Anammox bacteria convert ammonium and nitrite to dinitrogen gas under anaerobic conditions to obtain their energy for growth. The anammox reaction was deemed impossible until its discovery in the early 1990s. Now, anammox bacteria are recognized as major players in the global nitrogen cycle and estimated to be responsible for up to 50% of the nitrogen in the air that we breathe. In addition, anammox bacteria are extremely valuable for wastewater treatment where they are applied for the removal of ammonium. Besides their importance in industry and the environment, anammox bacteria defy some basic biological concepts. Whereas most other bacteria have only one cell compartment, the cytoplasm, anammox bacteria have three independent cell compartments bounded by bilayer membranes, from out- to inside; the paryphoplasm, riboplasm and anammoxosome. The anammoxosome is the largest compartment of the anammox cell and is proposed to be dedicated to energy conservation. As such it would be analogous to the mitochondria of eukaryotes. This review will discuss the anammox cell plan in detail, with the main focus on the anammoxosome. The identity of the anammoxosome as a prokaryotic organelle and the importance of this organelle for anammox bacteria are discussed as well as challenges these bacteria face by having three independent cell compartments.

1.
Alberts B, Johnson A, Lewis J, Raff M, Roberts K, Walter P: Molecular Biology of the Cell, ed 4. New York, Garland Science, 2002, p. G25.
2.
Berks BC, Palmer T, Sargent F: Protein targeting by the bacterial twin-arginine translocation (Tat) pathway. Curr Opin Microbiol 2005;8:174-181.
3.
Beutler M, Milucka J, Hinck S, Schreiber F, Brock J, Mussmann M, Schulz-Vogt HN, de Beer D: Vacuolar respiration of nitrate coupled to energy conversation in filamentous Beggiatoaceae. Environ Microbiol 2012;14:2911-2919.
4.
Bonafonte MA, Solano C, Sesma B, Alvarez M, Montuenga L, García-Ros D, Gamazo C: The relationship between glycogen synthesis, biofilm formation and virulence in Salmonella enteritidis. FEMS Microbiol Lett 2000;191:31-36.
5.
Boumann HA, Hopmans EC, van de Leemput I, Op den Camp HJM, van de Vossenberg J, Strous M, Jetten MSM, Sinninghe Damsté JS, Schouten S: Ladderane phospholipids in anammox bacteria comprise phosphocholine and phosphoethanolamine headgroups. FEMS Microbiol Lett 2006;258:297-304.
6.
Boumann HA, Longo ML, Stroeve P, Poolman B, Hopmans EC, Stuart MCA, Sinninghe Damsté JS, Schouten S: Biophysical properties of membrane lipids of anammox bacteria. I. Ladderane phospholipids form highly organized fluid membranes. Biochim Biophys Acta 2009;1788:1444-1451.
7.
Brandes JA, Devol AH, Deutsch C: New developments in the marine nitrogen cycle. Chem Rev 2007;107:577-589.
8.
Broda E: Two kinds of lithotrophs missing in nature. Z Allg Mikrobiol 1977;17:491-493.
9.
Byrne N, Strous M, Crépeau V, Kartal B, Birrien J-L, Schmid M, Lesongeur F, Schouten S, Jaeschke A, Jetten MSM, Prieur D, Godfroy A: Presence and activity of anaerobic ammonium-oxidizing bacteria at deep-sea hydrothermal vents. ISME J 2009;3:117-123.
10.
Carrondo MA: Ferritins, iron uptake and storage from the bacterioferritin viewpoint. EMBO J 2003;22:1959-1968.
11.
Cohen-Bazire G, Pfenning N, Kunisawa R: The fine structure of green bacteria. J Cell Biol 1964;22:207-225.
12.
Dudkina NV, Heinemeyer J, Keegstra W, Boekema EJ, Braun H-P: Structure of dimeric atp synthase from mitochondria: an angular association of monomers induces the strong curvature of the inner membrane. FEBS Lett 2005;579:5769-5772.
13.
Faivre D, Schüler D: Magnetotactic bacteria and magnetosomes. Chem Rev 2008;108:4875-4898.
14.
Fiencke C, Bock E: Immunocytochemical localization of membrane-bound ammonia monooxygenase in cells of ammonia oxidizing bacteria. Arch Microbiol 2006;185:99-106.
15.
Figueiredo MCO, Lobo SAL, Carita JN, Nobre LS, Saraiva LM: Bacterioferritin protects the anaerobe Desulfovibrio vulgaris Hildenborough against oxygen. Anaerobe 2012;18:454-458.
16.
Fuerst JA: The planctomycetes: emerging models for microbial ecology, evolution and cell biology. Microbiology 1995;141:1493-1506.
17.
Fuerst JA: Intracellular compartmentation in planctomycetes. Annu Rev Microbiol 2005;59:299-328.
18.
Fuerst JA, Sagulenko E: Beyond the bacterium: planctomycetes challenge our concepts of microbial structure and function. Nature Rev Microbiol 2011;9:403-413.
19.
Fuerst JA, Webb RI: Membrane-bounded nucleoid in the eubacterium Gemmata obscuriglobus. Proc Natl Acad Sci USA 1991;88:8184-8188.
20.
Hanson RS, Hanson TE: Methanotrophic bacteria. Microbiol Rev 1996;60:439-471.
21.
Hu B-L, Rush D, van der Biezen E, Zheng P, van Mullekom M, Schouten S, Sinninghe Damsté JS, Smolders AJP, Jetten MSM, Kartal B: New anaerobic, ammonium-oxidizing community enriched from peat soil. Appl Environ Microbiol 2011;77:966-971.
22.
Jannasch HW, Nelson DC, Wirsen CO: Massive natural occurrence of unusually large bacteria (Beggiatoa spp.) at a hydrothermal deep-sea vent site. Nature 1989;342:834-836.
23.
Jetten MSM, van Niftrik L, Strous M, Kartal B, Keltjens JT, Op den Camp HJM: Biochemistry and molecular biology of anammox bacteria. Crit Rev Biochem Mol Biol 2009;44:65-84.
24.
Jetten MSM, Op den Camp HJM, Kuenen JG, Strous M: Description of the order Brocadiales; in Krieg NR, Ludwig W, Whitman WB, Hedlund BP, Paster BJ, Staley JT, Ward N, Brown D, Parte A (eds): Bergey's Manual of Systematic Bacteriology, vol 4. Heidelberg, Springer, 2010, pp. 596-603.
25.
Karlsson R, Karlsson A, Bäckman O, Johansson BR, Hulth S: Identification of key proteins involved in the anammox reaction. FEMS Microbiol Lett 2009;297:87-94.
26.
Kartal B, Geerts W, Jetten MSM: Cultivation, detection, and ecophysiology of anaerobic ammonium-oxidizing bacteria; in Klotz MG (ed): Methods in Enzymology: Research on Nitrification and Related Processes, vol 486. San Diego, Elsevier Academic Press, 2011a, part A, pp 89-108.
27.
Kartal B, Kuenen JG, van Loosdrecht MCM: Sewage treatment with anammox. Science 2010;328:702-703.
28.
Kartal B, Kuypers MMM, Lavik G, Schalk J, den Camp H, Jetten MSM, Strous M: Anammox bacteria disguised as denitrifiers: nitrate reduction to dinitrogen gas via nitrite and ammonium. Env Microbiol 2007a;9:635-642.
29.
Kartal B, Maalcke WJ, de Almeida NM, Cirpus I, Gloerich J, Geerts W, Op den Camp HJM, Harhangi HR, Janssen-Megens EM, Francoijs K-J, Stunnenberg HG, Keltjens JT, Jetten MSM, Strous M: Molecular mechanism of anaerobic ammonium oxidation. Nature 2011b;479:127-130.
30.
Kartal B, Rattray J, van Niftrik LA, van de Vossenberg J, Schmid MC, Webb RI, Schouten S, Fuerst JA, Sinninghe Damsté J, Jetten MSM, Strous M: Candidatus ‘Anammoxoglobus propionicus' a new propionate oxidizing species of anaerobic ammonium oxidizing bacteria. Syst Appl Microbiol 2007b;30:39-49.
31.
Kartal B, van Niftrik L, Rattray J, de Vossenberg J, Schmid MC, Damste JSS, Jetten MSM, Strous M: Candidatus ‘brocadia fulgida': an autofluorescent anaerobic ammonium oxidizing bacterium. FEMS Microbiol Ecol 2008;63:46-55.
32.
König E, Schlesner H, Hirsch P: Cell wall studies on budding bacteria of the Planctomyces-Pasteuria group and on a Prosthecomicrobium spp. Arch Microbiol 1984;138:200-205.
33.
Kuypers MMM, Sliekers AO, Lavik G, Schmid M, Jørgensen BB, Kuenen JG, Sinninghe Damsté JS, Strous M, Jetten MSM: Anaerobic ammonium oxidation by anammox bacteria in the Black Sea. Nature 2003;422:608-611.
34.
Liesack W, König H, Schlesner H, Hirsch P: Chemical composition of the peptidoglycan-free cell envelopes of budding bacteria of the Pirella/Planctomyces group. Arch Microbiol 1986;145:361-366.
35.
Lindsay MR, Webb RI, Fuerst JA: Pirellulosomes: a new type of membrane-bounded cell compartment in planctomycete bacteria of the genus Pirellula. Microbiology 1997;143:739-748.
36.
Lindsay MR, Webb RI, Strous M, Jetten MSM, Butler MK, Forde RJ, Fuerst JA: Cell compartmentalisation in planctomycetes: novel types of structural organisation for the bacterial cell. Arch Microbiol 2001;175:413-429.
37.
Mannella CA: Structure and dynamics of the mitochondrial inner membrane cristae. Biochim et Biophys Acta 2006;1763:542-548.
38.
Margolin W: FtsZ and the division of prokaryotic cells and organelles. Nature Rev Mol Cell Biol 2005;6:862-871.
39.
McMahon HT, Gallop JL: Membrane curvature and mechanisms of dynamic cell membrane remodelling. Nature 2005;438:590-596.
40.
Medema MH, Zhou M, van Hijum SAFT, Gloerich J, Wessels HJCT, Siezen RJ, Strous M: A predicted physicochemically distinct sub-proteome associated with the intracellular organelle of the anammox bacterium Kuenenia stuttgartiensis. BMC Genomics 2010;11:299.
41.
Minauro-Sanmiguel F, Wilkens S, Garcia JJ: Structure of dimeric mitochondrial atp synthase: novel f-0 bridging features and the structural basis of mitochondrial cristae biogenesis. Proc Natl Acad Sci USA 2005;102:12356-12358.
42.
Murray RGE, Watson SW: Structure of Nitrosocystis oceanus and comparison with Nitrosomonas and Nitrobacter. J Bacteriol 1965;89:1594-1609.
43.
Neumann S, van Teeseling MCF, van Niftrik L: Cell biology of anaerobic ammonium oxidizing bacteria: unique prokaryotes with an energy conserving intracellular compartment; in Fuerst JA (ed): New Models for Structure, Origins and Biology of the Cell: Planctomycetes and Relatives. New York, Springer, in press.
44.
Op den Camp HJM, Islam T, Stott MB, Harhangi HR, Hynes A, Schouten S, Jetten MSM, Birkeland N-K, Pol A, Dunfield PF: Environmental, genomic and taxonomic perspectives on methanotrophic Verrucomicrobia. Environ Microbiol Rep 2009;1:293-306.
45.
Preiss J: Bacterial glycogen synthesis and its regulation. Ann Rev Microbiol 1984;38:419-458.
46.
Quan Z-X, Rhee S-K, Zuo J-E, Yang Y, Bae J-W, Ryeong JP, Lee S-T, Park Y-H: Diversity of ammonium-oxidizing bacteria in a granular sludge anaerobic ammonium-oxidizing (anammox) reactor. Environ Microbiol 2008;10:3130-3139.
47.
Ragsdale SW, Pierce E: Acetogenesis and the Wood-Ljungdahl pathway of CO2 fixation. Biochim Biophys Acta 2008;1784:1873-1898.
48.
Rattray JE, van de Vossenberg J, Hopmans EC, Kartal B, van Niftrik L, Rijpstra WIC, Strous M, Jetten MSM, Schouten S, Sinninghe Damsté JS: Ladderane lipid distribution in four genera of anammox bacteria. Arch Microbiol 2008;190:51-66.
49.
Rattray JE, Strous M, Op den Camp HJM, Schouten S, Jetten MSM, Sinninghe Damsté JS: A comparative genomics study of genetic products potentially encoding ladderane lipid biosynthesis. Biol Direct 2009;4:8.
50.
Rohmer M, Bouviernave P, Ourisson G: Distribution of hopanoid triterpenes in prokaryotes. J Gen Microbiol 1984;130:1137-1150.
51.
Schmid M, Schmitz-Esser S, Jetten M, Wagner M: 16S-23S rDNA intergenic spacer and 23S rDNA of anaerobic ammonium-oxidizing bacteria: implications for phylogeny and in situ detection. Environ Microbiol 2001;3:450-459.
52.
Schouten S, Strous M, Kuypers MMM, Rijpstra WIC, Baas M, Schubert CJ, Jetten MSM, Sinninghe Damsté JS: Stable carbon isotopic fractionations associated with inorganic carbon fixation by anaerobic ammonium oxidizing bacteria. Appl Env Microbiol 2004;40:3785-3788.
53.
Silhavy TJ, Kahne D, Walker S: The bacterial cell envelope. Cold Spring Harb Perspect Biol 2010;2:a000414.
54.
Sinninghe Damsté JS, Strous M, Rijpstra WIC, Hopmans EC, Geenevasen JAJ, van Duin ACT, van Niftrik LA, Jetten MSM: Linearly concatenated cyclobutane lipids form a dense bacterial membrane. Nature 2002;419:708-712.
55.
Sinninghe Damsté JS, Rijpstra WIC, Schouten S, Fuerst JA, Jetten MSM, Strous M: The occurrence of hopanoids in planctomycetes: implications for the sedimentary biomarker record. Org Geochem 2004;35:561-566.
56.
Speth DR, van Teeseling MCF, Jetten MSM: Genomic analysis indicates the presence of an asymmetric bilayer outer membrane in Planctomycetes and Verrucomicrobia. Front Microbiol 2012;3:304.
57.
Strous M, Fuerst JA, Kramer EHM, Logemann S, Muyzer G, van de Pas-Schoonen KT, Webb R, Kuenen JG, Jetten MSM: Missing lithotroph identified as new planctomycete. Nature 1999a;400:446-449.
58.
Strous M, Kuenen JG, Jetten MSM: Key physiology of anaerobic ammonium oxidation. Appl Environ Microbiol 1999b;65:3248-3250.
59.
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 BE, Op den 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 H-W, Weissenbach J, Jetten MSM, Wagner M, Le Paslier D: Deciphering the evolution and metabolism of an anammox bacterium from a community genome. Nature 2006;440:790-794.
60.
van de Graaf AA, Mulder A, de Bruijn P, Jetten MSM, Robertson LA, Kuenen JG: Anaerobic oxidation of ammonium is a biologically mediated process. Appl Environ Microbiol 1995;61:1246-1251.
61.
van de Graaf AA, de Bruijn P, Robertson LA, Jetten MSM, Kuenen JG: Autotrophic growth of anaerobic ammonium-oxidizing microorganisms in a fluidized bed reactor. Microbiology 1996;142:2187-2196.
62.
van de Vossenberg J, Rattray JE, Geerts W, Kartal B, van Niftrik L, van Donselaar EG, Sinninghe Damsté JS, Strous M, Jetten MSM: Enrichment and characterization of marine anammox bacteria associated with global nitrogen gas production. Environ Microbiol 2008;10:3120-3129.
63.
van der Star WRL, Abma WR, Blommers D, Mulder J-W, Tokutomi T, Strous M, Picioreanu C, van Loosdrecht MCM: Startup of reactors for anoxic ammonium oxidation: experiences from the first full-scale anammox reactor in Rotterdam. Water Res 2007;41:4149-4163.
64.
van der Star WRL, Miclea AI, van Dongen UGJM, Muyzer G, Picioreanu C, van Loosdrecht MCM: The membrane bioreactor: a novel tool to grow anammox bacteria as free cells. Biotechnol Bioeng 2008;101:286-294.
65.
van Heijenoort J: Formation of the glycan chains in the synthesis of bacterial peptidoglycan. Glycobiology 2001;11:25R-36R.
66.
van Niftrik LA, Fuerst JA, Sinninghe Damsté JS, Kuenen JG, Jetten MSM, Strous M: The anammoxosome: an intracytoplasmic compartment in anammox bacteria. FEMS Microbiol Lett 2004;233:7-13.
67.
van Niftrik L, Geerts WJC, van Donselaar EG, Humbel BM, Webb RI, Fuerst JA, Verkleij AJ, Jetten MSM, Strous M: Linking ultrastructure and function in four genera of anaerobic ammonium-oxidizing bacteria: cell plan, glycogen storage and localization of cytochrome c proteins. J Bacteriol 2008a;190:708-717.
68.
van Niftrik L, Geerts WJC, van Donselaar EG, Humbel BM, Webb RI, Harhangi HR, Op den Camp HJM, Fuerst JA, Verkleij AJ, Jetten MSM, Strous M: Cell division ring, a new cell division protein and vertical inheritance of a bacterial organelle in anammox planctomycetes. Mol Microbiol 2009;73:1009-1019.
69.
van Niftrik L, Geerts WJC, van Donselaar EG, Humbel BM, Yakushevska A, Verkleij AJ, Jetten MSM, Strous M: Combined structural and chemical analysis of the anammoxosome: a membrane-bounded intracytoplasmic compartment in anammox bacteria. J Struct Biol 2008b;161:401-410.
70.
van Niftrik L, Jetten MSM: Anaerobic ammonium-oxidizing bacteria: unique microorganisms with exceptional properties. Microbiol Mol Biol Rev 2012;76:585-596.
71.
van Niftrik L, van Helden M, Kirchen S, van Donselaar EG, Harhangi HR, Webb RI, Fuerst JA, Op den Camp HJM, Jetten MSM, Strous M: Intracellular localization of membrane-bound ATPases in the compartmentalized anammox bacterium ‘Candidatus Kuenenia stuttgartiensis'. Mol Microbiol 2010;77:701-715.
72.
Vollmer W, Höltje JV: The architecture of the murein (peptidoglycan) in Gram-negative bacteria: vertical scaffold or horizontal layer(s)? J Bacteriol 2004;186:5978-5987.
73.
Watson SW: Taxonomic considerations of the family Nitrobacteraceae buchanan. Int J Syst Bacteriol 1971;21:254-270.
74.
Watson SW, Mandel M: Comparison of morphology and deoxyribonucleic acid composition of 27 strains of nitrifying bacteria. J Bacteriol 1971;107:563-569.
75.
Yee B, Sagulenko E, Morgan GP, Webb RI, Fuerst JA: Electron tomography of the nucleoid of Gemmata obscuriglobus reveals complex liquid crystalline cholesteric structure. Front Microbiol 2012;3:326.
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