Abstract
Anaerobic ammonium oxidation (anammox) is a relatively new pathway within the N cycle discovered in the late 1990s. This eminent discovery not only modified the classical theory of biological metabolism and matter cycling, but also profoundly influenced our understanding of the energy sources for life. A new member of chemolithoautotrophic microorganisms capable of carbon fixation was found in the vast deep dark ocean. If the discovery of the chemosynthetic ecosystems in the deep-sea hydrothermal vent environments once challenged the old dogma “all living things depend on the sun for growth,” the discovery of anammox bacteria that are widespread in anoxic environments fortifies the victory over this dogma. Anammox bacteria catalyze the oxidization of NH4 + by using NO2 - as the terminal electron acceptor to produce N2. Similar to the denitrifying microorganisms, anammox bacteria play a biogeochemical role of inorganic N removal from the environment. However, unlike heterotrophic denitrifying bacteria, anammox bacteria are chemolithoautotrophs that can generate transmembrane proton motive force, synthesize ATP molecules and further carry out CO2 fixation through metabolic energy harvested from the anammox process. Although anammox bacteria and the subsequently found ammonia-oxidizing archaea (AOA), another very important group of N cycling microorganisms are both chemolithoautotrophs, AOA use ammonia rather than ammonium as the electron donor and O2 as the terminal electron acceptor in their energy metabolism. Therefore, the ecological process of AOA mainly takes place in oxic seawater and sediments, while anammox bacteria are widely distributed in anoxic water and sediments, and even in some typical extreme marine environments such as the deep-sea hydrothermal vents and methane seeps. Studies have shown that the anammox process may be responsible for 30%–70% N2 production in the ocean. In environmental engineering related to nitrogenous wastewater treatment, anammox provides a new technology with low energy consumption, low cost, and high efficiency that can achieve energy saving and emission reduction. However, the discovery of anammox bacteria is actually a hard-won achievement. Early in the 1960s, the possibility of the anammox biogeochemical process was predicted to exist according to some marine geochemical data. Then in the 1970s, the existence of anammox bacteria was further predicted via chemical reaction thermodynamic calculations. However, these microorganisms were not found in subsequent decades. What hindered the discovery of anammox bacteria, an important N cycling microbial group widespread in hypoxic and anoxic environments? What are the factors that finally led to their discovery? What are the inspirations that the analyses of these questions can bring to scientific research? This review article will analyze and elucidate the above questions by presenting the fundamental physiological and ecological characteristics of the marine anammox bacteria and the principles of scientific research.
Similar content being viewed by others
References
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
Amann R I, Ludwig W, Schleifer K H. 1995. Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol Rev, 59: 143–169
Arrigo K R. 2005. Marine microorganisms and global nutrient cycles. Nature, 437: 349–355
Boumann H A, Longo M L, Stroeve P, Poolman B, Hopmans E C, Stuart M C, Sinninghe D J S, Schouten S. 2009. Biophysical properties of membrane lipids of anammox bacteria: I. Ladderane phospholipids form highly organized fluid membranes. Biochim Biophys Acta, 1788: 1444–1451
Broda E. 1977. Two kinds of lithotrophs missing in nature. Z Allg Mikrobiol, 17: 491–493
Byrne N, Strous M, Crépeau V, Kartal B, Birrien J L, Schmid M, Lesongeur F, Schouten S, Jaeschke A, Jetten M, Prieur D, Godfroy A. 2009. Presence and activity of anaerobic ammonium-oxidizing bacteria at deep-sea hydrothermal vents. J ISME, 3: 117–123
Chen Z J, Wang J F, Zhang H Q, Shen Y L. 2014. Review: Wastewater treatment process with anaerobic ammonia oxidation and its practical application (in Chinese). Ecol Environ Sci, 23: 521–527
Dalsgaard T, Canfield D, Petersen J, Thamdrup B, Acuna-González J. 2003. N2 production by the anammox reaction in the anoxic water column of Golfo Dulce, Costa Rica. Nature, 422: 606–608
Dang H Y, Chen R P, Wang L, Guo L Z, Chen P P, Tang Z W, Tian F, Li S Z, Klotz M G. 2010. Environmental factors shape sediment anammox bacterial communities in hypernutrified Jiaozhou Bay, China. Appl Environ Microbiol, 76: 7036–7047
Dang H Y, Zhou H X, Zhang Z N, Yu Z S, Hua E, Liu X S, Jiao N Z. 2013. Molecular detection of Candidatus Scalindua pacifica and environmental responses of sediment anammox bacterial community in the Bohai Sea, China. PLoS ONE, 8: e61330
Devol A H. 2003. Solution to a marine mystery. Nature, 422: 575–576
Fuchsman C A, Staley J T, Oakley B B, Kirkpatrick J B, Murray J W. 2012. Free-living and aggregate-associated Planctomycetes in the Black Sea. FEMS Microbiol Ecol, 80: 402–416
Graaf A A, Bruijn P, Robertson L A, Jetten M S M, Kuenen J G. 1997. Metabolic pathway of anaerobic ammonium oxidation on the basis of 15N studies in a fluidized bed reactor. Microbiology, 143: 2415–2421
Graaf A A, Mulder A, Bruijn P, Jetten M S, Robertson L A, Kuenen J G. 1995. Anaerobic oxidation of ammonium is a biologically mediated process. Appl Environ Microbiol, 61: 1246–1251
Hu B L, Zheng P, Tang C J, Chen J W, Biezen E, Zhang L, Ni B J, Jetten M S, Yan J, Yu H Q, Kartal B. 2010. Identification and quantification of anammox bacteria in eight nitrogen removal reactors. Water Res, 44: 5014–5020
Hu Z, Alen T, Jetten M S, Kartal B. 2013. Lysozyme and penicillin inhibit the growth of anaerobic ammonium-oxidizing planctomycetes. Appl Environ Microbiol, 79: 7763–7769
Jaeschke A, Op den Camp H J, Harhangi H, Klimiuk A, Hopmans E C, Jetten M S, Schouten S, Sinninghe D J S. 2009. 16S rRNA gene and lipid biomarker evidence for anaerobic ammonium-oxidizing bacteria (anammox) in California and Nevada hot springs. FEMS Microbiol Ecol, 67: 343–350
Jetten M S, Niftrik L V, Strous M, Kartal B, Keltjens J T, Op den Camp H J. 2009. Biochemistry and molecular biology of anammox bacteria. Crit Rev Biochem Mol Biol, 44: 65–84
Jetten M S, Wagner M, Fuerst J, Loosdrecht M, Kuenen G, Strous M. 2001. Microbiology and application of the anaerobic ammonium oxidation (“anammox”) process. Curr Opin Biotechnol, 12: 283–288
Jogler C. 2014. The bacterial “mitochondrium”. Mol Microbiol, 10: 12814
Kartal B, Almeida N M, Maalcke W J, Op den Camp HJ, Jetten M S, Keltjens J T. 2013. How to make a living from anaerobic ammonium oxidation. FEMS Microbiol Rev, 37: 428–461
Kartal B, Kuenen J G, Loosdrecht M C. 2010. Sewage treatment with anammox. Science, 328: 702–703
Kartal B, Maalcke W J, Almeida N M, Cirpus I, Gloerich J, Geerts W, Op den Camp H J, Harhangi H R, Janssen-Megens E M, Francoijs K J, Stunnenberg H G, Keltjens J T, Jetten M S, Strous M. 2011. Molecular mechanism of anaerobic ammonium oxidation. Nature, 479: 127–130
Kartal B, Niftrik L, Rattray J, Vossenberg J L, Schmid M C, Sinninghe D J, Jetten M S, Strous M. 2008. Candidatus “Brocadia fulgida”: An autofluorescent anaerobic ammonium oxidizing bacterium. FEMS Microbiol Ecol, 63: 46–55
Kartal B, Rattray J, Niftrik L A, Vossenberg J, Schmid M C, Webb R I, Schouten S, Fuerst J A, Sinninghe D J, Jetten M S, Strous M. 2007. Candidatus “Anammoxoglobus propionicus” a new propionate oxidizing species of anaerobic ammonium oxidizing bacteria. Syst Appl Microbiol, 30: 39–49
Kuenen J G. 2008. Anammox bacteria: From discovery to application. Nat Rev Microbiol, 6: 320–326
Kuenen J G, Jetten M S. 2001. Extraordinary anaerobic ammonium oxidising bacteria. ASM News, 64: 456–463
Kuypers M M, Sliekers A O, Lavik G, Schmid M, Jøgensen B B, Kuenen J G, Sinninghe D J S, Strous M, Jetten M S M. 2003. Anaerobic ammonium oxidation by anammox bacteria in the Black Sea. Nature, 422: 608–611
Mulder A. 1992. Anoxic ammonia oxidation. US Patent US5078884 A
Mulder A, Graaf A A, Robertson L A, Kuenen J G. 1995. Anaerobic ammonium oxidation discovered in a denitrifying fluidized bed reactor. FEMS Microbiol Ecol, 16: 177–183
Neumann S, Jetten M S, Niftrik L. 2011. The ultrastructure of the compartmentalized anaerobic ammonium-oxidizing bacteria is linked to their energy metabolism. Biochem Soc Trans, 39: 1805–1810
Niftrik L, Jetten M S. 2012. Anaerobic ammonium-oxidizing bacteria: Unique microorganisms with exceptional properties. Microbiol Mol Biol Re, 76: 585–596
Quan Z X, Rhee S K, Zuo J E, Yang Y, Bae J W, Park J R, Lee S T, Park Y H. 2008. Diversity of ammonium-oxidizing bacteria in a granular sludge anaerobic ammonium-oxidizing (anammox) reactor. Environ Microbiol, 10: 3130–3139
Richard F A. 1965. Anoxic basins and fjords. In: Ripley J P, Skirrow G, eds. Chemical Oceanography. Manhattan: Academic Press. 1: 611–645
Rothrock M J J, Vanotti M B, Szögi A A, Gonzalez M C, Fujii T. 2011. Long-term preservation of anammox bacteria. Appl Microbiol Biotechnol, 92: 147–157
Russ L, Kartal B, Op den Camp H J, Sollai M, Le Bruchec J, Caprais J C, Godfroy A, Sinninghe D J S, Jetten M S. 2013. Presence and diversity of anammox bacteria in cold hydrocarbon-rich seeps and hydrothermal vent sediments of the Guaymas Basin. Front Microbiol, 4: 219
Schalk J, Oustad H, Kuenen J G, Jetten M S. 1998. The anaerobic oxidation of hydrazine: A novel reaction in microbial nitrogen metabolism. FEMS Microbiol Lett, 158: 61–67
Schmid M, Twachtmann U, Klein M, Strous M, Juretschko S, Jetten M, Metzger J W, Schleifer K H, Wagner M. 2000. Molecular evidence for genus level diversity of bacteria capable of catalyzing anaerobic ammonium oxidation. Syst Appl Microbiol, 23: 93–106
Schmid M, Walsh K, Webb R, Rijpstra W I, Pas-Schoonen K, Verbruggen M J, Hill T, Moffett B, Fuerst J, Schouten S, Sinninghe D J S, 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: 529–38
Shao S D, Luan X W, Dang H Y, Zhou H X, Zhao Y K, Liu H T, Zhang Y B, Dai L Q, Ye Y, Klotz M G. 2014. Deep-sea methane seep sediments in the Okhotsk Sea sustain diverse and abundant anammox bacteria. FEMS Microbiol Ecol, 87: 503–516
Sinninghe D J, Rijpstra W I, Geenevasen J A, Strous M, Jetten M S. 2005. Structural identification of ladderane and other membrane lipids of planctomycetes capable of anaerobic ammonium oxidation (anammox). FEBS J, 272: 4270–4283
Sinninghe D J, Strous M, Rijpstra W I, Hopmans E C, Geenevasen J A, Duin A C, Niftrik LA, Jetten M S. 2002. Linearly concatenated cyclobutane lipids form a dense bacterial membrane. Nature, 419: 708–712
Sonthiphand P, Hall M W, Neufeld J D. 2014. Biogeography of anaerobic ammonia-oxidizing (anammox) bacteria. Front Microbiol, 5: 399
Stahl D A, Torre J R. 2012. Physiology and diversity of ammoniaoxidizing archaea. Annu Rev Microbiol, 66: 83–101
Strous M, Fuerst J A, Kramer E H, Logemann S, Muyzer G, Pas-Schoonen K T, Webb R, Kuenen J G, Jetten M S. 1999. Missing lithotroph identified as new planctomycete. Nature, 400: 446–449
Strous M, Pelletier E, Mangenot S, Rattei T, Lehner A, Taylor MW, Horn M, Daims H, Bartol-Mavel D, Wincker P, Barbe V, Fonknechten N, Vallenet D, Segurens B, Schenowitz-Truong C, Médigue C, Collingro A, Snel B, Dutilh B E, Op den Camp H J, van der Drift C, Cirpus I, van de Pas-Schoonen K T, Harhangi H R, van Niftrik L, Schmid M, Keltjens J, van de Vossenberg J, Kartal B, Meier H, Frishman D, Huynen MA, Mewes H W, Weissenbach J, Jetten M S, Wagner M, Le Paslier D. 2006. Deciphering the evolution and metabolism of an anammox bacterium from a community genome. Nature, 440: 790–794
Teeseling M C, Neumann S, Niftrik L. 2013. The anammoxosome organelle is crucial for the energy metabolism of anaerobic ammonium oxidizing bacteria. J Mol Microbiol Biotechnol, 23: 104–117
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
Venter J C, Remington K, Heidelberg J F, Halpern A L, Rusc D, Eisen J A, Wu D Y, Paulsen I, Nelson K E, Nelson W, Fouts D E, Levy S, Knap A H, Lomas M W, Nealson K, White O, Peterson J, Hoffman J, Parsons R, Baden-Tillson H, Pfannkoch C, Rogers Y H, Smith H O A F. 2004. Environmental genome shotgun sequencing of the Sargasso Sea. Science, 304: 66–74
Vossenberg J, Woebken D, Maalcke W J, Wessels H J, Dutilh B E, Kartal B, Janssen-Megens E M, Roeselers G, Yan J, Speth D, Gloerich J, Geerts W, van der Biezen E, Pluk W, Francoijs K J, Russ L, Lam P, Malfatti S A, Tringe S G, Haaijer S C, Op den Camp H J, Stunnenberg H G, Amann R, Kuypers M M, Jetten M S. 2013. The metagenome of the marine anammox bacterium “Candidatus Scalindua profunda” illustrates the versatility of this globally important nitrogen cycle bacterium. Environ Microbiol, 15: 1275–1289
Woebken D, Lam P, Kuypers M M, Naqvi S W, Kartal B, Strous M, Jetten M S, Fuchs B M, Amann R. 2008. A microdiversity study of anammox bacteria reveals a novel Candidatus Scalindua phylotype in marine oxygen minimum zones. Environ Microbiol, 10: 3106–3119
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Dang, H., Huang, R. & Jiao, N. Inspirations from the scientific discovery of the anammox bacteria: A classic example of how scientific principles can guide discovery and development. Sci. China Earth Sci. 59, 449–455 (2016). https://doi.org/10.1007/s11430-015-5203-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11430-015-5203-6