophic denitrifies do better in sediments with high organic loadings. 8 Y = 33.95X.6235 R 2 =.954 (%) Anammox N 2 production NH 4 mineralisation (µm h 1 ) Data from Engström et al. 25
14 The contribution of anammox to benthic N removal increases with water depth A/(AD)% 7 m, Skagerrak, S4 695 m, Skagerrak S9 38 m, Skagerrak S6 116 m, Gullmarsfjorden, S3 1 m, Disko_B 9 m, Skagerrak S5 85 m, Dnb_C 75 m, Gullmarsfjorden, S1 5 m, Disko_C 5 m, Disko_A 4 m, Ile_A 4 m, Dmh_A 4 m, Hay_A 4 m, Ella_A 4 m, Sc_A 39 m, Moni Bay st. 1, Limassol, Cyprus 36 m, Dnb_Ab 36 m, Dnb_Aa 34 m, Long Island Sound, SD 28 m, El Campello st. 6 Alicante Spain 28 m, El Campello st. 2 Alicante Spain 27 m, Brofjorden, S2 2 m, Suonio st. 2, Greece 2 m, Suonio st. 1, Greece 16 m, Aarhus Bay 16 m, Long Island Sound, SP.5 m, Norsminde Fjord.5 m, Randers Fjord, Mellerup.5 m, Randers Fjord, Mellerup.5 m, Randers Fjord, Mellerup m, Grain 6 m, Southend 5 m, Allhallows 4 m, Gravesend 3 m, Grays 2 m, Crossness 1 Dalsgaard et al 25 The average depth of the ocean is 38 m. Anammox might be the dominant process for removal of N
15 The updated benthic nitrogen cycle Oxic NH 4 Ammonia oxidation Nitrite oxidation NO 3 Anoxic NH 4 Org C Nitrate reduction ANAMMOX DNRA Denitrification N 2 NH 4 N 2 Anammox
16 According to the present conceptual view removal of fixed N the oceans is mediated by prokaryotes But is it true?
17 Nitrate in Gullmar Fjord (S) Sediment 1 Water depth: 114 m : 251% sat NH 4 in water <.5 μm NO 3 in water 917 μm Temp: 6 C Salinity 34 psu Depth (mm) Porewater NO NO RisgaardPetersen et al. 26
18 Nitrate in Gullmar Fjord (S) Sediment Depth (mm) Porewater NO 3 "Strange" NO 3 Nitrate is not only present in the porewater. There are cell bound pools in sediments NO RisgaardPetersen et al. 26
19 Nitrate and distribution of foraminifers (Globobulimina pseudospiecens) Indv pr 5 cm Depth (mm) G. pseudospiecens Cell bound nitrate A B O NO 3 (µmol cm 3 2 sediment) Cell bound nitrate correlate with foraminiferal abundance (Pearson, r=.95; p<.1) RisgaardPetersen et al. 26
20 Nitrate in live and dead foraminifers (Globobulimina pseudospiecens) Concentration Live Dead Depth (mm) NO NO x
21 Nonionella cf. stella and Stainforthia sp from OMZ off Chile 1 µm Maximum NO 3 concentrat ion in porewater 12 Species Intracellular NO 3 content (pmol per individual) Nonionella cf. stella Mean 186 (25, n=43) Range Intracel lular NO 3 concent ration Stainforthia sp. 6 (9, n=26) RisgaardPetersen et al. 26
22 Why do benthic foraminifers accumulate nitrate? 8NO 3 5CH 3 COO 13H 4N 2 1C 14H 2 G=545 kj per mol NO 3
23 Denitrification by foraminifers (Globoubulimina pseudospinences) N 2 N (pmol N per indv.) B Anoxic incubations of foraminifers with a 15 Nlabelled intracellular nitrate pool Days Denitrification rate =565±151 pmol N cell 1 day 1 RisgaardPetersen et al. 26
24 Denitrification by foraminifers (Nonionella cf. Stella) Acetylene block: NO 3 NO N 2 O N 2 Setup N 2 microsensor Microtube (i.d:.5 mm height: 7.5 mm) Nitrate and oxygen free artificial seawater with 1% acetylene (1 kpa) N 2 Foraminifer
25 Denitrification by foraminifers (Nonionella cf. Stella) Distance from forams (mm) 1,,8,6,4,2, a n= b n=3 c n= N 2 O Denirification = DN 2 *dc/dx *surface area =84±33 pmol N cell 1 d 1
26 Who is responsible for denitrification of the intracellular nitrate?? GS2 EUB DAPI Autofluorescence FISH applied on G. pseudospinencens FISH analysis and TEM micrographs shows that endosymbiontic bacteria are absent TEM micrograph of G. pseudospinencens RisgaardPetersen et al. 26
27 This implies that denitrification is performed by the foraminifers Benthic foraminifers forms a hitherto unknown pathway for removal of fixed N from the sea
28 The updated benthic nitrogen cycle Version 2. Oxic NH 4 NO 3 Foramiferal Nitrate uptake Ammonia oxidation Nitrite oxidation Anoxic NH 4 Org C Nitrate reduction migration ANAMMOX DNRA Denitrification N 2 NH 4 N 2 Anammox Foramiferal denitrification
29 Thanks to: Tage Dalsgaard, National Environmental Research Institute (DK) Langezaal, A. M., Utrecht University, (NL) Ingvardsen, S, University of Aarhus, (DK) Schmid, M.C., Radboud University Nijmegen, (NL) Revsbech, N. P., University of Aarhus, (DK) Nielsen, L.P., University of Aarhus, (DK) Andreas Schramm, University of Aarhus, (DK) Mike S.M. Jetten Radboud University Nijmegen, (NL) Huub J.M. Op den Camp Radboud University Nijmegen, (NL) Jan W.M. Derksen Radboud, University Nijmegen, (NL) Elisa PiñaOchoa, Centre of Environmental Sciences, (E) Susanne P. Eriksson, Göteborg University, (S) Tomas Cedhagen,University of Aarhus (DK) Gijsbert J. van der Zwaan, Utrecht University, (NL) Britta Poulsen, University of Aarhus (DK) Preben Sørensen, University of Aarhus (DK) Kitte Gerlich Lauritsen, National Environmental Research Institute (DK) Marlene Venø Skjærbæk, National Environmental Research Institute (DK) Tanja Quotrup, National Environmental Research Institute (DK) The Carlsberg Foundation (DK) The Danish Natural Science Research Council (DK)
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