Skip to main content

Advertisement

Log in

Anaerobic ammonium oxidation in marine environments: contribution to biogeochemical cycles and biotechnological developments for wastewater treatment

  • Review Paper
  • Published:
Reviews in Environmental Science and Bio/Technology Aims and scope Submit manuscript

Abstract

Microbial processes are responsible for most reactions involved in the nitrogen cycle in the oceans, which determine the fluxes of this crucial nutrient in these environments. The present review provides an overview of the contribution of anaerobic ammonium oxidation (Anammox) to marine biogeochemical processes. Besides the conventional Anammox process, anaerobic ammonium oxidation coupled to the microbial reduction of alternative electron acceptors, such as sulfate (Sulfammox), ferric iron (Feammox), and natural organic matter (NOM-dependent Anammox) is also described in the context of global marine biogeochemical cycles. Also, the complex interactions among the oceanic biogeochemical cycles of N, S and Fe are discussed at the light of the new findings available in the literature. The review also underlines the important role of the microbial processes performing the Anammox reaction in the development of wastewater treatment systems for the removal of nitrogen from saline effluents. Strategies to enrich and immobilize Anammox bacteria in different reactor configurations for the treatment of saline wastewaters are also described as well as future directions for novel biotechnological developments based on Anammox.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  • Ali M, Okabe S (2015) Anammox-based technologies for nitrogen removal: advances in process start-up and remaining issues. Chemosphere 141:144–153

    Article  CAS  Google Scholar 

  • Ali M, Oshiki M, Awata T, Isobe K, Kimura Z, Yoshikawa H, Hira D, Kindaichi T, Satoh H, Fujii T, Okabe S (2015) Physiological characterization of anaerobic ammonium oxidizing bacterium ‘Candidatus Jettenia caeni’. Environ Microbiol 17:2172–2189

    Article  CAS  Google Scholar 

  • Arrigo KR (2005) Marine microorganisms and global nutrient cycles. Nature 437:349–355

    Article  CAS  Google Scholar 

  • Bale NJ, Villanueva L, Fan H, Stal LJ, Hopmans EC, Schouten S, Sinninghe Damsté JS (2014) Occurrence and activity of anammox bacteria in surface sediments of the southern North Sea. FEMS Microbiol Ecol 89:99–110

    Article  CAS  Google Scholar 

  • Borin S, Mapelli F, Rolli E, Song B, Tobias C, Schmid MC, De Lange GJ, Reichart GJ, Schouten S, Jetten M, Daffonchio D (2013) Anammox bacterial populations in deep marine hypersaline gradient systems. Extremophiles 17:289–299

    Article  CAS  Google Scholar 

  • Bradley PM, Chapelle FH, Lovley DR (1998) Humic acids as electron acceptors for anaerobic microbial oxidation of vinyl chloride and dichloroethene. Appl Environ Microbiol 64:3102–3105

    CAS  Google Scholar 

  • Brandsma J, van de Vossenberg J, Risgaard-Petersen N, Schmid MC, Engström P, Eurenius K, Hulth S, Jaeschke A, Abbas B, Hopmans EC, Strous M, Schouten S, Jetten MSM, Sinninghe Damsté JS (2011) A multi-proxy study of anaerobic ammonium oxidationin marine sediments of the Gullmar Fjord, Sweden. Environ Microbiol Rep 3:360–366

    Article  CAS  Google Scholar 

  • Broda E (1977) Two kinds of lithotrophs missing in nature. Zeitschrift für Allg Mikrobiol 17:491–493

    Article  CAS  Google Scholar 

  • Brunekreef B, Holgate ST (2002) Air pollution and health. Lancet 360:1233–1242

    Article  CAS  Google Scholar 

  • Cervantes FJ (2009) Environmental technologies to treat nitrogen pollution: principles and engineering. IWA Publishing, London

    Book  Google Scholar 

  • Cervantes F, Monroy O, Gómez J (1999) Influence of ammonium on the performance of a denitrifying culture under heterotrophic conditions. Appl Biochem Biotechnol 81:13–21

    Article  CAS  Google Scholar 

  • Cervantes FJ, van der Velde S, Lettinga G, Field JA (2000) Quinones as terminal electron acceptors for anaerobic microbial oxidation of phenolic compounds. Biodegradation 11:313–321

    Article  CAS  Google Scholar 

  • Cervantes FJ, Dijksma W, Duong-Dac T, Ivanova A, Lettinga G, Field JA (2001) Anaerobic mineralization of toluene by enriched sediments with quinones and humus as terminal electron acceptors. Appl Environ Microbiol 67:4471–4478

    Article  CAS  Google Scholar 

  • Cervantes FJ, Gutiérrez CH, López KY, Estrada-Alvarado MI, Meza-Escalante ER, Texier A-C, Cuervo F, Gómez J (2008) Contribution of quinone-reducing microorganisms on the anaerobic biodegradation of organic compounds under different redox conditions. Biodegradation 19:235–246

    Article  CAS  Google Scholar 

  • Cervantes FJ, Mancilla AR, Rios-del Toro EE, Alpuche-Solis AG, Montoya-Lorenzana L (2011) Anaerobic benzene oxidation by enriched inocula with humic acids as terminal electron acceptors. J Hazard Mat 195:201–207

    Article  CAS  Google Scholar 

  • Clément JC, Shrestha J, Ehrenfeld JG, Jaffé PR (2005) Ammonium oxidation coupled to dissimilatory reduction of iron under anaerobic conditions in wetland soils. Soil Biol Biochem 37:2323–2328

    Article  CAS  Google Scholar 

  • Dalsgaard T, Canfield DE, Petersen J, Thamdrup B, Acuña-González J (2003) N2 production by the anammox reaction in the anoxic water column of Golfo Dulce, Costa Rica. Nature 422:606–608

    Article  CAS  Google Scholar 

  • Dapena-Mora A, Arrojo B, Campos JL, Mosquera-Corral A, Méndez R (2004) Improvement of the settling properties of anammox sludge in an SBR. J Chem Technol Biotechnol 79:1417–1420

    Article  CAS  Google Scholar 

  • Dapena-Mora A, Vázquez-Padín JR, Campos JL, Mosquera-Corral A, Jetten MSM, Méndez R (2010) Monitoring the stability of an anammox reactor under high salinity conditions. Biochem Eng J 51:167–171

    Article  CAS  Google Scholar 

  • Devol AH (2003) Nitrogen cycle: solution to a marine mystery. Nature 422:575–576

    Article  CAS  Google Scholar 

  • Devol AH (2015) Denitrification, anammox, and N2 production in marine sediments. Annu Rev Mar Sci 7:403–423

    Article  Google Scholar 

  • Dietl A, Ferousi C, Maalcke WJ, Menzel A, de Vries S, Keltjens JT, Jetten MSM, Kartal B, Barends TRM (2015) The inner workings of the hydrazine synthase mulitprotein complex. Nature 527:394–397

    Article  CAS  Google Scholar 

  • Ding L-J, An XL, Li S, Zhang GL, Zhu YG (2014) Nitrogen loss through anaerobic ammonium oxidation coupled to iron reduction from paddy soils in a chronosequence. Environ Sci Technol 48:10641–10647

    Article  CAS  Google Scholar 

  • Doane TA (2017) The abiotic nitrogen cycle. ACS Earth Space Chem 1:411–421

    Article  CAS  Google Scholar 

  • 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 benthic nitrate reduction in tropical estuaries. Limnol Oceanogr 56:279–291

    Article  CAS  Google Scholar 

  • Engstrøm P, Dalsgaard T, Hulth S, Aller RC (2005) Anaerobic ammonium oxidation with nitrite (anammox): implications for N2 production in coastal marine sediments. Geochim Cosmochim Acta 69:2057–2065

    Article  CAS  Google Scholar 

  • Engstrøm P, Penton CR, Devol AH (2009) Anaerobic ammonium oxidation in deep-sea sediments off the Washington margin. Limnol Oceanogr 54:1643–1652

    Article  Google Scholar 

  • Falkowski PG (1997) Evolution of the nitrogen cycle and its influence on the biological sequestration of CO2 in the ocean. Nature 387:272–275

    Article  CAS  Google Scholar 

  • Falkowski PG, Barber RT, Smetacek V (1998) Biogeochemical controls and feedbacks on ocean primary production. Science 281:200–206

    Article  CAS  Google Scholar 

  • FAO (2004) The state of world fisheries and aquaculture 2004. Italy, Rome

    Google Scholar 

  • Fdz-Polanco F, Fdz-Polanco M, Fernandez N, Urueña MA, Garcia PA, Villaverde S (2001) New process for simultaneous removal of nitrogen and sulphur under anaerobic conditions. Water Res 35:1111–1114

    Article  CAS  Google Scholar 

  • Fernandes SO, Bharathi PA, Bonin PC, Michotey VS (2010) Denitrification: an important pathway for nitrous oxide production in tropical mangrove sediments (Goa, India). J Envrion Qual 39:1507–1516

    Article  CAS  Google Scholar 

  • Fowler D, Coyle M, Skiba U, Sutton MA, Cape JN, Reis S, Sheppard LJ, Jenkins A, Grizzetti B, Galloway JN, Vitousek P, Leach A, Bouwman AF, Butterbach-Bahl K, Dentener F, Stevenson D, Amann M, Voss M (2013) The global nitrogen cycle in the twenty-first century. Philos Trans R Soc B 368:20130164

    Article  CAS  Google Scholar 

  • Galloway JN, Townsend AR, Erisman JW, Bekunda M, Cai Z, Freney JR, Martinelli LA, Seitzinger SP, Sutton MA (2008) Transformation of the nitrogen cycle: recent trends, questions, and potential solutions. Science 320:889–892

    Article  CAS  Google Scholar 

  • Gihring TM, Lavik G, Kuypers MM, Kostka JE (2010) Direct determination of nitrogen cycling rates and pathways in Arctic fjord sediments (Svalbard, Norway). Limnol Oceanogr 55:43–54

    Article  CAS  Google Scholar 

  • Gilch S, Vogel M, Lorenz MW, Meyer O, Schmidt I (2009) Interaction of the mechanism-based inactivator acetylene with ammonia monooxygenase of Nitrosomonas europaea. Microbiology 155:279–284

    Article  CAS  Google Scholar 

  • Glud RN, Thamdrup B, Stahl H, Wenzhøefer F, Glud A, Nomaki H, Oguri K, Revsbech NP, Kitazato H (2009) Nitrogen cycling in a deep ocean margin sediment (Sagami Bay, Japan). Limnol Oceanogr 54:723–734

    Article  CAS  Google Scholar 

  • Gonzalez-Silva B, Rønning AJ, Andreassen IK, Bakke I, Cervantes FJ, Østgaard K, Vadstein O (2017) Changes in the microbial community of an anammox consortium during adaptation to marine conditions revealed by 454 pyrosequencing. Appl Microbiol Biotechnol 101:5149–5162

    Article  CAS  Google Scholar 

  • Hamersley MR, Lavik G, Woebken D, Rattray JE, Lam P, Hopmans EC, Sinninghe Damsté JS, Krüger S, Graco M, Gutiérrez D, Kuypers MMM (2007) Anaerobic ammonium oxidation in the Peruvian oxygen minimum zone. Limnol Oceanogr 52:923–933

    Article  CAS  Google Scholar 

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

    Google Scholar 

  • Hansell DA (2013) Recalcitrant dissolved organic carbon fractions. Annu Rev Mar Sci 5:421–445

    Article  Google Scholar 

  • He S, Niu Q, Ma H, Zhang Y, Li YY (2015) The treatment performance and the bacteria preservation of anammox: a review. Water Air Soil Pollut 226:163

    Article  CAS  Google Scholar 

  • Hietanen S, Kuparinen J (2008) Seasonal and short-term variation in denitrification and anammox at a coastal station of the Gulf of Finland, Baltyic Sea. Hydrobiologia 596:67–77

    Article  CAS  Google Scholar 

  • Hooper AB, Vannelli T, Bergmann DJ, Arciero DM (1997) Enzymology of the oxidation of ammonia to nitrite by bacteria. Anton Leeuw Int J G 71:59–67

    Article  CAS  Google Scholar 

  • Hu Z, Lotti T, Van Loosdrecht M, Kartal B (2013) Nitrogen removal with the anaerobic ammonium oxidation process. Biotechnol Lett 35:1145–1154

    Article  CAS  Google Scholar 

  • Huang S, Jaffé PR (2018) Isolation and characterization of an ammonium-oxidizing iron reducer: Acidimicrobiaceae sp. A6. PLoS ONE 10:2. https://doi.org/10.1371/journal.pone.0194007

    Article  CAS  Google Scholar 

  • Isobe K, Ohte N (2014) Ecological perspectives on microbes involved in N-cycling. Microbes Environ 29:4–16

    Article  Google Scholar 

  • Jantti H, Stange F, Leskinen E, Hietanen S (2011) Seasonal variation in nitrification and nitrate-reduction pathways in coastal sediments in the Gulf of Finland, Baltic Sea. Aquat Microb Ecol 63:171–181

    Article  Google Scholar 

  • Jetten MSM, van Niftrik L, Strous M, Kartal B, Keltjens JT, Op den Camp HJM (2009) Biochemistry and molecular biology of anammox bacteria. Crit Rev Biochem Mol Biol 44:65–84

    Article  CAS  Google Scholar 

  • Jetten MSM, Op de Camp HJM, Kuenen JG, Strous M (2010) Description of the order brocadiales. In: Krieg NR (ed) Bergey`s manual of systematic bacteriology, vol 4. Springer, Heidelberg, pp 506–603

    Google Scholar 

  • Jin RC, Ma C, Mahmood Q, Yang GF, Zheng P (2011) Anammox in a UASB reactor treating saline wastewater. Process Saf Environ Prot 89:342–348

    Article  CAS  Google Scholar 

  • Kartal B, Koleva M, Arsov R, van der Star W, Jetten MSM, Strous M (2006) Adaptation of a freshwater anammox population to high salinity wastewater. J Biotechnol 126:546–553

    Article  CAS  Google Scholar 

  • Kartal B, Kuypers MMM, Lavik G, Schalk J, Op den Camp HJM, Jetten MSM, Strous M (2007) Anammox bacteria disguised as denitrifiers: nitrate reduction to dinitrogen gas via nitrite and ammonium. Environ Microbiol 9:635–642

    Article  CAS  Google Scholar 

  • Kartal B, van Niftrik L, Rattray J, van de Vossenberg JL, Schmid MC, Sinninghe Damsté J, Jetten MSM, Strous M (2008) Candidatus ‘Brocadia fulgida’: an autofluorescent anaerobic ammonium oxidizing bacterium. FEMS Microbiol Ecol 63:46–55

    Article  CAS  Google Scholar 

  • Kartal B, Maalcke WJ, de Almeida NM, Cirpus I, Gloerich J, Geerts W, Op den Camp HJM, Harhangi HR, Janssen-Megens EM, Francoijs KJ, Stunnenberg HG, Keltjens JT, Jetten MSM, Strous M (2011) Molecular mechanism of anaerobic ammonium oxidation. Nature 479:127–130

    Article  CAS  Google Scholar 

  • Kartal B, de Almeida NM, Maalcke WJ, Op den Camp HJM, Jetten MSM, Keltjens JT (2013) How to make a living from anaerobic ammonium oxidation. FEMS Microbiol Rev 37:428–461

    Article  CAS  Google Scholar 

  • Kawagoshi Y, Nakamura Y, Kawashima H, Fujisaki K, Furukawa K, Fujimoto A (2010) Enrichment of marine anammox bacteria from seawater-related samples and bacterial community study. Water Sci Technol 61:119–126

    Article  CAS  Google Scholar 

  • Kim J, Lim J, Lee C (2013) Quantitative real-time PCR approaches for microbial community studies in wastewater treatment systems: applications and considerations. Biotechnol Adv 31:1358–1373

    Article  CAS  Google Scholar 

  • Kim T, An J, Lee H, Jang JK, Chang IS (2016) pH-dependent ammonia removal pathways in microbial fuel cell system. Bioresour Technol 215:290–295

    Article  CAS  Google Scholar 

  • Kindaichi T, Awata T, Suzuki Y, Tanabe K, Hatamoto M, Ozaki N, Ohashi A (2011) Enrichment using an up-flow column reactor and community structure of marine anammox bacteria from coastal sediment. Microbes Environ 26:67–73

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Kuypers MM, 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. Proc Natl Acad Sci USA 102:6478–6483

    Article  CAS  Google Scholar 

  • Kuypers MMM, Marchant HK, Kartal B (2018) The microbial nitrogen-cycling network. Nat Rev Microbiol 16:263–276

    Article  CAS  Google Scholar 

  • Lackner S, Gilbert EM, Vlaeminck SE, Joss A, Horn H, Van Loosdrecht MCM (2014) Full-scale partial nitritation/anammox experiences—an application survey. Water Res 55:292–303

    Article  CAS  Google Scholar 

  • Lam P, Jensen MM, Lavik G, McGinnis DF, Müller B, Schubert CJ, Amann R, Thamdrup B, Kuypers MMM (2007) Linking crenarchaeal and bacterial nitrification to anammox in the Black Sea. Proc Natl Acad Sci USA 104:7104–7109

    Article  CAS  Google Scholar 

  • Lam P, Lavik G, Jensen MM, van Vossenberg JD, Schmid M, Woebken D, Gutiérrez D, Amann R, Jetten MSM, Kuypers MMM (2009) Revising the nitrogen cycle in the Peruvian oxygen minimum zone. Proc Nat Acad Sci USA 106:4752–4757

    Article  CAS  Google Scholar 

  • Laufer K, Røy H, Jørgensen B (2016) Evidence for the existence of autotrophic nitrate-reducing Fe(II)-oxidizing bacteria in marine coastal sediment. Appl Environ Microbiol 82:6120–6131

    Article  CAS  Google Scholar 

  • Li M, Gu JD (2011) Advances in methods for detection of anaerobic ammonium oxidizing (anammox) bacteria. Appl Microbiol Biotechnol 90:1241–1252

    Article  CAS  Google Scholar 

  • Li X, Hou L, Liu M, Zheng Y, Yin G, Lin X, Cheng L, Li Y, Hu X (2015) Evidence of nitrogen loss from anaerobic ammonium oxidation coupled with ferric iron reduction in an intertidal wetland. Environ Sci Technol 49:11560–11568

    Article  CAS  Google Scholar 

  • Lipsewers YA, Bale NJ, Hopmans EC, Schouten S, Sinninghe Damsté JS, Villanueva L (2014) Seasonality and depth distribution of the abundance and activity of ammonia oxidizing microorganisms in marine coastal sediments (North Sea). Front Microbiol 5:472

    Google Scholar 

  • Liu S, Yang F, Gong Z, Chen H, Xue Y, Furukawa K (2008) Application of anaerobic ammonium-oxidizing consortium to achieve completely autotrophic ammonium and sulfate removal. Bioresour Technol 99:6817–6825

    Article  CAS  Google Scholar 

  • Lüke C, Speth DR, Kox MAR, Villanueva L, Jetten MSM (2016) Metagenomic analusis of nitrogen and methane cycling in the Arabian Sea oxygen minimum zone. Peer J 2016:e1924

    Article  CAS  Google Scholar 

  • Martinez CM, Alvarez LH, Celis LB, Cervantes FJ (2013) Humus reducing microorganisms and their valuable contribution in environmental processes. Appl Microbiol Biotechnol 97:10293–10308

    Article  CAS  Google Scholar 

  • Moss FR, Shuken SR, Mercer JAM, Cohen CM, Weiss TM, Boxer SG, Burns NZ (2018) Ladderane phospholipids form a densely packed membrane with normal hydrazine and anomalously low proton/hydroxide permeability. Proc Natl Acad Sci USA 115:9098–9103

    Article  CAS  Google Scholar 

  • Mulder A, van de Graaf A, Robertson L, Kuenen J (1995) Anaerobic ammonium oxidation discovered in a denitrifying fluidized bed reactor. FEMS Microbiol Ecol 16:177–184

    Article  CAS  Google Scholar 

  • Nakajima J, Sakka M, Kimura T, Furukawa K, Sakka K (2008) Enrichment of anammox bacteria from marine environment for the construction of a bioremediation reactor. Appl Microbiol Biotechnol 77:1159–1166

    Article  CAS  Google Scholar 

  • Neubacher EC, Parker RE, Trimmer M (2011) Short-term hypoxia alters the balance of the nitrogen cycle in coastal sediments. Limnol Oceanogr 56:651–665

    Article  CAS  Google Scholar 

  • Ni BJ, Hu BL, Fang F, Xie WM, Kartal B, Liu XW, Sheng GP, Jetten M, Zheng P, Yu HQ (2010) Microbial and physicochemical characteristics of compact anaerobic ammonium-oxidizing granules in an upflow anaerobic sludge blanket reactor. Appl Environ Microbiol 76:2652–2656

    Article  CAS  Google Scholar 

  • Nicholls JC, Trimmer M (2009) Widespread occurence of the anammox reaction in estuarine sediments. Aquat Microb Ecol 55:105–113

    Article  Google Scholar 

  • Nieto-Cid M, Álvarez-Salgado XA, Gago J, Pérez FF (2005) DOM fluorescence, a tracer for biogeochemical processes in a coastal upwelling system. Mar Ecol Prog Ser 297:33–50

    Article  CAS  Google Scholar 

  • Nikolaev YA, Kozlov MN, Kevbrina MV, Dorofeev AG, Pimenov NV, Kallistova AY, Grachev VA, Kazakova EA, Zharkov AV, Kuznetsov BB, Patutina EO, Bumazhkin BK (2015) CandidatusJettenia moscovienalis’ sp. nov., a new species of bacteria carrying out anaerobic ammonium oxidation. Microbiology 84:256–262

    Article  CAS  Google Scholar 

  • Oshiki M, Shimokawa M, Fujii N, Satoh H, Okabe S (2011) Physiological characteristics of the anaerobic ammonium-oxidizing bacterium ‘Candidatus Brocadia sinica’. Microbiology 157:1706–1713

    Article  CAS  Google Scholar 

  • Oshiki M, Ishii S, Yoshida K, Fujii N, Ishiguro M, Satoh H, Okabe S (2013) Nitrate-dependent ferrous iron oxidation by anaerobic ammonium oxidation (anammox) bacteria. Appl Environ Microbiol 79:4087–4093

    Article  CAS  Google Scholar 

  • Oshiki M, Ali M, Shinyako-Hata K, Satoh H, Okabe S (2016) Hydroxylamine-dependent anaerobic ammonium oxidation (anammox) by “Candidatus Brocadia sinica”. Environ Microbiol 18:3133–3143

    Article  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 

  • Park H, Brotto AC, van Loosdrecht MCM, Chandran K (2017) Discovery and metagenomic analysis of an anammox bacterial enrichment related to CandidatusBrocadia caroliniensis” in a full-scale glycerol-fed nitritation-denitritation separate centrate treatment process. Water Res 111:265–273

    Article  CAS  Google Scholar 

  • Peeters SH, van Niftrik L (2019) Trending topics and open questions in anaerobic ammonium oxidation. Curr Opin Chem Biol 49:45–52

    Article  CAS  Google Scholar 

  • Pitcher A, Villanueva L, Hopmans EC, Schouten S, Reichart G-J, Sinninghe Damsté JS (2011) Niche segregation of ammonia-oxidizing archaea and anammox bacteria in the Arabian Sea oxygen minimum zone. ISME J 5:1896–1904

    Article  CAS  Google Scholar 

  • Quan ZX, Rhee SK, Zuo JE, Yang Y, Bae JW, Park JR, Lee ST, Park YH (2008) Diversity of ammonium-oxidizing bacteria in a granular sludge anaerobic ammonium-oxidizing (anammox) reactor. Environ Microbiol 10:3130–3139

    Article  CAS  Google Scholar 

  • Rich JJ, Dale OR, Song B, Ward BB (2008) Anaerobic ammonium oxidation (anammox) in Chesapeake Bay sediments. Microb Ecol 55:311–320

    Article  CAS  Google Scholar 

  • Richards F (1965) Anoxic basins and fjords. In: Riley J, Skirrow G (eds) Chemical oceanography. Academic Press, London, pp 611–645

    Google Scholar 

  • Rikmann E, Zekker I, Tomingas M, Tenno T, Menert A, Loorits L, Tenno T (2012) Sulfate-reducing anaerobic ammonium oxidation as a potential treatment method for high nitrogen-content wastewater. Biodegradation 23:509–524

    Article  CAS  Google Scholar 

  • Rikmann E, Zekker I, Tomingas M, Vabamäe P, Kroon K, Saluste A, Tenno T, Menert A, Loorits L, Rubin SS, Tenno T (2014) Comparison of sulfate-reducing and conventional anammox upflow anaerobic sludge blanket reactors. J Biosci Bioeng 118:426–433

    Article  CAS  Google Scholar 

  • Rikmann E, Zekker I, Tomingas M, Tenno T, Loorits L, Vabamäe P, Mandel A, Raudkivi M, Daija L, Kroon K, Tenno T (2016) Sulfate-reducing anammox for sulfate and nitrogen containing wastewaters. Desalin Water Treat 7:3132–3141

    Article  CAS  Google Scholar 

  • Rios-Del Toro EE, Cervantes FJ (2016) Coupling between anammox and autotrophic denitrification for simultaneous removal of ammonium and sulfide by enriched marine sediments. Biodegradation 27:107–118

    Article  CAS  Google Scholar 

  • Rios-del Toro EE, López-Lozano NE, Cervantes FJ (2017) Up-flow anaerobic sediment trapped (UAST) reactor as a new configuration for the enrichment of anammox bacteria from marine sediments. Bioresour Technol 238:528–533

    Article  CAS  Google Scholar 

  • Rios-Del Toro EE, Cortés-Martínez MG, Sánchez-Rodríguez MA, Calvario-Martínez O, Sánchez-Carrillo S, Cervantes FJ (2018a) Anaerobic ammonium oxidation linked to sulfate and ferric iron reduction fuels nitrogen loss in marine sediments. Biodegradation 29:429–442

    Article  CAS  Google Scholar 

  • Rios-del Toro EE, Valenzuela EI, Ramírez JE, López-Lozano NE, Cervantes FJ (2018b) Anaerobic ammonium oxidation linked to microbial reduction of natural organic matter in marine sediments. Environ Sci Technol Lett 5:571–577

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Rooks C, Schmid MC, Mehsana W, Trimmer M (2012) The depth-specific significance and relative abundance of anaerobic ammonium-oxidizing bacteria in estuarine sediments (Medway Estuary, UK). FEMS Microbiol Ecol 80:19–29

    Article  CAS  Google Scholar 

  • Rooze J, Meile C (2016) The effect of redox conditions and bioirrigation on nitrogen isotope fractionation in marine sediments. Geochim Cosmochim Acta 184:227–239

    Article  CAS  Google Scholar 

  • Santarella-Mellwig R, Franke J, Jaedicke A, Gorjanacz M, Bauer U, Budd A, Mattaj IW, Devos DP (2010) The compartmentalized bacteria of the planctomycetes–cerrucomicrobia–chlamydiae superphylum have membrane coat-like proteins. PLoS Biol 8:e10000281

    Article  CAS  Google Scholar 

  • Sawayama S (2006) Possibility of anoxic ferric ammonium oxidation. J Biosci Bioeng 101:70–72

    Article  CAS  Google Scholar 

  • Schalk J, Oustad H, Kuenen JG, Jetten MSM (1998) The anaerobic oxidation of hydrazine: a novel reaction in microbial nitrogen metabolism. FEMS Microbiol Lett 158:61–67

    Article  CAS  Google Scholar 

  • Schmid M, Walsh K, Webb R, Rijpstra WIC, Van De Pas-Schoonen K, Verbruggen MJ, Hill T, Moffett B, Fuerst J, Schouten S, Damsté JSS, Harris J, Shaw P, Jetten M, Strous M (2003) CandidatusScalindua brodae”, sp. nov., CandidatusScalindua wagneri”, sp. nov., two new species of anaerobic ammonium oxidizing bacteria. Syst Appl Microbiol 26:529–538

    Article  CAS  Google Scholar 

  • Schmid MC, Maas B, Dapena A, van de Pas-Schoonen K, van de Vossenberg J, Kartal B, van Niftrik L, Schmidt I, Cirpus I, Kuenen JG, Wagner M, Sinninghe Damsté JS, Kuypers M, Revsbech NP, Mendez R, Jetten MSM, Strous M (2005) Biomarkers for in situ detection of anaerobic ammonium-oxidizing (anammox) bacteria. Appl Environ Microbiol 71:1677–1684

    Article  CAS  Google Scholar 

  • Schmid MC, Risgaard-Petersen N, Van De Vossenberg J, Kuypers MM, Lavik G, Petersen J, Hulth S, Thamdrup B, Canfield D, Dalsgeerd T, Rysgaard S, Sejr MK, Strous M, Op den Camp HJ, Jetten MSM (2007) Anaerobic ammonium-oxidizing bacteria in marine environments: widespread occurrence but low diversity. Environ Microbiol 9:1476–1484

    Article  CAS  Google Scholar 

  • Schrum HN, Spivack AJ, Kastner M, D’Hondt S (2009) Sulfate-reducing ammonium oxidation: a thermodynamically feasible metabolic pathway in subseafloor sediment. Geology 37:939–942

    Article  CAS  Google Scholar 

  • Shimamura M, Nishiyama T, Shinya K, Kawahara Y, Furukawa K, Fujii T (2008) Another multiheme protein, hydroxylamine oxidoreductase, abundantly produced in an anammox bacteriumbesides the hydrazine-oxidizing enzyme. J Biosci Bioeng 105:243–248

    Article  CAS  Google Scholar 

  • Sinninghe Damsté JS, Strous M, Rijpstra WIC, Hopmans EC, Geenevasen JAJ, van Diun ACT, van Niftrik L, Jetten MSM (2002) Linearly concatenated cyclobutane lipids form a dense bacterial membrane. Nature 419:708–712

    Article  CAS  Google Scholar 

  • Sinninghe Damsté JS, Rijpstra WIC, Geenevasen JAJ, Strous M, Jetten MSM (2005) Structural identification of ladderane and other membrane lipids of plantomycetes capable of anaerobic ammonium oxidation (anammox). FEBS J 272:4270–4283

    Article  CAS  Google Scholar 

  • Sliekers AO, Third KA, Abma W, Kuenen JG, Jetten MSM (2003) CANON and anammox in a gas-lift reactor. FEMS Microbiol Lett 218:339–344

    Article  CAS  Google Scholar 

  • Speth DR, Lagkouvardos I, Wang Y, Qian P-Y, Dutilh BE, Jetten MSM (2017) Draft genome of Scalindua rubra, obtained from the interface above the discovery deep brine in the Red Sea, sheds light on potential salt adaptation strategies in anammox bacteria. Microb Ecol 74:1–5

    Article  CAS  Google Scholar 

  • Stevenson DS, Dentener FJ, Schultz MG, Ellingsen K, van Noije TPC, Wild O, Zeng G, Amann M, Atherton CS, Bell N, Bergmann DJ, Bey I, Butler T, Cofala J, Collins WJ, Derwent RG, Doherty RM, Drvet J, Eskes HJ, Fiore AM, Gauss M, Hauglustaine DA, Horowitz LW, Isaksen ISA, Krol MC, Lamarque J-F, Lawrence MG, Montanaro V, Müller J-F, Pitari G, Prather MJ, Pyle JA, Rast S, Rodriguez JM, Sanderson MG, Savage NH, Shindell DT, Strahan SE, Sudo K, Szopa S (2006) Multimodel ensemble simulations of present-day and near-future tropospheric ozone. J Geophys Res Atmos 111:D08301

    Article  CAS  Google Scholar 

  • Strous M, Heijnen JJ, Kuenen JG, Jetten MSM (1998) The sequencing batch reactor as a powerful tool for the study of slowly growing anaerobic ammonium-oxidizing microorganisms. Appl Microb Biotechnol 50:589–596

    Article  CAS  Google Scholar 

  • Strous M, Fuerst JA, Kramer EH, Logemann S, Muyzer G, van de Pas-Schoonen KT, Webb R, Kuenen JG, Jetten MSM (1999) Missing lithotroph identified as new planctomycete. Nature 400:446–449

    Article  CAS  Google Scholar 

  • Strous M, Pelletier E, Mangenot S, Rattei T, Lehner A, Taylor MW, Horn M, Daims H, Bartol-Mavel D, Wincker P, Berbe V, Fonknechten N, Vallenet D, Segurens B, Schenowitz-Truong C, Médigue C, Collingro A, Snel B, Dutilh BE, Op del Camp HJM, van der Drift C, Cirpus I, van de Pas-Schoonen KT, Harhangi HR, van Niftrik L, Schmid M, Keltjens J, van de Vossenberg J, Kartal B, Meier H, Frishman D, Huynen MA, Mewes HW, Weissenbach J, Jetten MSM, Wagner M, Le Paslier D (2006) Deciphering the evolution and metabolism of an anammox bacterium from a community genome. Nature 440:790–794

    Article  Google Scholar 

  • Tang CJ, Zheng P, Wang CH, Mahmood Q, Zhang JQ, Chen XG, Zhang L, Chen JW (2011) Performance of high-loaded ANAMMOX UASB reactors containing granular sludge. Water Res 45:135–144

    Article  CAS  Google Scholar 

  • Teixeira C, Magalhaes C, Joye SB, Bordalo AA (2012) Potential rates and environmental controls of anaerobic ammonium oxidation in estuarine sediments. Aquat Micriob Ecol 66:23–32

    Article  Google Scholar 

  • Thamdrup B, Dalsgaard T (2002) Production of N2 through anaerobic ammonium oxidation coupled to nitrate reduction in marine sediments. Appl Environ Microbiol 68:1312–1318

    Article  CAS  Google Scholar 

  • 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 54:577–589

    Article  CAS  Google Scholar 

  • Trimmer M, Engstrøm P, Thamdrup B (2013) Stark contrast in denitrification and anammox across the deep Norwegian Trench in the Skagerrak. Appl Environ Microbiol 79:7381–7389

    Article  CAS  Google Scholar 

  • Valenzuela EI, Prieto-Davó A, López-Lozano NE, Hernández-Eligio A, Vega-Alvarado L, Juárez K, García-González AS, López MG, Cervantes FJ (2017) Anaerobic methane oxidation driven by microbial reduction of natural organic matter in a tropical wetland. Appl Environ Microbiol 83:e00645-17

    Article  Google Scholar 

  • Valenzuela EI, Avendaño KA, Balagurusamy N, Arriaga S, Nieto-Delgado C, Thalasso F, Cervantes FJ (2019) Electron shuttling mediated by humic substances fuels anaerobic methane oxidation and carbon burial in wetland sediments. Sci Total Environ 650:2674–2684

    Article  CAS  Google Scholar 

  • Van de Graaf AA, Mulder A, de Bruijn P, Jetten MSM, Robertson LA, Kuenen JG (1995) Anaerobic oxidation of ammoinium is a biologically mediated process. Appl Environ Microbiol 61:1246–1251

    Google Scholar 

  • Van de Graaf AA, de Bruijn P, Robertson LA, Jetten MSM, Kuenen JG (1996) Autotrophic growth of anaerobic ammonium-oxidizing micro-organisms in a fluidized bed reactor. Microbiology 142:2187–2196

    Article  Google Scholar 

  • Van de Vossenberg J, Rattray JE, Geerts W, Kartal B, van Niftrik L, van Donselaar EG, Sinninghe Damsté JS, Strous M, Jetten MSM (2008) Enrichment and characterization of marine anammox bacteria associated with global nitrogen gas production. Environ Microbiol 10:3120–3129

    Article  CAS  Google Scholar 

  • Van der Star WRL, Abma WR, Blommers D, Mulder JW, Tokutomi T, Strous M, Picioreanu C, van Loosdrecht MCM (2007) Startup of reactors for anoxic ammonium oxidation: experiences from the first full-scale anammox reactor in Rotterdam. Water Res 41:4149–4163

    Article  CAS  Google Scholar 

  • Van der Star WRL, Miclea AI, van Dongen UGJM, Muyzer G, Picioreanu C, van Loosdrecht MCM (2008) The membrane bioreactor: a novel tool to grow anammox bacteria as free cells. Biotechnol Bioeng 101:286–294

    Article  CAS  Google Scholar 

  • Van Dingenen R, Dentener FJ, Raes F, Krol MC, Emberson L, Cofala J (2009) The global impact of ozone on agricultural crop yields under current and future air quality legislation. Atmos Environ 43:604–618

    Article  CAS  Google Scholar 

  • Van Niftrik L, Jetten MSM (2012) Anaerobic ammonium oxidizing bacteria: unique microorganisms with exceptional properties. Microbiol Mol Biol Rev 76:585–596

    Article  CAS  Google Scholar 

  • Van Niftrik L, Fuerst JA, Sinninghe Damsté JS, Kuenen JG, Jetten MSM, Strous M (2004) The anammoxosome: an intracytoplasmic compartment in anammox bacteria. FEMS Microbiol Lett 233:7–13

    Article  CAS  Google Scholar 

  • Van Teeseling MCF, Mesman RJ, Kuru E, Espaillat A, Cava F, Brun YV, VanNieuwenhze MS, Kartal B, van Niftrik L (2015) Anammox planctomycetes have a peptidoglycan cell wall. Nat Commun 6:6878

    Article  CAS  Google Scholar 

  • Wang Z, Ni S-Q, Zhang J, Zhu T, Ma Y, Liu X, Kong Q, Miao M (2016) Gene expression and biomarker discovery of anammox bacteria in different reactors. Biochem Eng J 115:108–114

    Article  CAS  Google Scholar 

  • Woebken D, Lam P, Kuypers MMM, Naqvi SWA, Kartal B, Strous M, Jetten MSM, Fuchs BM, Aman R (2008) A microdiversity study of anammox bacteria reveals a novel Candidatus Scalindua phylotype in marine oxygen minimum zones. Environ Microbiol 10:3106–3119

    Article  CAS  Google Scholar 

  • Yang Z, Zhou S, Sun Y (2009) Start-up of simultaneous removal of ammonium and sulfate from an anaerobic ammonium oxidation (anammox) process in an anaerobic up-flow bioreactor. J Hazard Mater 169:113–118

    Article  CAS  Google Scholar 

  • Yang WH, Weber KA, Silver WL (2012) Nitrogen loss from soil through anaerobic ammonium oxidation coupled to iron reduction. Nat Geosci 5:538–541

    Article  CAS  Google Scholar 

  • Zandt MH, de Jong AEE, Slomp CP, Jetten MSM (2018) The hunt for the most-wanted chemolithoautotrophic spookmicrobes. FEMS Microbiol Ecol 94:fiy064

    Google Scholar 

  • Zhang L, Zheng P, YuHui H, RenCun J (2009) Performance of sulfate-dependent anaerobic ammonium oxidation. Sci China Ser B Chem 52:86–92

    Article  CAS  Google Scholar 

  • Zhao R, Zhang H, Li Y, Jiang T, Yang F (2014) Research of iron reduction and the iron reductase localization of anammox bacteria. Curr Microbiol 69:880–887

    Article  CAS  Google Scholar 

Download references

Acknowledgements

FJC thanks financial support from Council of Science and Technology of Mexico (CONACYT, Grant 1289 from the program Frontiers in Science). EERD thanks CONACYT for the Ph.D. fellowship 250305.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Francisco J. Cervantes.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rios-Del Toro, E.E., Cervantes, F.J. Anaerobic ammonium oxidation in marine environments: contribution to biogeochemical cycles and biotechnological developments for wastewater treatment. Rev Environ Sci Biotechnol 18, 11–27 (2019). https://doi.org/10.1007/s11157-018-09489-3

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11157-018-09489-3

Keywords

Navigation