Skip to main content
SpringerLink
Log in

The history of aerobic ammonia oxidizers: from the first discoveries to today

  • Minireview
  • Published:
Journal of Microbiology Aims and scope Submit manuscript

Abstract

Nitrification, the oxidation of ammonia to nitrite and nitrate, has long been considered a central biological process in the global nitrogen cycle, with its first description dated 133 years ago. Until 2005, bacteria were considered the only organisms capable of nitrification. However, the recent discovery of a chemoautotrophic ammonia-oxidizing archaeon, Nitrosopumilusmaritimus, changed our concept of the range of organisms involved in nitrification, highlighting the importance of ammonia-oxidizing archaea (AOA) as potential players in global biogeochemical nitrogen transformations. The uniqueness of these archaea justified the creation of a novel archaeal phylum, Thaumarchaeota. These recent discoveries increased the global scientific interest within the microbial ecology society and have triggered an analysis of the importance of bacterial vs archaeal ammonia oxidation in a wide range of natural ecosystems. In thismini review we provide a chronological perspective of the current knowledge on the ammonia oxidation pathway of nitrification, based on the main physiological, ecological and genomic discoveries.

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

Refrerences

  • Abeliovich, A. and Vonshak, A. 1992. Anaerobic metabolism of Nitrosomonas europaea. Arch. Microbiol. 158, 267–270.

    CAS  Google Scholar 

  • Ali, T.U., Kim, M., and Kim, D.J. 2013. Selective inhibition of ammonia oxidation and nitrite oxidation linked to N2O emission with activated sludge and enriched nitrifiers. J. Microbiol. Biotechnol. 23, 719–723.

    CAS  PubMed  Google Scholar 

  • Alonso-Saez, L., Waller, A.S., Mende, D.R., Bakker, K., Farnelid, H., Yager, P.L., Lovejoy, C., Tremblay, J.E., Potvin, M., Heinrich, F., and et al. 2012. Role for urea in nitrification by polar marine Archaea. Proc. Natl. Acad. Sci. USA 109, 17989–17994.

    CAS  PubMed Central  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Alzerreca, J.J., Norton, J.M., and Klotz, M.G. 1999. The amo operon in marine, ammonia-oxidizing gamma-proteobacteria. FEMS Microbiol. Lett. 180, 21–29.

    CAS  PubMed  Google Scholar 

  • Arp, D.J., Chain, P.S., and Klotz, M.G. 2007. The impact of genome analyses on our understanding of ammonia-oxidizing bacteria. Annu. Rev. Microbiol. 61, 503–528.

    CAS  PubMed  Google Scholar 

  • Auguet, J.C., Nomokonova, N., Camarero, L., and Casamayor, E.O. 2011. Seasonal changes of freshwater ammonia-oxidizing archaeal assemblages and nitrogen species in oligotrophic alpine lakes. Appl. Environ. Microbiol. 77, 1937–1945.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Baker, B.J., Lesniewski, R.A., and Dick, G.J. 2012. Genome-enabled transcriptomics reveals archaeal populations that drive nitrification in a deep-sea hydrothermal plume. ISME J. 6, 2269–2279.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Bano, N. and Hollibaugh, J.T. 2000. Diversity and distribution of DNA sequences with affinity to ammonia-oxidizing bacteria of the β subdivision of the class proteobacteria in the arctic ocean. Appl. Environ. Microbiol. 66, 1960–1969.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Bartossek, R., Nicol, G.W., Lanzen, A., Klenk, H.P., and Schleper, C. 2010. Homologues of nitrite reductases in ammonia-oxidizing archaea: diversity and genomic context. Environ. Microbiol. 12, 1075–1088.

    CAS  PubMed  Google Scholar 

  • Beaumont, H.J.E., Hommes, N.G., Sayavedra-Soto, L.A., Arp, D.J., Arciero, D.M., Hooper, A.B., Westerhoff, H.V., and van Spanning, R.J.M. 2002. Nitrite reductase of Nitrosomonas europaea is not essential for production of gaseous nitrogen oxides and confers tolerance to nitrite. J. Bacteriol. 184, 2557–2560.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Beman, J.M. and Francis, C.A. 2006. Diversity of ammonia-oxidizing archaea and bacteria in the sediments of a hypernutrified subtropical estuary: Bahia del Tobari, Mexico. Appl. Environ. Microbiol. 72, 7767–7777.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Bergmann, D.J. and Hooper, A.B. 1994. Sequence of the gene, amo B, for the 43-kDa polypeptide of ammonia monoxygenase of Nitrosomonas europaea. Biochem. Biophys. Res. Commun. 204, 759–762.

    CAS  PubMed  Google Scholar 

  • Bergmann, D.J., Hooper, A.B., and Klotz, M.G. 2005. Structure and sequence conservation of hao cluster genes of autotrophic ammonia-oxidizing bacteria: evidence for their evolutionary history. Appl. Environ. Microbiol. 71, 5371–5382.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Bhandari, B. and Nicholas, D. 1981. Some properties of glutamine synthetase from the nitrifying bacteriumNitrosomonas europaea. Aust. J. Biol. Sci. 34, 527–540.

    CAS  PubMed  Google Scholar 

  • Biller, S.J., Mosier, A.C., Wells, G.F., and Francis, C.A. 2012. Global biodiversity of aquatic ammonia-oxidizing archaea is partitioned by habitat. Front. Microbiol. 3, 2–2.

    Google Scholar 

  • Blainey, P.C., Mosier, A.C., Potanina, A., Francis, C.A., and Quake, S.R. 2011. Genome of a low-salinity ammonia-oxidizing archaeondetermined by single-cell and metagenomic analysis. PLoS ONE 6, 166–6.

    Google Scholar 

  • Bock, E., Koops, H.P., and Harms, H. 1986. Cell biology of nitrifying bacteria, pp. 17-38. In Prosser, J.I. (ed.), Nitrification. Society for General Microbiology, IRL Press, Oxford.

    Google Scholar 

  • Bock, E. and Wagner, M. 2006. Oxidation of inorganic nitrogen compounds as an energy source. Prokaryotes 2, 457–495.

    Google Scholar 

  • Bothe, H., Jost, G., Schloter, M., Ward, B.B., and Witzel, K.P. 2000. Molecular analysis of ammonia oxidation and denitrification in natural environments. FEMS Microbiol. Rev. 24, 673–690.

    CAS  PubMed  Google Scholar 

  • Brochier-Armanet, C., Boussau, B., Gribaldo, S., and Forterre, P. 2008. Mesophilic Crenarchaeota: proposal for a third archaeal phylum, the Thaumarchaeota. Nature Rev.Microbiol. 6, 245–252.

    CAS  Google Scholar 

  • Brochier-Armanet, C., Gribaldo, S., and Forterre, P. 2012. Spotlight on the Thaumarchaeota. ISME J. 6, 227–230.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Burrell, P.C., Phalen, C.M., and Hovanec, T.A. 2001. Identification of bacteria responsible for ammonia oxidation in freshwater aquaria. Appl. Environ. Microbiol. 67, 5791–5800.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Caffrey, J.M., Bano, N., Kalanetra, K., and Hollibaugh, J.T. 2007. Ammonia oxidation and ammonia-oxidizing bacteria and archaea from estuaries with differing histories of hypoxia. ISME J. 1, 660–662.

    PubMed  Google Scholar 

  • Caffrey, J.M., Harrington, N., Solem, I., and Ward, B.B. 2003. Biogeochemical processes in a small California estuary. 2. Nitrification activity, community structure and role in nitrogen budgets. Mar. Ecol. Prog. Ser. 248, 27–40.

    CAS  Google Scholar 

  • Calvo, L. and Garcia-Gil, L.J. 2004. Use of amoB as a new molecular marker for ammonia-oxidizing bacteria. J. Microbiol. Methods 57, 69–78.

    CAS  PubMed  Google Scholar 

  • Cebron, A., Berthe, T., and Garnier, J. 2003. Nitrification and nitrifying bacteria in the lower Seine River and estuary (France). Appl. Environ. Microbiol. 69, 7091–7100.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Chain, P., Lamerdin, J., Larimer, F., Regala, W., Lao, V., Land, M., Hauser, L., Hooper, A., Klotz, M., Norton, J., and et al. 2003. Complete genome sequence of the ammonia-oxidizing bacterium and obligate chemolithoautotroph Nitrosomonas europaea. J. Bacteriol. 185, 2759–2773.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Clark, C. and Schmidt, E.L. 1967. Growth response of Nitrosomonas europaea to amino acids. J. Bacteriol. 93, 1302–1308.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Damste, J.S., Rijpstra, W.I., Hopmans, E.C., Jung, M.Y., Kim, J.G., Rhee, S.K., Stieglmeier, M., and Schleper, C. 2012. Intact polar and core glycerol dibiphytanyl glycerol tetraether lipids of group I.1a and I.1b thaumarchaeota in soil. Appl. Environ. Microbiol. 78, 6866–6874.

    CAS  PubMed  Google Scholar 

  • Dang, H., Zhang, X., Sun, J., Li, T., Zhang, Z., and Yang, G. 2008. Diversity and spatial distribution of sediment ammonia-oxidizing crenarchaeota in response to estuarine and environmental gradients in the Changjiang Estuary and East China Sea. Microbiology 154, 2084–2095.

    CAS  PubMed  Google Scholar 

  • de la Torre, J.R., Walker, C.B., Ingalls, A.E., Konneke, M., and Stahl, D.A. 2008. Cultivation of a thermophilic ammonia oxidizing archaeon synthesizing crenarchaeol. Environ. Microbiol. 10, 810–818.

    CAS  PubMed  Google Scholar 

  • Di, H.J., Cameron, K.C., Shen, J.P., Winefield, C.S., Ocallaghan, M., Bowatte, S., and He, J.Z. 2009. Nitrification driven by bacteria and not archaea in nitrogen-rich grassl and soils. Nat. Geosci. 2, 621–624.

    CAS  Google Scholar 

  • Fernandez-Guerra, A. and Casamayor, E.O. 2012. Habitat-associated phylogenetic community patterns of microbial ammonia oxidizers. PLoS ONE 7, e473-0.

    Google Scholar 

  • Francis, C.A., O’Mullan, G.D., and Ward, B.B. 2003. Diversity of ammonia monooxygenase (amoA) genes across environmental gradients in Chesapeake Bay sediments. Geobiology 1, 129–140.

    CAS  Google Scholar 

  • Francis, C.A., Roberts, K.J., Beman, J.M., Santoro, A.E., and Oakley, B.B. 2005. Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean. Proc. Natl. Acad. Sci. USA 102, 14683–14688.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Freitag, T.E. and Prosser, J.I. 2003. Community structure of ammonia-oxidizing bacteria within anoxic marine sediments. Appl. Environ. Microbiol. 69, 1359–1371.

    CAS  PubMed Central  PubMed  Google Scholar 

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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Gubry-Rangin, C., Nicol, G.W., and Prosser, J.I. 2010. Archaea rather than bacteria control nitrification in two agricultural acidic soils. FEMS Microbiol. Ecol. 74, 566–574.

    CAS  PubMed  Google Scholar 

  • Hallam, S.J., Konstantinidis, K.T., Putnam, N., Schleper, C., Watanabe, Y., Sugahara, J., Preston, C., de la Torre, J., Richardson, P.M., and DeLong, E.F. 2006a. Genomic analysis of the uncultivated marine crenarchaeote Cenarchaeum symbiosum. Proc. Natl. Acad. Sci. USA 103, 18296–18301.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hallam, S.J., Mincer, T.J., Schleper, C., Preston, C.M., Roberts, K., Richardson, P.M., and DeLong, E.F. 2006b. Pathways of carbon assimilation and ammonia oxidation suggested by environmental genomic analyses of marine Crenarchaeota. PLoS Biol. 4, e95.

    Google Scholar 

  • Harms, G., Layton, A.C., Dionisi, H.M., Gregory, I.R., Garrett, V.M., Hawkins, S.A., Robinson, K.G., and Sayler, G.S. 2003. Real-time PCR quantification of nitrifying bacteria in a municipal wastewater treatment plant. Environ. Sci. Technol. 37, 343–351.

    CAS  PubMed  Google Scholar 

  • Hashimoto, L., Kaplan, W., Wofsy, S., and McElroy, M. 1983. Transformations of fixed nitrogen and N2O in the Cariaco Trench. Deep-Sea Res. Oceanogr. A 30, 575–590.

    CAS  Google Scholar 

  • Hatzenpichler, R. 2012. Diversity, physiology, and niche differentiation of ammonia-oxidizing archaea. Appl. Environ. Microbiol. 78, 7501–7510.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hatzenpichler, R., Lebedeva, E.V., Spieck, E., Stoecker, K., Richter, A., Daims, H., and Wagner, M. 2008. A moderately thermophilic ammonia-oxidizing crenarchaeote from a hot spring. Proc. Natl. Acad. Sci. USA 105, 2134–2139.

    CAS  PubMed Central  PubMed  Google Scholar 

  • He, J.Z., Hu, H.W., and Zhang, L.M. 2012. Current insights into the autotrophic thaumarchaeal ammonia oxidation in acidic soils. Soil Biol. Biochem. 55, 146–154.

    CAS  Google Scholar 

  • Head, I.M., Hiorns, W.D., Embley, T.M., McCarthy, A.J., and Saunders, J.R. 1993. The phylogeny of autotrophic ammoniaoxidizing bacteria as determined by analysis of 16S ribosomal RNA gene sequences. J. Gen. Microbiol. 139, 1147–1153.

    CAS  PubMed  Google Scholar 

  • Hermansson, A. and Lindgren, P.E. 2001. Quantification of ammonia-oxidizing bacteria in arable soil by real-time PCR. Appl. Environ. Microbiol. 67, 972–976.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hollibaugh, J.T., Bano, N., and Ducklow, H.W. 2002. Widespread distribution in polar oceans of a 16S rRNA gene sequence with affinity to nitrosospira-like ammonia-oxidizing bacteria. Appl. Environ. Microbiol. 68, 1478–1484.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hommes, N.G., Sayavedra-Soto, L.A., and Arp, D.J. 1994. Sequence of hcy, a gene encoding cytochrome c 554 from Nitrosomonas europaea. Gene 146, 87–89.

    CAS  PubMed  Google Scholar 

  • Horz, H.P., Barbrook, A., Field, C.B., and Bohannan, B.J.M. 2004. Ammonia-oxidizing bacteria respond to multifactorial global change. Proc. Natl. Acad. Sci. USA 101, 15136–15141.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Houzeau, A. 1872. Faits pour servir a l’histoire de la nitrification, composition des terreaux de tantah (basse-égypte). Ann. Chim. Phys. 25, 161–167.

    Google Scholar 

  • Hyman, M.R. and Arp, D.J. 1992. 14C2H2- and 14CO2-labeling studies of the de novo synthesis of polypeptides by Nitrosomonas europaea during recovery from acetylene and light inactivation of ammonia monooxygenase. J. Biol. Chem. 267, 1534–1545.

    CAS  PubMed  Google Scholar 

  • Jia, Z. and Conrad, R. 2009. Bacteria rather than Archaea dominate microbial ammonia oxidation in an agricultural soil. Environ. Microbiol. 11, 1658–1671.

    CAS  PubMed  Google Scholar 

  • Juliette, L.Y., Hyman, M.R., and Arp, D.J. 1993. Inhibition of ammonia oxidation in Nitrosomonas europaea by sulfur compounds: Thioethers are oxidized to sulfoxides by ammoniamonooxygenase. Appl. Environ. Microbiol. 59, 3718–3727.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Jung, M.Y., Park, S.J., Min, D., Kim, J.S., Rijpstra, W.I., Sinninghe Damste, J.S., Kim, G.J., Madsen, E.L., and Rhee, S.K. 2011. Enrichment and characterization of an autotrophic ammoniaoxidizing archaeon of mesophilic crenarchaeal group I.1a from an agricultural soil. Appl. Environ. Microbiol. 77, 8635–8647.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Jung, M.Y., Well, R., Min, D., Giesemann, A., Park, S.J., Kim, J.G., Kim, S.J., and Rhee, S.K. 2014. Isotopic signatures of N2O produced by ammonia-oxidizing archaea from soils. ISME J. 8, 1115–1125.

    CAS  PubMed  Google Scholar 

  • Junier, P., Molina, V., Dorador, C., Hadas, O., Kim, O.S., Junier, T., Witzel, J.P., and Imhoff, J.F. 2010. Phylogenetic and functional marker genes to study ammonia-oxidizing microorganisms (AOM) in the environment. Appl. Microbiol. Biotechnol. 85, 425–440.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kalanetra, K.M., Bano, N., and Hollibaugh, J.T. 2009. Ammoniaoxidizing Archaea in the Arctic Ocean and Antarctic coastal waters. Environ. Microbiol. 11, 2434–2445.

    CAS  PubMed  Google Scholar 

  • Kim, B.K., Jung, M.Y., Yu, D.S., Park, S.J., Oh, T.K., Rhee, S.K., and Kim, J.F. 2011. Genome sequence of an ammonia-oxidizing soil archaeon, “Candidatus Nitrosoarchaeum koreensis” MY1. J. Bacteriol. 193, 5539–5540.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Könneke, M., Bernhard, A.E., de la Torre, J.R., Walker, C.B., Waterbury, J.B., and Stahl, D.A. 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., and Wagner, M. 2006. The lithoautotrophic ammonia-oxidizing bacteria. The Prokaryotes 5, 778–811.

    Google Scholar 

  • Kowalchuk, G.a. and Stephen, J.R. 2001. Ammonia-oxidizing bacteria: a model for molecular microbial ecology. Annu. Rev. Microb. 55, 485–529.

    CAS  Google Scholar 

  • Lam, P., Jensen, M.M., Lavik, G., McGinnis, D.F., Muller, B., Schubert, C.J., Amann, R., Thamdrup, B., and Kuypers, M.M. 2007. Linking crenarchaeal and bacterial nitrification to anammox in the Black Sea. Proc. Natl. Acad. Sci. USA 104, 7104–7109.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lebedeva, E.V., Hatzenpichler, R., Pelletier, E., Schuster, N., Hauzmayer, S., Bulaev, A., Grigor’eva, N.V., Galushko, A., Schmid, M., Palatinszky, M., and et al. 2013. Enrichment and genome sequence of the group I.1a ammonia-oxidizing Archaeon “Ca. Nitrosotenuis uzonensis” representing a clade globally distributed in thermal habitats. PLoS ONE 8, e808-5.

    Google Scholar 

  • Leininger, S., Urich, T., Schloter, M., Schwark, L., Qi, J., Nicol, G.W., Prosser, J.I., Schuster, S.C., and Schleper, C. 2006. Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 442, 806–809.

    CAS  PubMed  Google Scholar 

  • Limpiyakorn, T., Shinohara, Y., Kurisu, F., and Yagi, O. 2005. Communities of ammonia-oxidizing bacteria in activated sludge of various sewage treatment plants in Tokyo. FEMS Microbiol. Ecol. 54, 205–217.

    CAS  PubMed  Google Scholar 

  • Löscher, C.R., Kock, A., Könneke, M., LaRoche, J., Bange, H.W., and Schmitz, R.A. 2012. Production of oceanic nitrous oxide by ammonia-oxidizing archaea. Biogeosciences 9, 2419–2429.

    Google Scholar 

  • Lu, L. and Jia, Z. 2012. Urease gene-containing Archaea dominate autotrophic ammonia oxidation in two acid soils. Environ. Microbiol. 15, 1–15.

    Google Scholar 

  • Luo, H., Tolar, B.B., Swan, B.K., Zhang, C.L., Stepanauskas, R., Moran, M.A., and Hollibaugh, J.T. 2014. Single cell genomics shedding light on marine Thaumarchaeota diversification. ISME J. doi:10.1038/ismej.2013-202.

    Google Scholar 

  • Magalhaes, C., Bano, N., Wiebe, W.J., Hollibaugh, J.T., and Bordalo, A.A. 2007. Composition and activity of beta-Proteobacteria ammonia-oxidizing communities associated with intertidal rocky biofilms and sediments of the Douro River estuary, Portugal. J. Appl. Microbiol. 103, 1239–1250.

    CAS  PubMed  Google Scholar 

  • Magalhães, C.M., Machado, A., and Bordalo, A.A. 2009. Temporal variability in the abundance of ammonia-oxidizing bacteria vs. archaea in sandy sediments of the Douro River estuary, Portugal. Aquat. Microb. Ecol. 56, 13.

    Google Scholar 

  • Martens-Habbena, W., Berube, P.M., Urakawa, H., de la Torre, J.R., and Stahl, D.A. 2009. Ammonia oxidation kinetics determine niche separation of nitrifying Archaea and Bacteria. Nature 461, 976–979.

    CAS  PubMed  Google Scholar 

  • Martens-Habbena, W. and Stahl, D.A. 2011. Nitrogen metabolism and kinetics of ammonia-oxidizing archaea. Methods Enzymol. 496, 465–487.

    CAS  PubMed  Google Scholar 

  • McCaig, A.E., Phillips, C.J., Stephen, J.R., Kowalchuk, G.A., Martyn Harvey, S., Herbert, R.A., Martin Embley, T., and Prosser, J.I. 1999. Nitrogen cycling and community structure of proteobacterial β-subgroup ammonia-oxidizing bacteria within polluted marine fish farm sediments. Appl. Environ. Microbiol. 65, 213–20.

    CAS  PubMed Central  PubMed  Google Scholar 

  • McTavish, H., Fuchs, J.A., and Hooper, A.B. 1993. Sequence of the gene coding for ammonia monooxygenase in Nitrosomonas europaea. J. Bacteriol. 175, 2436–2444.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Molina, V., Belmar, L., and Ulloa, O. 2010. High diversity of ammonia-oxidizing archaea in permanent and seasonal oxygendeficient waters of the eastern South Pacific. Environ. Microbiol. 12, 2450–2465.

    CAS  PubMed  Google Scholar 

  • Mosier, A.C. and Francis, C.A. 2008. Relative abundance and diversity of ammonia-oxidizing archaea and bacteria in the San Francisco Bay estuary. Environ. Microbiol. 10, 3002–3016.

    CAS  PubMed  Google Scholar 

  • Mosier, A.C., Lund, M.B., and Francis, C.A. 2012. Ecophysiology of an ammonia-oxidizing archaeon adapted to low-salinity habitats. Microb. Ecol. 64, 955–963.

    CAS  PubMed  Google Scholar 

  • Müller, A. 1873. Landw. Versuchs-Stationen. xvi p. 2–3.

    Google Scholar 

  • Mußmann, M., Brito, I., Pitcher, A., Damsté, J.S.S., Hatzenpichler, R., Richter, A., Nielsen, J.L., Nielsen, P.H., Müller, A., and Daims, H. 2011. Thaumarchaeotes abundant in refinery nitrifying sludges express amoA but are not obligate autotrophic ammonia oxidizers. Proc. Natl. Acad. Sci. USA 108, 16771–16776.

    PubMed Central  PubMed  Google Scholar 

  • Nicol, G.W., Leininger, S., Schleper, C., and Prosser, J.I. 2008. The influence of soil pH on the diversity, abundance and transcriptional activity of ammonia oxidizing archaea and bacteria. Environ. Microbiol. 10, 2966–2978.

    CAS  PubMed  Google Scholar 

  • Norton, J.M., Alzerreca, J.J., Suwa, Y., and Klotz, M.G. 2002. Diversity of ammonia monooxygenase operon in autotrophic ammonia- oxidizing bacteria. Arch. Microbiol. 177, 139–149.

    CAS  PubMed  Google Scholar 

  • O’Mullan, G.D. and Ward, B.B. 2005. Relationship of temporal and spatial variabilities of ammonia-oxidizing bacteria to nitrification rates in Monterey Bay, California. Appl. Environ. Microbiol. 71, 697–705.

    PubMed Central  PubMed  Google Scholar 

  • Offre, P., Nicol, G.W., and Prosser, J.I. 2011. Community profiling and quantification of putative autotrophic thaumarchaeal communities in environmental samples. Environ. Microbiol. Rep. 3, 245–253.

    PubMed  Google Scholar 

  • Olson, R.J. 1981. 15N tracer studies of the primary nitrite maximum. J. Mar. Res. 39, 203–226.

    CAS  Google Scholar 

  • Omeliansky, V. 1899. Ueber die Isolierung der Nitrifikations-mikroben aus dem Erdboden. Zentr. Bakteriol. Parasitenk. Abt. II 5, 587

    Google Scholar 

  • Park, B.J., Park, S.J., Yoon, D.N., Schouten, S., Sinninghe Damste, J.S., and Rhee, S.K. 2010. Cultivation of autotrophic ammoniaoxidizing archaea from marine sediments in coculture with sulfur-oxidizing bacteria. Appl. Environ. Microbiol. 76, 7575–7587.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Park, H.D., Wells, G.F., Bae, H., Criddle, C.S., Francis, C.A., and Francis, C.A. 2006. Occurrence of ammonia-oxidizing archaea in wastewater treatment plant bioreactors. Appl. Environ. Microbiol. 72, 5643–5647.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Pedneault, E., Galand, P.E., Polvin, M., Tremblay, J.E., and Lovejoy, C. 2014. Archaeal amoA and ureC genes and their transcriptional activity in the Arctic Ocean. Sci. Rep. 4, 46–1.

    Google Scholar 

  • Pester, M., Rattei, T., Flechl, S., Gröngröft, A., Richter, A., Overmann, J., Reinhold-Hurek, B., Loy, A., and Wagner, M. 2012. amoA-based consensus phylogeny of ammonia-oxidizing archaea and deep sequencing of amoA genes from soils of four different geographic regions. Environ. Microbiol. 14, 525–539.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Pester, M., Schleper, C., and Wagner, M. 2011. The Thaumarchaeota: an emerging view of their phylogeny and ecophysiology. Curr. Opin. Microbiol. 14, 300–306.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Pitcher, A., Schouten, S., and Sinninghe Damste, J.S. 2009. In situ production of crenarchaeol in two california hot springs. Appl. Environ. Microbiol. 75, 4443–4451.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Pommerening-Röser, A., Rath, G., and Koops, H.P. 1996. Phylogenetic diversity within the genus Nitrosomonas. Syst. Appl. Microbiol. 19, 344–351.

    Google Scholar 

  • Pratscher, J., Dumont, M.G., and Conrad, R. 2011. Ammonia oxidation coupled to CO2 fixation by archaea and bacteria in an agricultural soil. Proc. Natl. Acad. Sci. USA 108, 4170–4175.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Prosser, J.I. and Nicol, G.W. 2012. Archaeal and bacterial ammoniaoxidisers in soil: the quest for niche specialisation and differentiation. Trends Microbiol. 20, 523–531.

    CAS  PubMed  Google Scholar 

  • Purkhold, U., Pommerening-Röser, A., Juretschko, S., Schmid, M.C., Koops, H.P., and Wagner, M. 2000. Phylogeny of all recognized species of ammonia oxidizers based on comparative 16S rRNA and amoA sequence analysis: Implications for molecular diversity surveys. Appl. Environ. Microbiol. 66, 5368–5382.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Purkhold, U., Wagner, M., Timmermann, G., Pommerening-Röser, A., and Koops, H.P. 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.

    CAS  PubMed  Google Scholar 

  • Ritchie, G. and Nicholas, D. 1974. The partial characterization of purified nitrite reductase and hydroxylamine oxidase from Nitrosomonas europaea. Biochem. J. 138, 471–480.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Rotthauwe, J.H., Witzel, K.P., and Liesack, W. 1997. The ammonia monooxygenase structural gene amoA as a functional marker: Molecular fine-scale analysis of natural ammonia-oxidizing populations. Appl. Environ. Microbiol. 63, 4704–4712.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Santoro, A.E., Buchwald, C., McIlvin, M.R., and Casciotti, K.L. 2011. Isotopic signature of N2O produced by marine ammoniaoxidizing archaea. Science 333, 1282–1285.

    CAS  PubMed  Google Scholar 

  • Santoro, A.E., Casciotti, K.L., and Francis, C.A. 2010. Activity, abundance and diversity of nitrifying archaea and bacteria in the central California Current. Environ. Microbiol. 12, 1989–2006.

    CAS  PubMed  Google Scholar 

  • Santoro, A.E., Francis, C.A., de Sieyes, N.R., and Boehm, A.B. 2008. Shifts in the relative abundance of ammonia-oxidizing bacteria and archaea across physicochemical gradients in a subterranean estuary. Environ. Microbiol. 10, 1068–1079.

    CAS  PubMed  Google Scholar 

  • Schauss, K., Focks, A., Leininger, S., Kotzerke, A., Heuer, H., Thiele-Bruhn, S., Sharma, S., Wilke, B.M., Matthies, M., Smalla, K., and et al. 2009. Dynamics and functional relevance of ammonia-oxidizing archaea in two agricultural soils. Environ. Microbiol. 11, 446–456.

    CAS  PubMed  Google Scholar 

  • Schleper, C., Jurgens, G., and Jonuscheit, M. 2005. Genomic studies of uncultivated archaea. Nature Rev. Microb. 3, 479–488.

    CAS  Google Scholar 

  • Schleper, C. and Nicol, G.W. 2010. Ammonia-oxidising archaea-physiology, ecology and evolution. Adv. Microb. Physiol. 57, 1–41.

    CAS  PubMed  Google Scholar 

  • Schloesing, T. and Müntz, N.T.Z. 1877. Sur la nitrification par les ferments organises. Comptes Rendus Ebdomadaire des Seánces de l’Academie des Sciences (Paris) 85, 1018–1020.

    Google Scholar 

  • Schmid, M.C., Hooper, A.B., Klotz, M.G., Woebken, D., Lam, P., Kuypers, M.M.M., Pommerening-Roeser, A., Op Den Camp, H.J.M., and Jetten, M.S.M. 2008. Environmental detection of octahaem cytochrome c hydroxylamine/hydrazine oxidoreductase genes of aerobic and anaerobic ammonium-oxidizing bacteria. Environ. Microbiol. 10, 3140–3149.

    CAS  PubMed  Google Scholar 

  • Schouten, S., Hopmans, E.C., Baas, M., Boumann, H., Standfest, S., Könneke, M., Stahl, D.A., and Damsté, J.S.S. 2008. Intact membrane lipids of “Candidatus Nitrosopumilus maritimus,” a cultivated representative of the cosmopolitan mesophilic group I crenarchaeota. Appl. Environ. Microbiol. 74, 2433–2440.

    CAS  PubMed Central  PubMed  Google Scholar 

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

    CAS  Google Scholar 

  • Schramm, A., De Beer, D., Van Den Heuvel, J.C., Ottengraf, S., and 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.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Shen, T., Stieglmeier, M., Dai, J., Urich, T., and Schleper, C. 2013. Responses of the terrestrial ammonia-oxidizing archaeon Ca. Nitrososphaera viennensis and the ammonia-oxidizing bacterium Nitrosospira multiformis to nitrification inhibitors. FEMS Microbiol. Lett. 344, 121–129.

    CAS  Google Scholar 

  • Sinigalliano, C.D., Kuhn, D.N., and Jones, R.D. 1995. Amplification of the amoA gene from diverse species of ammonium-oxidizing bacteria and from an indigenous bacterial population from seawater. Appl. Environ. Microbiol. 61, 2702–2706.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Spang, A., Hatzenpichler, R., Brochier-Armanet, C., Rattei, T., Tischler, P., Spieck, E., Streit, W., Stahl, D.A., Wagner, M., and Schleper, C. 2010. Distinct gene set in two different lineages of ammonia-oxidizing archaea supports the phylum Thaumarchaeota. Trends Microbiol. 18, 331–340.

    CAS  PubMed  Google Scholar 

  • Spang, A., Poehlein, A., Offre, P., Zumbrägel, S., Haider, S., Rychlik, N., Nowka, B., Schmeisser, C., Lebedeva, E.V., and Rattei, T. 2012. The genome of the ammonia-oxidizing Candidatus Nitrososphaera gargensis: insights into metabolic versatility and environmental adaptations. Environ. Microbiol. 14, 3122–3145.

    CAS  PubMed  Google Scholar 

  • Stahl, D.A. and de la Torre, J.R. 2012. Physiology and diversity of ammonia-oxidizing archaea. Annu. Rev. Microbiol. 66, 83–101.

    CAS  PubMed  Google Scholar 

  • Stehr, G., Böttcher, B., Dittberner, P., Rath, G., and Koops, H.P. 1995. The ammonia-oxidizing nitrifying population of the River Elbe estuary. FEMS Microbiol. Ecol. 17, 177–186.

    CAS  Google Scholar 

  • Stephen, J.R., McCaig, A.E., Smith, Z., Prosser, J.I., and Embley, T.M. 1996. Molecular diversity of soil and marine 16S rRNA gene sequences related to beta-subgroup ammonia-oxidizing bacteria. Appl. Environ. Microbiol. 62, 4147–4154.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Stieglmeier, M., Mooshammer, M., Kitzler, B., Wanek, W., Zechmeister-Boltenstern, S., Richter, A., and Schleper, C. 2014. Aerobic nitrous oxide production through N-nitrosating hybrid formation in ammonia-oxidizing archaea. ISME J. 8, 1135–1146.

    CAS  PubMed  Google Scholar 

  • Teske, A., Alm, E., Regan, J., Toze, S., Rittmann, B., and Stahl, D. 1994. Evolutionary relationships among ammonia- and nitriteoxidizing bacteria. J. Bacteriol. 176, 6623–6630.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Tourna, M., Stieglmeier, M., Spang, A., Konneke, M., Schintlmeister, A., Urich, T., Engel, M., Schloter, M., Wagner, M., Richter, A., and et al. 2011. Nitrososphaera viennensis, an ammonia oxidizing archaeon from soil. Proc. Natl. Acad. Sci. USA 108, 8420–8425.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Treusch, A.H., Leininger, S., Kletzin, A., Schuster, S.C., Klenk, H.P., and 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.

    CAS  PubMed  Google Scholar 

  • Urakawa, H., Kurata, S., Fujiwara, T., Kuroiwa, D., Maki, H., Kawabata, S., Hiwatari, T., Ando, H., Kawai, T., Watanabe, M., and et al. 2006. Characterization and quantification of ammonia-oxidizing bacteria in eutrophic coastal marine sediments using polyphasic molecular approaches and immunofluorescence staining. Environ. Microbiol. 8, 787–803.

    CAS  PubMed  Google Scholar 

  • Vajrala, N., Martens-Habbena, W., Sayavedra-Soto, L.A., Schauer, A., Bottomley, P.J., Stahl, D.A., and Arp, D.J. 2013. Hydroxylamine as an intermediate in ammonia oxidation by globally abundant marine archaea. Proc. Natl. Acad. Sci. USA 110, 1006–1011.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Venter, J.C., Remington, K., Heidelberg, J.F., Halpern, A.L., Rusch, D., Eisen, J.A., Wu, D., Paulsen, I., Nelson, K.E., Nelson, W., and et al. 2004. Environmental genome shotgun sequencing of the Sargasso Sea. Science 304, 66–74.

    CAS  PubMed  Google Scholar 

  • Voytek, M. and Ward, B. 1995. Detection of ammonium-oxidizing bacteria of the beta-subclass of the class Proteobacteria in aquatic samples with the PCR. Appl. Environ. Microbiol. 61, 1444–1450.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wagner, M. 2009. Single-cell ecophysiology of microbes as revealed by Raman microspectroscopy or secondary ion mass spectrometry imaging. Annu. Rev. Microbiol. 63, 411–429.

    CAS  PubMed  Google Scholar 

  • Walker, C.B., de la Torre, J.R., Klotz, M.G., Urakawa, H., Pinel, N., Arp, D.J., Brochier-Armanet, C., Chain, P.S., Chan, P.P., Gollabgir, A., and et al. 2010. Nitrosopumilus maritimus genome reveals unique mechanisms for nitrification and autotrophy in globally distributed marine crenarchaea. Proc. Natl. Acad. Sci. USA 107, 8818–8823.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Warington, R. 1878. On nitrification (Part II.). J. Chem. Soc. 33, 44–51.

    CAS  Google Scholar 

  • Warington, R. 1891. On nitrification (Part IV.). J. Chem. Soc. 59, 484.

    CAS  Google Scholar 

  • Winogradsky, S. 1890. Recherches sur les organismes de la nitrification. Ann. Inst. Pasteur 4, 213–331.

    Google Scholar 

  • Winogradsky, S. 1904. Die Nitrifikation, Vol. III, pp. 1904–1906. Handbuch derTechnischen Mykologie. In Lafar F. (ed.), Jena: Gustav-Fischer.

    Google Scholar 

  • Wuchter, C., Abbas, B., Coolen, M.J., Herfort, L., van Bleijswijk, J., Timmers, P., Strous, M., Teira, E., Herndl, G.J., Middelburg, J.J., and et al. 2006. Archaeal nitrification in the ocean. Proc. Natl. Acad. Sci. USA 103, 12317–12322.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Yan, J., Haaijer, S.C., Op den Camp, H.J., van Niftrik, L., Stahl, D.A., Konneke, M., Rush, D., Sinninghe Damste, J.S., Hu, Y.Y., and Jetten, M.S. 2012. Mimicking the oxygen minimum zones: stimulating interaction of aerobic archaeal and anaerobic bacterial ammonia oxidizers in a laboratory-scale model system. Environ. Microbiol. 14, 3146–3158.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Yao, H., Gao, Y., Nicol, G.W., Campbell, C.D., Prosser, J.I., Zhang, L., Han, W., and Singh, B.K. 2011. Links between ammonia oxidizer community structure, abundance, and nitrification potential in acidic soils. Appl. Environ. Microbiol. 77, 4618–4625.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zehr, J.P. and Ward, B.B. 2002. Nitrogen cycling in the ocean: new perspectives on processes and paradigms. Appl. Environ. Microbiol. 68, 1015–1024.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zhang, L.M., Hu, H.W., Shen, J.P., and He, J.Z. 2012. Ammoniaoxidizing archaea have more important role than ammonia-oxidizing bacteria in ammonia oxidation of strongly acidic soils. ISME J. 6, 1032–1045.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zhang, C.L., Pearson, A., Li, Y.L., Mills, G., and Wiegel, J. 2006. Thermophilic temperature optimum for crenarchaeol synthesis and its implication for archaeal evolution. Appl. Environ. Microbiol. 72, 4419–4422.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zhang, L.M., Wang, M., Prosser, J.I., Zheng, Y.M., and He, J.Z. 2009. Altitude ammonia-oxidizing bacteria and archaea in soils of Mount Everest. FEMS Microbiol. Ecol. 70, 208–217.

    CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. EcoBioTec Laboratory, Interdisciplinary Centre of Marine and Environmental Research (CIIMAR/CIMAR), University of Porto, Rua dos Bragas 289, P 4050-123, Porto, Portugal

    Maria Monteiro, Joana Séneca & Catarina Magalhães

Authors
  1. Maria Monteiro
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Joana Séneca
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Catarina Magalhães
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Catarina Magalhães.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Monteiro, M., Séneca, J. & Magalhães, C. The history of aerobic ammonia oxidizers: from the first discoveries to today. J Microbiol. 52, 537–547 (2014). https://doi.org/10.1007/s12275-014-4114-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12275-014-4114-0

Keywords

Search

Navigation