Skip to main content
SpringerLink
Log in

Nitrogen transformations in stratified aquatic microbial ecosystems

  • Original paper
  • Published:
Antonie van Leeuwenhoek Aims and scope Submit manuscript

Abstract

New analytical methods such as advanced molecular techniques and microsensors have resulted in new insights about how nitrogen transformations in stratified microbial systems such as sediments and biofilms are regulated at a µm–mm scale. A large and ever-expanding knowledge base about nitrogen fixation, nitrification, denitrification, and dissimilatory reduction of nitrate to ammonium, and about the microorganisms performing the processes, has been produced by use of these techniques. During the last decade the discovery of anammmox bacteria and migrating, nitrate accumulating bacteria performing dissimilatory reduction of nitrate to ammonium have given new dimensions to the understanding of nitrogen cycling in nature, and the occurrence of these organisms and processes in stratified microbial communities will be described in detail.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Ahmad A, Barry JP, Nelson DC (1999) Phylogenetic affinity of a wide, vacuolate, nitrate-accumulatlng Beggiatoa sp. from Monterey Canyon, California, with Thioploca spp. Appl. Environ Microbiol 65:270–277

    PubMed  CAS  Google Scholar 

  • Altmann D, Stief P, Amann R, de Beer D, Schramm A (2003) In situ distribution and activity of nitrifying bacteria in freshwater sediment. Environ Microbiol 5:798–803

    PubMed  CAS  Google Scholar 

  • Batchelor SE, Cooper M, Chhabra SR, Glover LA, Stewart GSAB, Williams P, Prosser JI (1997) Cell density-regulated recovery of starved biofilm populations of ammonia-oxidizing bacteria Appl Environ Microbiol 63:2281–2286

    CAS  Google Scholar 

  • Bergman B, Gallon JR, Rai AN, Stal LJ (1997) N2 fixation by non-heterocystous cyanobacteria. FEMS Microbiol Rev 19:139–185

    Article  CAS  Google Scholar 

  • Bernhard AE, Donn T, Giblin AE, Stahl DA (2005) Loss of diversity of ammonia-oxidizing bacteria correlates with increasing salinity in an estuary system. Environ Microbiol 7:1289–1297

    PubMed  CAS  Google Scholar 

  • Binnerup SJ, Jensen K, Revsbech NP, Jensen MH, Sørensen J (1992) Denitrification, dissimilatory reduction of nitrate to ammonium, and nitrification in a bioturbated estuarine sediment as measured with N-15 and microsensor techniques. Appl Environ Microbiol 58:303–313

    PubMed  CAS  Google Scholar 

  • Bock E, Koops H-P (1992) The genus Nitrobacter and related genera. In: Balows A, Trüper HG, Dworkin M, Harder W, Schleifer K-H (eds) The prokaryotes,␣2nd edn. Springer Verlag, New York, pp 2302–2309

    Google Scholar 

  • Bollmann A, Bar-Gilissen MJ, Laanbroek HJ (2002) Growth at low ammonium concentrations and starvation response as potential factors involved in niche differentiation among ammonia-oxidizing bacteria. Appl Environ Microbiol 68:4751–4757

    PubMed  CAS  Google Scholar 

  • Bothe H, Jost G, Schloter M, Ward BB, Witzel KP (2000) Molecular analysis of ammonia oxidation and denitrification in natural environments. FEMS Microbiol Rev 24:673–690

    PubMed  CAS  Google Scholar 

  • Casciotti KL, Ward BB (2001) Dissimilatory nitrite reductase genes from autotrophic ammonia-oxidizing bacteria. Appl Environ Microbiol 67:2213–2221

    CAS  Google Scholar 

  • Casciotti KL, Ward BB (2005) Phylogenetic analysis of nitric oxide reductase gene homologues from aerobic ammonia-oxidizing bacteria. FEMS Microbiol Ecol 52:197–205

    PubMed  CAS  Google Scholar 

  • Christensen PB, Nielsen LP, Revsbech NP, Sørensen J (1989) Microzonation of denitrification activity in stream sediments as studied with a combined oxygen and nitrous oxide microsensor. Appl Environ Microbiol 55:1234–1241

    PubMed  CAS  Google Scholar 

  • 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. Aquat Microb Ecol 21:73–84

    Google Scholar 

  • Church MJ, Short CM, Jenkins BD, Karl DM, Zehr JP (2005) Temporal patterns of nitrogenase gene (nifH) expression in the oligotrophic North Pacific Ocean. Appl Environ Microbiol 71:5362–5370

    PubMed  CAS  Google Scholar 

  • Coci M, Riechmann D, Bodelier PLE, Stefani S, Zwart G, Laanbroek HJ (2005) Effect of salinity on temporal and spatial dynamics of ammonia-oxidising bacteria from intertidal freshwater sediment. FEMS Microbiol Ecol 53:359–368

    PubMed  CAS  Google Scholar 

  • Dalsgaard T, Canfield DE, Petersen J, Thamdrup B, Acuna-Gonzalez J (2003) N-2 production by the anammox reaction in the anoxic water column of Golfo Dulce, Costa Rica. Nature 422:606–608

    PubMed  CAS  Google Scholar 

  • Dalsgaard T, de Zwart J, Robertson LA, Kuenen JG, Revsbech NP (1995) Nitrification, denitrification and␣growth in artificial Thiosphaera pantotropha biofilms as measured with a combined microsensor for oxygen and nitrous oxide. FEMS Microbiol Ecol 17:137–148

    CAS  Google Scholar 

  • Dalsgaard T, Revsbech NP (1992) Regulating factors of denitrification in trickling filter biofilms as measured with the oxygen nitrous-oxide microsensor. FEMS Microbiol Ecol 101:151–164

    CAS  Google Scholar 

  • Dalsgaard T, Thamdrup B, Canfield DE (2005) Anaerobic ammonium oxidation (anammox) in the marine environment. Res Microbiol 156:457–464

    PubMed  CAS  Google Scholar 

  • Engström P, Dalsgaard T, Hulth S, Allerr RC (2005) Anaerobic ammonium oxidation by nitrite (anammox): Implications for N-2 production in coastal marine sediments. Geochim Cosmochim Acta 69:2057–2065

    Google Scholar 

  • Fossing H, Gallardo VA, Jørgensen BB, Hüttel M, Nielsen LP, Schulz H, Canfield DE, Forster S, Glud RN, Gundersen JK, Kuver J, Ramsing NB, Teske A, Thamdrup B, Ulloa O (1995) Concentration and transport of nitrate by the mat-forming sulphur bacterium Thioploca. Nature 374:713–715

    CAS  Google Scholar 

  • Francis CA, Roberts KJ, Beman JM, Santoro AE, Oakley BB (2005) Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean. PNAS 102:14683–14688

    PubMed  CAS  Google Scholar 

  • Galloway JN, Aber JD, Erisman JW, Seitzinger SP, Howarth RW, Cowling EB, Cosby BJ (2003) The nitrogen cascade. BioScience 53:341–356

    Google Scholar 

  • Gieseke A, Purkhold U, Wagner M, Amann R, Schramm A (2001) Community structure and activity dynamics of nitrifying bacteria in a phosphate-removing biofilm. Appl Environ Microbiol 67:1351–1362

    PubMed  CAS  Google Scholar 

  • Gieseke A, Bjerrum L, Wagner M, Amann R (2003) Structure and activity of multiple nitrifying bacterial populations co-existing in a biofilm. Environ Microbiol 5:355–369

    PubMed  CAS  Google Scholar 

  • Gilbert F, Souchu P, Bianchi M, Bonin P (1997) Influence of shellfish farming activities on nitrification, nitrate reduction to ammonium and denitrification at the water-sediment interface of the Thau lagoon, France. Mar Ecol Progr Ser 151:143–153

    CAS  Google Scholar 

  • Groffman PM, Altabet MA, Böhlke JK, Butterbach-Bahl K, David MB, Firestone MK, Giblin AE, Kana TM, Nielsen LP, Voytek MA (in press) Bad solutions to a difficult problem: methods for measuring denitrification. Ecol Appl

  • Guven D, Dapena A, Kartal B, Schmid MC, Maas B, van de Pas-Schoonen K, Sozen S, Mendez R, Op den Camp HJM, Jetten MSM, Strous M, Schmidt I (2005) Propionate oxidation by and methanol inhibition of anaerobic ammonium-oxidizing bacteria. Appl Environ Microbiol 71:1066–1071

    PubMed  Google Scholar 

  • Hamm RE, Thomoson TG (1941) Dissolved nitrogen in the sea water of the Northeast Pacific with notes on the total carbon dioxide and dissolved oxygen. J Mar Res 4:11–27

    CAS  Google Scholar 

  • Hulth S, Aller RC, Canfield DE, Dalsgaard T, Engstrom P, Gilbert F, Sundback K, Thamdrup B (2005) Nitrogen removal in marine environments: recent findings and future research challenges. Mar Chem 94:125–145

    CAS  Google Scholar 

  • Jetten MSM, Strous M, van de Pas-Schoonen KT, Schalk J, van Dongen U, van de Graaf AA, Logemann S, Muyzer G, van Loosdrecht MCM, Kuenen JG (1998) The anaerobic oxidation of ammonium. FEMS Microbiol Rev 22:421–437

    PubMed  CAS  Google Scholar 

  • Jetten MSM, Cirpus I, Kartal B, van Niftrik L, van de Pas-Schoonen KT, Sliekers O, Haaijer S, van der Star W, Schmid M, van de Vossenberg J, Schmidt I, Harhangi H, van Loosdrecht M, Kuenen JG, den Camp HO, Strous M (2005) 1994–2004: 10 years of research on the anaerobic oxidation of ammonium. Biochem Soc Trans 33:119–123

    PubMed  CAS  Google Scholar 

  • Joo HS, Hirai M, Shoda M (2005) Characteristics of ammonium removal by heterotrophic nitrification-aerobic denitrification by Alcaligenes faecalis no. 4. J Biosci Bioeng 100:184–191

    PubMed  CAS  Google Scholar 

  • Jordan FL, Cantera JJL, Fenn ME, Stein LY (2005) Autotrophic ammonia-oxidizing bacteria contribute minimally to nitrification in a nitrogen-impacted forested ecosystem. Appl Environ Microbiol 71:197–206

    PubMed  CAS  Google Scholar 

  • Kanungo PK, Panda D, Adhya TK, Ramakrishnan B, Rao VR (1997) Nitrogenase activity and nitrogen-fixing bacteria associated with rhizosphere of rice cultivars with varying N absorption efficiency. J Sci Food Agric 73:485–488

    CAS  Google Scholar 

  • Karl D, Michaels A, Bergman B, Capone D, Carpenter E, Letelier R, Lipschultz F, Paerl H, Sigman D, Stal L (2002) Dinitrogen fixation in the world’s oceans. Biogeochemistry 57:47–98

    Google Scholar 

  • Kartal B, van der Star W, Jetten M, Picioreanu C, van Loosdrecht M, Strous M (2005) New visions on life style and application of anammox bacteria. J Biotechnol 118:S166-S167

    Google Scholar 

  • Kaspar HF, Hall GH, Holland AJ (1988) Effects of sea cage salmon farming on sediment nitrification and dissimilatory nitrate reductions. Aquaculture 70:333–344

    Google Scholar 

  • Kelly-Gerreyn BA, Trimmer M, Hydes DJA (2001) Diagenetic model discriminating denitrification and dissimilatory nitrate reduction to ammonium in a temperate estuarine sediment. Ecol Progr Ser 220:33–46

    CAS  Google Scholar 

  • Könneke M, Bernhard AE, de la Torre JR, Walker CB, Waterbury JB, Stahl DA (2005) Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 437:543–546

    PubMed  Google Scholar 

  • Koops H-P, Purkhold U, Pommerening-Röser A, Timmermann G, Wagner M (2003) The lithoautotrophic ammonia-oxidizing bacteria. The prokaryotes: an evolving electronic resource for the microbiological community, III edn. Springer

  • Kowalchuk GA, Stephen JR (2001) Ammonia-oxidizing bacteria:a model for molecular microbial ecology. Ann Rev Microbiol 55:485–529

    CAS  Google Scholar 

  • Krug EC, Winstanley D (2002) The need for comprehensive and consistent treatment of the nitrogen cycle in nitrogen cycling and mass balance studies: I Terrestrial nitrogen cycle. Sci Tot Environ 293:1–29

    CAS  Google Scholar 

  • Kuenen JG, Jetten MSM (2001) Extraordinary anaerobic ammonium-oxidizing bacteria. ASM News 67:456–458

    Google Scholar 

  • Kuenen JG, Robertson LA (1994) Combined nitrification-denitrification processes. FEMS Microbiol Rev 15:109–117

    CAS  Google Scholar 

  • Kuypers MMM, Sliekers AO, Lavik G, Schmid M, Jorgensen BB, Kuenen JG, Damste JSS, Strous M, Jetten MSM (2003) Anaerobic ammonium oxidation by anammox bacteria in the Black Sea. Nature 422:608–611

    PubMed  CAS  Google Scholar 

  • Kuypers MMM, Lavik G, Woebken D, Schmid M, Fuchs BM, Amann R, Jørgensen BB, Jetten MSM (2005) Massive nitrogen loss from the Benguela upwelling system through anaerobic ammonium oxidation. PNAS 102:6478–6483

    PubMed  CAS  Google Scholar 

  • LaRoche J, Breitbarth E (2005) Importance of the diazotrophs as a source of new nitrogen in the ocean. J Sea Res 53:67–91

    CAS  Google Scholar 

  • Littleton HX, Daigger GT, Strom PF, Cowan RM (2002) Evaluation of autotrophic denitrification, heterotrophic nitrification, and PAOs in full scale simultaneous biological nutrient removal systems. Water Sci Technol 46:305–312

    PubMed  CAS  Google Scholar 

  • Lorenzen J, Larsen LH, Kjær T, Revsbech NP (1998) Biosensor determination of the microscale distribution of nitrate, nitrate assimilation, nitrification, and denitrification in a diatom inhabited freshwater sediment. Appl Environ Microbiol 64:3264–3269

    PubMed  CAS  Google Scholar 

  • Mehta MP, Huber JA, Baross JA (2005) Incidence of novel and potentially archaeal nitrogenase genes in the deep Northeast Pacific Ocean. Environ Microbiol 7:1525–1534

    PubMed  CAS  Google Scholar 

  • Metz S, Beisker W, Hartmann A, Schloter M (2003) Detection methods for the expression of the dissimilatory copper-containing nitrite reductase gene (DnirK) in environmental samples. J Microbiol Meth 55:41–50

    CAS  Google Scholar 

  • Meyer RL, Kjær T, Revsbech NP (2001) Use of NO3- Microsensors to estimate the activity of sediment nitrification and NO3-consumption along an estuarine salinity, nitrate, and light gradient. Aquat Microb Ecol 26:181–193

    Google Scholar 

  • Meyer RL, Risgaard-Petersen N, Allen DE (2005) Correlation between anammox activity and microscale distribution of nitrite in a subtropical mangrove sediment. Appl Environ Microbiol 71:6142–6149

    PubMed  CAS  Google Scholar 

  • Morgenroth E, Obermayer A, Arnold E, Bruhl A, Wagner M, Wilderer PA (2000) Effect of long-term idle periods on the performance of sequencing batch reactors. Water Sci Technol 41(1):105–113

    CAS  Google Scholar 

  • Mulder A, van de Graaf AA, Robinson LA, Kuenen JG (1995) Anaerobic ammonium oxidation in a denitrifying fluidized bed reactor. FEMS Microbiol Ecol 16:177–184

    CAS  Google Scholar 

  • Murray JW, Codispoti LA, Friederich GE (1995) Oxidation-reduction environments – the suboxic zone in the Black-Sea. Aquat Chem 244:157–176

    Article  CAS  Google Scholar 

  • Mussmann M, Schulz HN, Strotmann B, Kjaer T, Nielsen LP, Rossello-Mora RA, Amann RI, Jørgensen BB (2003) Phylogeny and distribution of nitrate-storing Beggiatoa spp. in coastal marine sediments. Environ Microbiol 5:523–533

    PubMed  CAS  Google Scholar 

  • Nayak S, Prasanna R, Pabby A, Dominic TK, Singh PK (2004) Effect of urea, blue green algae and Azolla on nitrogen fixation and chlorophyll accumulation in soil under rice. Biol Fertil Soils 40:67–72

    CAS  Google Scholar 

  • Nielsen M, Larsen LH, Jetten M, Revsbech NP (2004) A bacterium-based \(\hbox{NO}_{2}^{-}\) biosensor for environmental application. Appl Environ Microbiol 70:6551–6558

    PubMed  CAS  Google Scholar 

  • Nishio T, Koike I, Hattori A (1983) Estimates of denitrification and nitrification in coastal and estuarine sediments. Appl Environ Microbiol 45:444–450

    PubMed  CAS  Google Scholar 

  • Nogales B, Timmis KN, Nedwell DB, Osborn AM (2002) Detection and diversity of expressed denitrification genes in estuarine sediments after reverse transcription-PCR amplification from mRNA Appl Environ Microbiol 68:5017–5025

    PubMed  CAS  Google Scholar 

  • Okabe S, Kindaichi T, Ito T (2005) Fate of 14C-labeled microbial products derived from nitrifying bacteria in autotrophic nitrifying biofilms. Appl Environ Microbiol 71:3987–3994

    PubMed  CAS  Google Scholar 

  • Okabe S, Satoh H, Watanabe Y (1999) In situ analysis of nitrifying biofilms as determined by in situ hybridization and the use of microelectrodes. Appl Environ Microbiol 65:3182–3191

    PubMed  CAS  Google Scholar 

  • Omoregie EO, Crumbliss LL, Bebout BM, Zehr JP (2004) Comparison of diazotroph community structure in Lyngbya sp. and Microcoleus chthonoplastes dominated microbial mats from Guerrero Negro, Baja, Mexico. FEMS Microb Ecol 47:305–318

    CAS  Google Scholar 

  • Otani Y, Hasegawa K, Hanaki K (2004) Comparison of aerobic denitrifying activity among three cultural species with various carbon sources. Water Sci Technol 50:15–22

    PubMed  CAS  Google Scholar 

  • Otte S, Kuenen JG, Nielsen LP, Paerl HW, Zopfi J, Schulz HN, Teske A, Strotmann B, Gallardo VA, Jørgensen BB (1999) Nitrogen, carbon, and sulfur metabolism in natural Thioploca samples. Appl Environ Microbiol 65:3148–3157

    CAS  Google Scholar 

  • Philippot L (2005) Tracking nitrate reducers and denitrifiers in the environment. Biochem Soc Transact 33:200–2004

    PubMed  CAS  Google Scholar 

  • Philippot L, Hallin S (2005) Finding the missing link between diversity and activity using denitrifying bacteria as model functional community. Curr Opin Microbiol 8:234–239

    PubMed  CAS  Google Scholar 

  • Piao Z, Cui ZJ, Yin B, Hu J, Zhou CH, Xie GH, Su BL, Yin SX (2005) Changes in acetylene reduction activities and effects of inoculated rhizosphere nitrogen-fixing bacteria on rice. Biol Fertil Soils 41:371–378

    CAS  Google Scholar 

  • Purkhold U, Wagner M, Timmermann G, Pommerening-Roser A, Koops HP (2003) 16S rRNA and amoA-based phylogeny of 12 novel betaproteobacterial ammonia-oxidizing isolates: extension of the dataset and proposal of a new lineage within the nitrosomonads. Int J Syst Evol Microbiol 53:1485–1494

    PubMed  CAS  Google Scholar 

  • Qiu XY, Hurt RA, Wu LY, Chen CH, Tiedje JM, Zhou Z (2004) Detection and quantification of copper-denitrifying bacteria by quantitative competitive PCR. J Microbiol Meth 59:199–210

    CAS  Google Scholar 

  • Revsbech NP (1989) An oxygen microelectrode with a guard cathode. Limnol Oceanogr 34:472–476

    Google Scholar 

  • Revsbech NP (2005) Analysis of microbial communities with electrochemical microsensors and microscale biosensors. Meth Enzymol 397:147–166

    PubMed  CAS  Google Scholar 

  • Revsbech NP, Jørgensen BB, Blackburn TH, Y Cohen (1983) Microelectrode studies of the photosynthesis and O2, H2S and pH profiles of a microbial mat. Limnol Oceanogr 28:1062–1074

    Article  Google Scholar 

  • Revsbech NP, Kjær T, Damgaard L, Lorenzen J, Larsen LH (2000) Biosensors for analysis of water, sludge, and sediments with emphasis on microscale biosensors. In: Buffle J, Horvai G (eds) In situ monitoring of aquatic systems: chemical analysis and speciation. Wiley, New York, pp 195–222

    Google Scholar 

  • Richards FA (1965) Anoxic basins and Fjords. In: Riley JP, Skirrow G (eds) Chemical oceanography, vol 1. Academic Press, London

    Google Scholar 

  • Risgaard-Petersen N (2003) Coupled nitrification-denitrification in autotrophic and heterotrophic estuarine sediments: on the influence of benthic microalgae. Limnol Oceanogr 48:93–105

    Article  CAS  Google Scholar 

  • Risgaard-Petersen N, Meyer RL, Revsbech NP (2005) Denitrification and anaerobic ammonium oxidation in sediments: effects of microphytobenthos and NO3. Aquat Microb Ecol 40:67–76

    Google Scholar 

  • Risgaard-Petersen N, Meyer RL, Schmid M, Jetten MSM, Enrich-Prast A, Rysgaard S, Revsbech NP (2004a) Anaerobic ammonium oxidation in an estuarine sediment. Aquat Microb Ecol 36:293–304

    Google Scholar 

  • Risgaard-Petersen N, Nicolaisen MH, Revsbech NP, Lomstein BA (2004b) Competition between ammonia-oxidizing bacteria and benthic microalgae. Appl Environ Microbiol 70:5528–5537

    CAS  Google Scholar 

  • Risgaard-Petersen N, Rysgaard S, Nielsen LP, Revsbech NP (1994) Diurnal variation of denitrification and nitrification in sediments colonized by benthic microphytes. Limnol Oceanogr 39:573–579

    Article  CAS  Google Scholar 

  • Robertson LA, Dalsgaard T, Revsbech NP, Kuenen JG (1995) Confirmation of aerobic denitrification in batch cultures, using gas chromatography and 15N mass spectrometry. FEMS Microbiol Ecol 18:113–120

    CAS  Google Scholar 

  • Rysgaard S, Christensen PB, Nielsen LP (1995) Seasonal-variation in nitrification and denitrification in estuarine sediment colonized by benthic microalgae and bioturbating infauna. Mar Ecol Progr Ser 126:111–121

    CAS  Google Scholar 

  • Rysgaard S, Glud RN (2004) Anaerobic N2 production in Arctic sea ice. Limnol Oceanogr 49:86–94

    Article  CAS  Google Scholar 

  • Rysgaard S, Glud RN, Risgaard-Petersen N, Dalsgaard T␣(2004) Denitrification and anammox activity in␣Arctic marine sediments. Limnol Oceanogr 49:1493–1502

    Article  CAS  Google Scholar 

  • Rysgaard S, Risgaard-Petersen N, Nielsen LP, Revsbech NP (1993) Nitrification and denitrification in lake and estuarine sediments measured by the 15N dilution technique and isotope pairing. Appl Environ Microbiol 59:2093–2098

    PubMed  CAS  Google Scholar 

  • Sayama M, Risgaard-Petersen N, Nielsen LP, Fossing H, Christensen PB (2005) Impact of bacterial NO3- transport on sediment biogeochemistry. Appl Environ Microbiol 71:7575–7577

    PubMed  CAS  Google Scholar 

  • Schleper C, Jurgens G, Jonuscheit M (2005) Genomic studies of uncultivated Archaea. Nat Rev Microbiol 3:479–488

    PubMed  CAS  Google Scholar 

  • Schmid M, Schmitz-Esser S, Jetten M, Wagner M (2001) 16S-23S rDNA intergenic spacer and 23S rDNA of anaerobic ammonium-oxidizing bacteria: implications for phylogeny and in situ detection. Environ. Microbiol. 3:450–459

    PubMed  CAS  Google Scholar 

  • Schmid M, Walsh K, Webb R, Rijpstra W, van de Pas-Schoonen K, Verbruggen M, Hill T, Moffett B, Fuerst J, Schouten S, Damste J, Harris J, Shaw P, Jetten M, Strous M (2003) Candidatus “Scalindua brodae”, sp. nov., Candidatus Scalindua wagneri, sp. nov., two new species of anaerobic ammonium oxidizing bacteria. Syst Appl Microbiol 26:529–538

    PubMed  CAS  Google Scholar 

  • Schmidt I, Sliekers O, Schmid M, Bock E, Fuerst J, Kuenen JG, Jetten MSM, Strous M (2003) New concepts of microbial treatment processes for the nitrogen removal in wastewater FEMS Microbiol. Rev. 27:481–492

    PubMed  CAS  Google Scholar 

  • Schramm A (2003) In situ analysis of structure and activity of the nitrifying community in biofilms, aggregates, and sediments. Geomicrobiol J 20:313–333

    CAS  Google Scholar 

  • Schramm A, de Beer D, Gieseke A, Amann R (2000) Microenvironments and distribution of nitrifying bacteria in a membrane-bound biofilm. Environ Microbiol 2:680–686

    PubMed  CAS  Google Scholar 

  • Schramm A, de Beer D, van den Heuvel JC, SO, Amann R (1999) Microscale distribution of populations and activities of Nitrosospira and Nitrospira spp. along a macroscale gradient in a nitrifying bioreactor: quantification by in situ hybridization and the use of microsensors. Appl Environ Microbiol 65:3690–3696

  • Schramm A, Larsen LH, Revsbech NP, Ramsing NB, Amann R, Schleifer K-H (1996) Structure and function of a nitrifying biofilm as determined by in situ hybridization and microelectrodes. Appl Environ Microbiol 62:4641–4647

    PubMed  CAS  Google Scholar 

  • Sharma S, Aneja MK, Mayer J, Munch JC, Schloter M (2005) Diversity of transcripts of nitrite reductase genes (nirK and nirS) in rhizospheres of grain legumes. Appl. Environ. Microbiol. 71(4):2001–2007

    PubMed  CAS  Google Scholar 

  • Stange F, Dohling F (2005) N-15 tracing model SimKIM to analyse the NO and N2O production during autotrophic, heterotrophic nitrification, and denitrification in soils. Isotopes Environ Health Stud 41:261–274

    PubMed  CAS  Google Scholar 

  • Strous M, Jetten MSM (2004) Anaerobic oxidation of methane and ammonium. Ann Rev Microbiol 58:99–117

    CAS  Google Scholar 

  • Thamdrup B, Dalsgaard T (2002) Production of N-2 through anaerobic ammonium oxidation coupled to nitrate reduction in marine sediments. Appl Environ Microbiol 68:1312–1318

    PubMed  CAS  Google Scholar 

  • Tiedje JM (1987) Ecology of denitrification and dissimilatory nitrate reduction to ammonium. In: Zehnder AJB (eds) Biology of anaerobic microorganisms. Wiley, New York, pp 179–244

    Google Scholar 

  • Treusch AH, Leininger S, Kletzin A, Schuster SC, Klenk H-P, Schleper C (2005) Novel genes for nitrite reductase and Amo-related proteins indicate a role of uncultivated mesophilic crenarchaeota in nitrogen cycling. Environ Microbiol 7:1985–1995

    PubMed  CAS  Google Scholar 

  • Trimmer M, Nicholls JC, Deflandre B (2003) Anarobic Ammonium Oxidation measured in sediments along the Thames Estuary, United Kingdom. Appl Environ Microbiol 69:6447–6454

    PubMed  CAS  Google Scholar 

  • van de Graaf AA, de Bruijn P, Robertson LA, Jetten MSM, Kuhnen JG (1997) Metabolic pathway of anaerobic ammonium oxidation on the basis of N-15 studies in a fludized bed reactor. Microbiology 141:2415–2421

    Article  Google Scholar 

  • Venter JC, Remington K, Heidelberg JF, Halpern AL, Rusch D, Eisen JA, Wu D, Paulsen I, Nelson KE, Nelson W, Fouts DE, Levy S, Knap AH, Lomas MW, Nealson K, White O, Peterson J, Hoffman J, Parsons R, Baden-Tillson H, Pfannkoch C, Rogers Y-H, Smith HO (2004) Environmental genome shotgun sequencing of the Sargasso Sea. Science 304:66–74

    PubMed  CAS  Google Scholar 

  • Zehr JP, Ward BB (2002) Nitrogen cycling in the ocean: new perspectives on processes and paradigms. Appl Environ Microbiol 68:1015–1024

    PubMed  CAS  Google Scholar 

  • Zumft WG (1991) The denitrifying prokaryotes. In: Balows A, Trüper HG, Dworkin M, Harder W, Schleifer KH (eds) The Prokaryotes, 2nd edn. Springer Verlag, New York, pp 554–582

    Google Scholar 

Download references

Acknowlegdements

The work presented here was partly supported by grants from the The Carlsberg Foundation (NRI) and The Danish Natural Science Research Council (NPR and AS).

Author information

Authors and Affiliations

  1. Institute of Biological Sciences, Microbiology, University of Aarhus, bd. 540, DK-8000, Aarhus C, Denmark

    Niels Peter Revsbech, Andreas Schramm & Lars Peter Nielsen

  2. National Environmental Research Institute, Vejlsøvej 25, DK-8600, Silkeborg, Denmark

    Nils Risgaard-Petersen

Authors
  1. Niels Peter Revsbech
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Nils Risgaard-Petersen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Andreas Schramm
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Lars Peter Nielsen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Niels Peter Revsbech.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Revsbech, N.P., Risgaard-Petersen, N., Schramm, A. et al. Nitrogen transformations in stratified aquatic microbial ecosystems. Antonie van Leeuwenhoek 90, 361–375 (2006). https://doi.org/10.1007/s10482-006-9087-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10482-006-9087-5

Keywords

Search

Navigation