Skip to main content

Advertisement

Log in

Cell biology of unique anammox bacteria that contain an energy conserving prokaryotic organelle

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

Abstract

Anammox bacteria obtain their energy for growth from the anaerobic oxidation of ammonium with nitrite to dinitrogen gas. This property has made anammox bacteria very valuable for industry where they are applied for the removal of nitrogen compounds from industrial and domestic wastewaters. Anammox bacteria are also important in nature where they contribute significantly to oceanic nitrogen loss. Further, anammox bacteria have similarities to both Archaea and Eukarya, making them extremely interesting from a cell biological perspective. The anammox cell does not conform to the typical prokaryotic cell plan: single bilayer membranes divide the anammox cell into three distinct cellular compartments that possibly also have distinct cellular functions. The innermost and largest compartment, the anammoxosome, is the location of the energy metabolism. The middle compartment, the riboplasm, contains the nucleoid and ribosomes and thus has a genetic, information processing function. Finally, the outermost compartment, the paryphoplasm, has an as yet unknown function. In addition, anammox bacteria are proposed to have an atypical cell wall devoid of both peptidoglycan and a typical outer membrane. Here, I review the current knowledge on the cell biology of this enigmatic group of bacteria.

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
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • 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 (2006) Ladderane phospholipids in anammox bacteria comprise phosphocholine and phosphoethanolamine headgroups. FEMS Microbiol Lett 258:297–304

    Article  PubMed  CAS  Google Scholar 

  • Boumann HA, Longo ML, Stroeve P, Poolman B, Hopmans EC, Stuart MCA, Sinninghe Damsté JS, 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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Clark I, Timlin R, Bourbonnais A, Jones K, Lafleur D, Wickens K (2008) Origin and fate of industrial ammonium in anoxic ground water—(15)N evidence for anaerobic oxidation (anammox). Ground Water Monit R 28:73–82

    Article  CAS  Google Scholar 

  • de Almeida NM, Maalcke WJ, Keltjens JT, Jetten MSM, Kartal B (2011) Proteins and protein complexes involved in the biochemical reactions of anaerobic ammonium-oxidizing bacteria. Biochem Soc Trans 39:303–308

    Article  PubMed  Google Scholar 

  • Fuerst JA (2005) Intracellular compartmentation in planctomycetes. Annu Rev Microbiol 59:299–328

    Article  PubMed  CAS  Google Scholar 

  • Ghuysen JM (1997) Penicillin-binding proteins. Wall peptidoglycan assembly and resistance to penicillin: facts, doubts and hopes. Int J Antimicrob Ag 8:45–60

    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 4:11–27

    CAS  Google Scholar 

  • Hirsch MD, Long ZT, Song B (2011) Anammox bacterial diversity in various aquatic ecosystems based on the detection of hydrazine oxidase genes (hzoA/hzoB). Microbial Ecol 61:264–276

    Article  CAS  Google Scholar 

  • Hu BL, Rush D, van der Biezen E, Zheng P, van Mullekom M, Schouten S, Sinninghe Damsté JS, Smolders AJP, Jetten MSM, Kartal B (2011) New anaerobic, ammonium-oxidizing community enriched from peat soil. Appl Environ Microbiol 77:966–971

    Article  PubMed  CAS  Google Scholar 

  • Hu BL, Shen LD, Zheng P, Hu AH, Chen TT, Cai C, Liu S, Lou LP (2012a) Distribution and diversity of anaerobic ammonium-oxidizing bacteria in the sediments of the Qiantang river. Environ Microbiol Rep 4:540–547

    Article  PubMed  CAS  Google Scholar 

  • Hu Z, Speth DR, Francoijs KJ, Quan ZX, Jetten MSM (2012b) Metagenome analysis of a complex community reveals the metabolic blueprint of anammox bacterium “Candidatus Jettenia asiatica”. Front Microbiol 3:366

    Article  PubMed  Google Scholar 

  • Jetten MSM, Sliekers O, Kuypers M, Dalsgaard T, van Niftrik L, Cirpus I, van de Pas-Schoonen K, Lavik G, Thamdrup B, Le Paslier D, Op den Camp HJM, Hulth S, Nielsen LP, Abma W, Third K, Engström P, Kuenen JG, Jørgensen BB, Canfield DE, Sinninghe Damsté JS, Revsbech NP, Fuerst J, Weissenbach J, Wagner M, Schmidt I, Schmid M, Strous M (2003) Anaerobic ammonium oxidation by marine and freshwater planctomycete-like bacteria. Appl Microbiol Biotechnol 63:107–114

    Article  PubMed  CAS  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

    PubMed  CAS  Google Scholar 

  • Jetten MSM, Op den Camp HJM, Kuenen JG, Strous M (2010) Family I. “Candidatus Brocadiaceae” fam. nov. In: Krieg NR, Staley JT, Brown DR, Hedlund B, Paster BJ, Ward N, Ludwig W, Whitman WB (eds) Bergey’s manual of systematic bacteriology. Springer, New York, pp 596–602

    Google Scholar 

  • 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 (2007) Candidatus “Anammoxoglobus propionicus” a new propionate oxidizing species of anaerobic ammonium oxidizing bacteria. Syst Appl Microbiol 30:39–49

    Article  PubMed  CAS  Google Scholar 

  • Kartal B, van Niftrik L, Rattray J, van de Vossenberg JLCM, 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  PubMed  CAS  Google Scholar 

  • Kartal B, Kuenen JG, van Loosdrecht MCM (2010) Sewage treatment with anammox. Science 328:702–703

    Article  PubMed  CAS  Google Scholar 

  • Kartal B, Geerts W, Jetten MSM (2011a) Cultivation, detection, and ecophysiology of anaerobic ammonium-oxidizing bacteria. In: Klotz MG (ed) Methods in enzymology: research on nitrification and related processes, vol 486, Part A. Elsevier Academic Press Inc., San Diego, pp 89–108

    Chapter  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 K-J, Stunnenberg HG, Keltjens JT, Jetten MSM, Strous M (2011b) Molecular mechanism of anaerobic ammonium oxidation. Nature 479:127–130

    Article  PubMed  CAS  Google Scholar 

  • Kartal B, van Niftrik L, Keltjens JT, Op den Camp HJM, Jetten MSM (2012) Anammox—growth, physiology, cell biology, and metabolism. In: Poole RK (ed) Advances in microbial physiology, vol 60. Elsevier Academic Press Inc., San Diego, pp 211–262

    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  PubMed  CAS  Google Scholar 

  • König E, Schlesner H, Hirsch P (1984) Cell wall studies on budding bacteria of the PlanctomycesPasteuria group and on a Prosthecomicrobium sp. Arch Microbiol 138:200–205

    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  PubMed  CAS  Google Scholar 

  • Lam P, Kuypers MMM (2011) Microbial nitrogen cycling processes in oxygen minimum zones. In: Carlson CA, Giovannoni SJ (eds) Annual review of marine science, vol 3. Annual Reviews, Palo Alto, pp 317–345

    Google Scholar 

  • Li M, Cao HL, Hong YG, Gu JD (2011) Seasonal dynamics of anammox bacteria in estuarial sediment of the Mai Po Nature Reserve revealed by analyzing the 16S rRNA and hydrazine oxidoreductase (hzo) genes. Microbes Environ 26:15–22

    Article  PubMed  CAS  Google Scholar 

  • Lindsay MR, Webb RI, Fuerst JA (1997) Pirellulosomes: a new type of membrane-bounded cell compartment in planctomycete bacteria of the genus Pirellula. Microbiol 143:739–748

    Article  CAS  Google Scholar 

  • Lindsay MR, Webb RI, Strous M, Jetten MSM, Butler MK, Forde RJ, Fuerst JA (2001) Cell compartmentalisation in planctomycetes: novel types of structural organisation for the bacterial cell. Arch Microbiol 175:413–429

    Article  PubMed  CAS  Google Scholar 

  • Margolin W (2005) FtsZ and the division of prokaryotic cells and organelles. Nat Rev Mol Cell Biol 6:862–871

    Article  PubMed  CAS  Google Scholar 

  • Medema MH, Zhou M, van Hijum SAFT, Gloerich J, Wessels HJCT, Siezen RJ, Strous M (2010) A predicted physicochemically distinct sub-proteome associated with the intracellular organelle of the anammox bacterium Kuenenia stuttgartiensis. BMC Genomics 11:299

    Article  PubMed  Google Scholar 

  • Neumann S, van Teeseling MCF, van Niftrik L (2013) Cell biology of anaerobic ammonium-oxidizing bacteria: unique prokaryotes with an energy-conserving intracellular compartment. In: Fuerst JA (ed) Planctomycetes: cell structure, origins and biology. Springer, New York, pp 89–123

    Google Scholar 

  • Penton CR, Devol AH, Tiedje JM (2006) Molecular evidence for the broad distribution of anaerobic ammonium-oxidizing bacteria in freshwater and marine sediments. Appl Environ Microbiol 72:6829–6832

    Article  PubMed  CAS  Google Scholar 

  • Preiss J (1984) Bacterial glycogen synthesis and its regulation. Ann Rev Microbiol 38:419–458

    Article  CAS  Google Scholar 

  • Quan Z-X, Rhee S-K, Zuo J-E, Yang Y, Bae J-W, Ryeong JP, 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

    Article  PubMed  CAS  Google Scholar 

  • Rattray JE, van de Vossenberg J, Hopmans EC, Kartal B, van Niftrik L, Rijpstra WIC, Strous M, Jetten MSM, Schouten S, Sinninghe Damsté JS (2008) Ladderane lipid distribution in four genera of anammox bacteria. Arch Microbiol 190:51–66

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Richards FA (1965) Chemical observations in some anoxic, sulfide-bearing basins and fjords. In: Pearson EA (ed) Advances in water pollution research, vol 3. Pergamon Press Inc., London, pp 215–232

    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. Aquatic Microbial Ecol 36:293–304

    Article  Google Scholar 

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

    Article  PubMed  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, Sinninghe Damsté JS, Harris J, Shaw P, Jetten M, Strous M (2003) Candidatus “Scalindua brodae”, sp. nov., Candidatus “Scalindua wagneri”, sp. nov., two new species of anaerobic ammonium oxidizing bacteria. Syst Appl Microbiol 26:529–538

    Article  PubMed  CAS  Google Scholar 

  • Schubert CJ, Durisch-Kaiser E, Wehrli B, Thamdrup B, Lam P, Kuypers MMM (2006) Anaerobic ammonium oxidation in a tropical freshwater system (Lake Tanganyika). Environ Microbiol 8:1857–1863

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Sinninghe Damsté JS, Rijpstra WIC, Strous M, Jetten MSM, David ORP, Geenevasen JAJ, van Maarseveen JH (2004) A mixed ladderane/n-alkyl glycerol diether membrane lipid in an anaerobic ammonium-oxidizing bacterium. Chem Commun (Camb) 22:2590–2591

    Article  Google Scholar 

  • Speth DR, van Teeseling MCF, Jetten MSM (2012) Genomic analysis indicates the presence of an asymmetric bilayer outer membrane in Planctomycetes and Verrucomicrobia. Front Microbiol 3:304

    PubMed  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 Microbiol Biot 50:589–596

    Article  CAS  Google Scholar 

  • Strous M, Fuerst JA, Kramer EHM, 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  PubMed  CAS  Google Scholar 

  • 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 (2006) Deciphering the evolution and metabolism of an anammox bacterium from a community genome. Nature 440:790–794

    Article  PubMed  Google Scholar 

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

    PubMed  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  PubMed  Google Scholar 

  • van de Vossenberg J, Woebken D, Maalcke WJ, Wessels HJCT, Dutilh BE, Kartal B, Janssen-Megens EM, Roeselers G, Yan J, Speth D, Gloerich J, Geerts W, van der Biezen E, Pluk W, Francoijs K, Russ L, Lam P, Malfatti SA, Green Tringe S, Haaijer SCM, Op den Camp HJM, Stunnenberg HG, Amann R, Kuypers MMM, Jetten MSM (2012) 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

    Article  PubMed  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  PubMed  Google Scholar 

  • van Niftrik LA, Fuerst JA, Damste JSS, Kuenen JG, Jetten MSM, Strous M (2004) The anammoxosome: an intracytoplasmic compartment in anammox bacteria. FEMS Microbiol Lett 233:7–13

    Article  PubMed  Google Scholar 

  • van Niftrik L, Geerts WJC, van Donselaar EG, Humbel BM, Webb RI, Fuerst JA, Verkleij AJ, Jetten MSM, Strous M (2008a) Linking ultrastructure and function in four genera of anaerobic ammonium-oxidizing bacteria: cell plan, glycogen storage and localization of cytochrome c proteins. J Bacteriol 190:708–717

    Article  PubMed  Google Scholar 

  • van Niftrik L, Geerts WJC, van Donselaar EG, Humbel BM, Yakushevska A, Verkleij AJ, Jetten MSM, Strous M (2008b) Combined structural and chemical analysis of the anammoxosome: a membrane-bounded intracytoplasmic compartment in anammox bacteria. J Struct Biol 161:401–410

    Article  PubMed  Google Scholar 

  • 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 (2009) Cell division ring, a new cell division protein and vertical inheritance of a bacterial organelle in anammox planctomycetes. Mol Microbiol 73:1009–1019

    Article  PubMed  Google Scholar 

  • 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 (2010) Intracellular localization of membrane-bound ATPases in the compartmentalized anammox bacterium “Candidatus Kuenenia stuttgartiensis”. Mol Microbiol 77:701–715

    Article  PubMed  Google Scholar 

  • Woebken D, Lam P, Kuypers MMM, Naqvi SWA, Kartal B, Strous M, Jetten MSM, Fuchs BM, 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

    Article  PubMed  CAS  Google Scholar 

  • Yoshinaga I, Amano T, Yamagishi T, Okada K, Ueda S, Sako Y, Suwa Y (2011) Distribution and diversity of anaerobic ammonium oxidation (anammox) bacteria in the sediment of a eutrophic freshwater lake, Lake Kitaura, Japan. Microbes Environ 26:189–197

    Article  PubMed  Google Scholar 

  • Zhang Y, Ruan X-H, Op den Camp HJM, Smits TJM, Jetten MSM, Schmid MC (2007) Diversity and abundance of aerobic and anaerobic ammonium-oxidizing bacteria in freshwater sediments of the Xinyi River (China). Environ Microbiol 9:2375–2382

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

I would like to thank our past and present co-workers at the department of Microbiology and all of our (inter)national collaborators and granting agencies. Further, I would specifically like to thank Sarah Neumann, Muriel van Teeseling, Huub Op den Camp, Boran Kartal, Jan Keltjens and Mike Jetten for discussions. LvN is supported by the Netherlands Organization for Scientific Research (VENI Grant Number 863.09.009).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Laura van Niftrik.

Rights and permissions

Reprints and permissions

About this article

Cite this article

van Niftrik, L. Cell biology of unique anammox bacteria that contain an energy conserving prokaryotic organelle. Antonie van Leeuwenhoek 104, 489–497 (2013). https://doi.org/10.1007/s10482-013-9990-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10482-013-9990-5

Keywords

Navigation