, Volume 126, Issue 1–2, pp 131–152 | Cite as

Oxygenation of an anoxic fjord basin strongly stimulates benthic denitrification and DNRA

  • Loreto De BrabandereEmail author
  • Stefano Bonaglia
  • Mikhail Y. Kononets
  • Lena Viktorsson
  • Anders Stigebrandt
  • Bo Thamdrup
  • Per O. J. Hall


Hypoxia hampers eutrophication reduction efforts by enabling high nutrient fluxes from sediment to bottom waters. Oxygenation of hypoxic water bodies is often proposed to reduce benthic ammonium and phosphate release. This study investigates the functional response of benthic nitrate-reducing processes to a long-term engineered oxygenation effort in a density-stratified fjord with euxinic bottom waters. Oxygenation was achieved by mixing surface water with deep, euxinic water, which increased oxygen and nitrate concentrations in the deep water column. The presence of nitrate instigated benthic nitrate reduction in the newly oxidized sediments by equally stimulating denitrification and dissimilatory nitrate reduction to ammonium (DNRA). DNRA and total nitrate reduction rates, as well as the contribution of DNRA to total nitrate reduction, decreased with increasing exposure time of the sediments to oxygen. The relative importance of DNRA as a nitrate sink was correlated to nitrate concentrations, with more nitrate being reduced to ammonium at higher bottom water nitrate concentrations. Overall, engineered oxygenation decreased the net efflux of dissolved inorganic nitrogen from the sediments by stimulating net nitrate removal through denitrification.


Dissimilatory nitrate reduction Denitrification DNRA Anammox Engineered oxygenation Hypoxia By Fjord 



We thank Anders Sjösten (Department of Ecology, Environment and Plant Sciences, Stockholm University) and Lars Ljungqvist (Sven Lovén Centre for Marine Sciences, University of Gothenburg) for nutrient analyses; Dariia Atamanchuk and Madeleine Nilsson for help during cruises; and the crew of the R/V Skagerak (University of Gothenburg) for technical and logistic assistance at sea. Constructive criticism from three anonymous reviewers helped us improve the submitted manuscript. Financial support for this study came from the Swedish Environmental Protection Agency (NV 08/307 F-255-08) through the project BOX (A pilot study to evaluate effects of possible Baltic deep water OXygenation), the Agouron Institute, and the Danish National Research Foundation (DNRF53).


This study was funded by the Swedish Environmental Protection Agency (Grant Number NV 08/307 F-255-08).

Compliance with ethical standards

Statement of human and animal rights

This research did not involve human participants or animals.

Supplementary material

10533_2015_148_MOESM1_ESM.docx (2.9 mb)
Supplementary material 1 (docx 2957 kb)


  1. Behrendt A, de Beer D, Stief P (2013) Vertical activity distribution of dissimilatory nitrate reduction in coastal marine sediments. Biogeosciences 10:7509–7523CrossRefGoogle Scholar
  2. Beutel MW (2006) Inhibition of ammonia release from anoxic profundal sediments in lakes using hypolimnetic oxygenation. Ecol Eng 28:271–279CrossRefGoogle Scholar
  3. Binnerup SJ, Jensen K, Revsbech NP, Jensen MH, Sorensen J (1992) Denitrification, dissimilatory reduction of nitrate to ammonium, and nitrification in a bioturbated estuarine sediment as measured with 15N and microsensor techniques. Appl Environ Microb 58:303–313Google Scholar
  4. Bonaglia S, Bartoli M, Gunnarsson JS, Rahm L, Raymond C, Svensson O, Shakeri Yekta S, Bruchert V (2013) Effect of reoxygenation and Marenzelleria spp. bioturbation on Baltic Sea sediment metabolism. Mar Ecol Prog Ser 482:43–55CrossRefGoogle Scholar
  5. Bonaglia S, Deutsch B, Bartoli M, Marchant HK, Bruchert V (2014a) Seasonal oxygen, nitrogen and phosphorus benthic cycling along an impacted Baltic Sea estuary: regulation and spatial patterns. Biogeochemistry 119:139–160CrossRefGoogle Scholar
  6. Bonaglia S, Nascimento FJA, Bartoli M, Klawonn I, Bruchert V (2014b) Meiofauna increases bacterial denitrification in marine sediments. Nat Commun 5:5133. doi: 10.1038/ncomms6133 CrossRefGoogle Scholar
  7. Bouldin DR (1968) Models for describing the diffusion of oxygen and other mobile constituents across the mud-water interface. J Ecol 56:77–87CrossRefGoogle Scholar
  8. Brunnegård J, Grandel S, Ståhl H, Tengberg A, Hall POJ (2004) Nitrogen cycling in deep-sea sediments of the Porcupine Abyssal Plain, NE Atlantic. Prog Oceanogr 63:159–181CrossRefGoogle Scholar
  9. Cai WJ, Sayles FL (1996) Oxygen penetration depths and fluxes in marine sediments. Mar Chem 52:123–131CrossRefGoogle Scholar
  10. Carpenter SR (2005) Eutrophication of aquatic ecosystems: bistability and soil phosphorus. P Natl Acad Sci USA 102:10002–10005CrossRefGoogle Scholar
  11. Christensen PB, Nielsen LP, Sørensen J, Revsbech NP (1990) Denitrification in nitrate-rich streams—diurnal and seasonal-variation related to benthic oxygen-metabolism. Limnol Oceanogr 35:640–651CrossRefGoogle Scholar
  12. Christensen PB, Rysgaard S, Sloth NP, Dalsgaard T, Schwaerter S (2000) Sediment mineralization, nutrient fluxes, denitrification and dissimilatory nitrate reduction to ammonium in an estuarine fjord with sea cage trout farms. Aquat Microb Ecol 21:73–84CrossRefGoogle Scholar
  13. Conley DJ, Humborg C, Rahm L, Savchuk OP, Wulff F (2002) Hypoxia in the Baltic Sea and basin-scale changes in phosphorus biogeochemistry. Environ Sci Technol 36:5315–5320CrossRefGoogle Scholar
  14. Dale AW, Sommer S, Bohlen L, Treude T, Bertics VJ, Bange HW, Pfannkuche O, Schorp T, Mattsdotter M, Wallmann K (2011) Rates and regulation of nitrogen cycling in seasonally hypoxic sediments during winter (Boknis Eck, SW Baltic Sea): sensitivity to environmental variables. Estuar Coast Shelf S 95:14–28CrossRefGoogle Scholar
  15. Dalsgaard T, Thamdrup B, Canfield DE (2005) Anaerobic ammonium oxidation (anammox) in the marine environment. Res Microbiol 156:457–464CrossRefGoogle Scholar
  16. Dong LF, Sobey MN, Smith CJ, Rusmana I, Phillips W, Stott A, Osborn AM, Nedwell DB (2011) Dissimilatory reduction of nitrate to ammonium, not denitrification or anammox, dominates benthic nitrate reduction in tropical estuaries. Limnol Oceanogr 56:279–291CrossRefGoogle Scholar
  17. Fennel K, Brady D, DiToro D, Fulweiler RW, Gardner WS, Giblin A, McCarthy MJ, Rao A, Seitzinger S, Thouvenot-Korppoo M, Tobias C (2009) Modeling denitrification in aquatic sediments. Millbrook, NY, pp 159–178Google Scholar
  18. Friedrich J, Janssen F, Aleynik D et al (2014) Investigating hypoxia in aquatic environments: diverse approaches to addressing a complex phenomenon. Biogeosciences 11(4):1215–1259CrossRefGoogle Scholar
  19. Giblin AE, Tobias CR, Song B, Weston N, Banta GT, Rivera-Monroy VH (2013) The importance of dissimilatory nitrate reduction to ammonium (DNRA) in the nitrogen cycle of coastal ecosystems. Oceanography 26:124–131CrossRefGoogle Scholar
  20. Gran V, Pitkanen H (1999) Denitrification in estuarine sediments in the eastern Gulf of Finland, Baltic Sea. Hydrobiologia 393:107–115CrossRefGoogle Scholar
  21. Hall POJ, Holby O, Kollberg S, Samuelsson M-O (1992) Chemical fluxes and mass balances in a marine fish cage farm. IV. Nitrogen. Mar Ecol Prog Ser 89:81–91CrossRefGoogle Scholar
  22. Hansen JI, Henriksen K, Blackburn TH (1981) Seasonal distribution of nitrifying bacteria and rates of nitrification in coastal marine sediments. Microb Ecol 7:297–304CrossRefGoogle Scholar
  23. Hansen JW, Thamdrup B, Jørgensen BB (2000) Anoxic incubation of sediment in gas-tight plastic bags: a method for biogeochemical process studies. Mar Ecol Prog Ser 208:273–282CrossRefGoogle Scholar
  24. Hansson D, Stigebrandt A, Liljebladh B (2013) Modelling the Orust fjord system on the Swedish west coast. J Marine Sys 113:29–41CrossRefGoogle Scholar
  25. Hietanen S, Lukkari K (2007) Effects of short-term anoxia on benthic denitrification, nutrient fluxes and phosphorus forms in coastal Baltic sediment. Aquat Microb Ecol 49:293–302CrossRefGoogle Scholar
  26. Høgslund S, Revsbech NP, Cedhagen T, Nielsen LP, Gallardo VA (2008) Denitrification, nitrate turnover, and aerobic respiration by benthic foraminiferans in the oxygen minimum zone off Chile. J Exp Mar Biol Ecol 359:85–91CrossRefGoogle Scholar
  27. Høgslund S, Nielsen JL, Nielsen LP (2010) Distribution, ecology and molecular identification of Thioploca from Danish brackish water sediments. FEMS Microbiol Ecol 73:110–120Google Scholar
  28. Jørgensen KS (1989) Annual pattern of denitrification and nitrate ammonification in estuarine sediment. Appl Environ Microb 55:1841–1847Google Scholar
  29. Joye SB, Hollibaugh JT (1995) Influence of sulfide inhibition of nitrification on nitrogen regeneration in sediments. Science 270:623–625CrossRefGoogle Scholar
  30. Kemp WM, Boynton WR, Adolf JE et al (2005) Eutrophication of Chesapeake Bay: historical trends and ecological interactions. Mar Ecol Prog Ser 303:1–29CrossRefGoogle Scholar
  31. Kemp WM, Testa JM, Conley DJ, Gilbert D, Hagy JD (2009) Temporal responses of coastal hypoxia to nutrient loading and physical controls. Biogeosciences 6:2985–3008CrossRefGoogle Scholar
  32. Koroleff F (1983) Methods of seawater analysis. Verlag Chemie, WeinheimGoogle Scholar
  33. Laima MCJ (1994) Is KCl a reliable extractant of (NH4 +)-15N added to coastal marine sediments. Biogeochemistry 27:83–95CrossRefGoogle Scholar
  34. Lam P, Lavik G, Jensen MM, van de Vossenberg J, Schmid M, Woebken D, Dimitri G, Amann R, Jetten MSM, Kuypers MMM (2009) Revising the nitrogen cycle in the Peruvian oxygen minimum zone. P Natl Acad Sci USA 106:4752–4757CrossRefGoogle Scholar
  35. Laverman AM, Canavan RW, Slomp CP, Van Cappellen P (2007) Potential nitrate removal in a coastal freshwater sediment (Haringvliet Lake, the Netherlands) and response to salinization. Water Res 41:3061–3068CrossRefGoogle Scholar
  36. Lehman JT (2011) Nuisance cyanobacteria in an urbanized impoundment: interacting internal phosphorus loading, nitrogen metabolism, and polymixis. Hydrobiologia 661:277–287CrossRefGoogle Scholar
  37. Malkin SY, Rao AMF, Seitaj D, Vasquez-Cardenas D, Zetsche E-M, Hidalgo-Martinez S, Boschker HTS, Meysman FJR (2014) Natural occurrence of microbial sulphur oxidation by long-range electron transport in the seafloor. ISME J 8:2551–2552CrossRefGoogle Scholar
  38. Marzocchi U, Trojan D, Larsen S, Meyer RL, Revsbech NP, Schramm A, Nielsen LP, Risgaard-Petersen N (2014) Electric coupling between distant nitrate reduction and sulfide oxidation in marine sediment. ISME J 8:1682–1690CrossRefGoogle Scholar
  39. Matzinger A, Mueller B, Niederhauser P, Schmid M, Wueest A (2010) Hypolimnetic oxygen consumption by sediment-based reduced substances in former eutrophic lakes. Limnol Oceanogr 55:2073–2084CrossRefGoogle Scholar
  40. McHatton SC, Barry JP, Jannasch HW, Nelson DC (1996) High nitrate concentrations in vacuolate, autotrophic marine Beggiatoa spp. Appl Environ Microb 62:954–958Google Scholar
  41. Mengis M, Gachter R, Wehrli B, Bernasconi S (1997) Nitrogen elimination in two deep eutrophic lakes. Limnol Oceanogr 42:1530–1543CrossRefGoogle Scholar
  42. Neubacher EC, Parker RE, Trimmer M (2013) The potential effect of sustained hypoxia on nitrogen cycling in sediment from the southern North Sea: a mesocosm experiment. Biogeochemistry 113:69–84CrossRefGoogle Scholar
  43. Nielsen LP (1992) Denitrification in sediment determined from nitrogen isotope pairing. FEMS Microbiol Ecol 86:357–362CrossRefGoogle Scholar
  44. Nogaro G, Burgin AJ (2014) Influence of bioturbation on denitrification and dissimilatory nitrate reduction to ammonium (DNRA) in freshwater sediments. Biogeochemistry 120:279–294CrossRefGoogle Scholar
  45. Ogilvie BG, Rutter M, Nedwell DB (1997) Selection by temperature of nitrate-reducing bacteria from estuarine sediments: species composition and competition for nitrate. FEMS Microbiol Ecol 23:11–22CrossRefGoogle Scholar
  46. Piña-Ochoa E, Hogslund S, Geslin E, Cedhagen T, Revsbech NP, Nielsen LP, Schweizer M, Jorissen F, Rysgaard S, Risgaard-Petersen N (2010) Widespread occurrence of nitrate storage and denitrification among Foraminifera and Gromiida. P Natl Acad Sci USA 107:1148–1153CrossRefGoogle Scholar
  47. Preisler A, de Beer D, Lichtschlag A, Lavik G, Boetius A, Jørgensen BB (2007) Biological and chemical sulfide oxidation in a Beggiatoa inhabited marine sediment. ISME J 1:341–353Google Scholar
  48. Prokopenko MG, Hirst MB, De Brabandere L, Berelson WM, Lawrence DJ, Granger J, Chang BX, Dawson S, Crane EJ, Chong L, Thamdrup B, Sigman DM (2013) Nitrogen losses in anoxic marine sediments driven by Thioploca–anammox bacterial consortia. Nature 500:194–200CrossRefGoogle Scholar
  49. Revsbech NP, Jacobsen JP, Nielsen LP (2005) Nitrogen transformations in microenvironments of river beds and riparian zones. Ecol Eng 24:447–455CrossRefGoogle Scholar
  50. Risgaard-Petersen N, Langezaal AM, Ingvardsen S, Schmid MC, Jetten MSM, Op den Camp HJM, Derksen JWM, Piña-Ochoa E, Eriksson SP, Nielsen LP, Revsbech NP, Cedhagen T, van der Zwaan GJ (2006) Evidence for complete denitrification in a benthic foraminifer. Nature 443:93–96CrossRefGoogle Scholar
  51. Risgaard-Petersen N, Nielsen LP, Rysgaard S, Dalsgaard T, Meyer RL (2003) Application of the isotope pairing technique in sediments where anammox and denitrification coexist. Limnol Oceanogr Methods 1:63–73CrossRefGoogle Scholar
  52. Risgaard-Petersen N, Rysgaard S, Nielsen LP, Revsbech NP (1994) Diurnal-variation of denitrification and nitrification in sediments colonized by benthic microphytes. Limnol Oceanogr 39:573–579CrossRefGoogle Scholar
  53. Risgaard-Petersen N, Damgaard LR, Revil A, Nielsen LP (2014) Mapping electron sources and sinks in a marine biogeobattery. J Geophys Res-Biogeo 119:1475–1486CrossRefGoogle Scholar
  54. Roberts KL, Eate VM, Eyre BD, Holland DP, Cook PLM (2012) Hypoxic events stimulate nitrogen recycling in a shallow salt-wedge estuary: the Yarra River estuary, Australia. Limnol Oceanogr 57:1427–1442CrossRefGoogle Scholar
  55. Roberts KL, Kessler AJ, Grace MR, Cook PLM (2014) Increased rates of dissimilatory nitrate reduction to ammonium (DNRA) under oxic conditions in a periodically hypoxic estuary. Geochim Cosmochim Ac 133:313–324CrossRefGoogle Scholar
  56. Rysgaard S, Risgaard-Petersen N, Sloth NP (1996) Nitrification, denitrification, and nitrate ammonification in sediments of two coastal lagoons in Southern France. Hydrobiologia 329:133–141CrossRefGoogle Scholar
  57. Rysgaard S, Risgaard-Petersen N, Sloth NP, Jensen K, Nielsen LP (1994) Oxygen regulation of nitrification and denitrification in sediments. Limnol Oceanogr 39:1643–1652CrossRefGoogle Scholar
  58. Sayama M, Risgaard-Petersen N, Nielsen LP, Fossing H, Christensen PB (2005) Impact of bacterial NO3- transport on sediment biogeochemistry. Appl Environ Microb 71:7575–7577CrossRefGoogle Scholar
  59. Silvennoinen H, Liikanen A, Torssonen J, Stange CF, Martikainen PJ (2008) Denitrification and N2O effluxes in the Bothnian Bay (northern Baltic Sea) river sediments as affected by temperature under different oxygen concentrations. Biogeochemistry 88:63–72CrossRefGoogle Scholar
  60. Song GD, Liu SM, Marchant H, Kuypers MMM, Lavik G (2013) Anammox, denitrification and dissimilatory nitrate reduction to ammonium in the East China Sea sediment. Biogeosciences 10:6851–6864CrossRefGoogle Scholar
  61. Ståhl H, Tengberg A, Brunnegard J, Hall POJ (2004) Recycling and burial of organic carbon in sediments of the Porcupine Abyssal Plain, NE Atlantic. Deep-Sea Res Pt I 51:777–791CrossRefGoogle Scholar
  62. Stigebrandt A, Gustafsson BG (2007) Improvement of Baltic proper water quality using large-scale ecological engineering. Ambio 36:280–286CrossRefGoogle Scholar
  63. Stigebrandt A, Rahm L, Viktorsson L, Ödalen M, Hall POJ, Liljebladh B (2014) A new phosphorus paradigm for the Baltic proper. Ambio 43:634–643CrossRefGoogle Scholar
  64. Stigebrandt A, Liljebladh B, De Brabandere L, Forth M, Granmo Å, Hall POJ, Hammar J, Hansson D, Kononets M, Magnusson M, Norén F, Rahm L, Treusch AH, Viktorsson L (2015) An experiment with forced oxygenation of the deepwater of the anoxic By Fjord, Western Sweden. Ambio 44:42–54CrossRefGoogle Scholar
  65. Tengberg A, Ståhl H, Gust G, Muller V, Arning U, Andersson H, Hall POJ (2004) Intercalibration of benthic flux chambers I. Accuracy of flux measurements and influence of chamber hydrodynamics. Prog Oceanogr 60:1–28CrossRefGoogle Scholar
  66. Thamdrup B (2012) New pathways and processes in the global nitrogen cycle. Annu Rev Ecol Evol Syst 43:407–428CrossRefGoogle Scholar
  67. Thamdrup B, Dalsgaard T (2002) Production of N2 through anaerobic ammonium oxidation coupled to nitrate reduction in marine sediments. Appl Environ Microb 68:1312–1318CrossRefGoogle Scholar
  68. Thamdrup B, Fleischer S (1998) Temperature dependence of oxygen respiration, nitrogen mineralization, and nitrification in Arctic sediments. Aquat Microb Ecol 15:191–199CrossRefGoogle Scholar
  69. Tiedje JM, Sexstone AJ, Myrold DD, Robinson JA (1982) Denitrification—Ecological niches, competition and survival. Antonie Van Leeuw J Microb 48:569–583CrossRefGoogle Scholar
  70. Trimmer M, Engström P (2011) Distribution, activity, and ecology of anammox bacteria in aquatic environments. In: Ward BB, Arp DJ, Klotz MG (eds) Nitrification. Nitrification ASM Press, Washington, DC, pp 201–235CrossRefGoogle Scholar
  71. Trimmer M, Nicholls JC (2009) 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 54:577–589CrossRefGoogle Scholar
  72. Trimmer M, Risgaard-Petersen N, Nicholls JC, Engström P (2006) Direct measurement of anaerobic ammonium oxidation (anammox) and denitrification in intact sediment cores. Mar Ecol Prog Ser 326:37–47CrossRefGoogle Scholar
  73. Van Luijn F, Boers PCM, Lijklema L (1996) Comparison of denitrification rates in lake sediments obtained by the N2 flux method, the 15N isotope pairing technique and the mass balance approach. Water Res 30:893–900CrossRefGoogle Scholar
  74. Viktorsson L, Almroth Rosell E, Tengberg A, Vankevich R, Neelov I, Isaev A, Kravtsov V, Hall POJ (2012) Benthic phosphorus dynamics in the Gulf of Finland, Baltic Sea. Aquat Geochem 18:543–564CrossRefGoogle Scholar
  75. Viktorsson L, Kononets M, Roos P, Hall POJ (2013) Recycling and burial of phosphorus in sediments of an anoxic fjord-the By Fjord, western Sweden. J Mar Res 71:351–374CrossRefGoogle Scholar
  76. Zilius M, Bartoli M, Bresciani M, Katarzyte M, Ruginis T, Petkuviene J, Lubiene I, Giardino C, Bukaveckas PA, de Wit R, Razinkovas-Baziukas A (2014) Feedback mechanisms between cyanobacterial blooms, transient hypoxia, and benthic phosphorus regeneration in shallow coastal environments. Estuar Coast 37:680–694CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  • Loreto De Brabandere
    • 1
    • 2
    Email author
  • Stefano Bonaglia
    • 3
  • Mikhail Y. Kononets
    • 4
  • Lena Viktorsson
    • 5
    • 6
  • Anders Stigebrandt
    • 5
  • Bo Thamdrup
    • 2
  • Per O. J. Hall
    • 4
  1. 1.Analytical and Environmental Geo-ChemistryVrije Universiteit BrusselBrusselsBelgium
  2. 2.Nordic Center for Earth Evolution, Department of BiologyUniversity of Southern DenmarkOdenseDenmark
  3. 3.Department of Geological SciencesStockholm UniversityStockholmSweden
  4. 4.Department of Marine SciencesUniversity of GothenburgGothenburgSweden
  5. 5.Department of Marine SciencesUniversity of GothenburgGothenburgSweden
  6. 6.Baltic Sea CentreStockholm UniversityStockholmSweden

Personalised recommendations