The Metabolism of Anammox

Abstract

Anaerobic ammonium‐oxidizing (anammox) bacteria derive their energy for growth from the conversion of ammonium and nitrite into dinitrogen gas. The bacteria are the latest addition to the biogeochemical nitrogen cycle. The slowly growing micro‐organisms that belong to the Planctomycetes are characterized by a compartmentalized cell architecture featuring a central cell organelle, the ‘anammoxosome’. Membrane systems surrounding the different cellular compartments are composed of unique ‘ladderane’ lipid molecules. Although the metabolism has not been completely resolved, nitrogen formation seems to involve the intermediary formation of hydrazine, a most reactive and toxic compound. Anammox bacteria have been detected in many oxygen‐limited freshwater and marine ecosystems investigated. In the marine environment, over 50% of the nitrogen gas released is made by anammox bacteria. Application of the anammox process offers an attractive alternative to current wastewater treatment systems for the removal of fixed nitrogen.

Key concepts

  • Ammonium is converted under anaerobic conditions into dinitrogen gas by a newly discovered and specialized group of micro‐organisms, the anammox bacteria.

  • Anammox bacteria are chemolithoautotrophic organisms that gain their energy for growth from the conversion of the inorganic substrates ammonium and nitrite. Cell carbon is derived from carbon dioxide.

  • Anammox bacteria are characterised by a unique cell plan featuring a central cell organelle, the anammoxosome.

  • The lipids from anammox bacteria are composed of highly unusual ‘ladderane’ molecules.

  • The conversion of ammonium and nitrite into dinitrogen gas proceeds through the intermediary formation of the toxic and highly reactive hydrazine.

  • Anammox bacteria synthesize adenosine triphosphate (ATP) by an electrochemical proton gradient most likely established across the anammoxosome membrane.

  • In nature approximately 50% of the dinitrogen gas released into the atmosphere is made by anammox bacteria.

  • Anammox bacteria offer an economically attractive and environmentally friendly alternative to current wastewater treatment processes for the removal of fixed nitrogen.

Keywords: anammox; anammoxosome; ladderane lipids; hydrazine

Figure 1.

The central steps in the biogeochemical nitrogen cycle. (1) Nitrogen fixation, (2) aerobic ammonium oxidation, (3) nitrite oxidation, (4) nitrate reduction, (5) denitrification and (6) nitrite reduction to ammonium.

Figure 2.

Growth of anammox bacteria in a sequencing batch reactor. The figure shows the experimental set‐up of a reactor containing the red anammox bacteria (left) and fluorescence in situ hybridization (FISH) analysis of the bacterial population present in the reactor (right). For FISH analysis, anammox bacteria were specifically labelled with a red fluorescent probe; blue fluorescent micro‐organisms represent non‐anammox species visualized by DAPI staining.

Figure 3.

Transmission electron microscopy of Candidatus ‘Anammoxoglobus propionicus’ showing the anammoxosome (A) containing tubule‐like structures, riboplasm (R) containing the nucloid (N) opposed to the anammoxosome membrane, paryphoplasm (P) separated from the riboplasm by an intracytoplasmic membrane (ICM) and the cytoplasmic membrane (CM). Scale bar, 200 nm. Adapted from Kartal et al. with permission from Elsevier.

Figure 4.

General structure of ladderane lipids from anammox bacteria.

Figure 5.

Hypothetical metabolism of anammox bacteria. (a) Anammox central catabolism; (b) central catabolism in connection nitrite oxidation to generate low‐redox‐potential electrons for cell carbon fixation. Abbreviations: Nir, nitrite reductase; HH, hydrazine hydrolase; HZO, hydrazine dehydrogenase; Nar, nitrate reductase; Q(H2), (reduced) ubiquinone; atp, F1F0 ATP synthase; fdh, formate dehydrogenase; nuo, NADH:ubiquinone oxidoreductase; RET, reversed electron transport. Symbols: red diamonds, cytochromes; yellow diamond, ferredoxin; solid arrows, reductions; dashed arrows, oxidations. Please note that the localization of the enzymic reactions and the direction of proton translocation are arbitrarily chosen, at which ΔΨ+ and ΔΨ are thought to represent the anammoxosome and riboplasmic compartments, respectively.

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Schmidt I, Sliekers O, Schmid M et al. (2003) New concepts of microbial treatment processes for the nitrogen removal in wastewater. FEMS Microbiology Reviews 27: 481–492.

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Kartal, Boran, Keltjens, Jan T, and Jetten, Mike SM(Dec 2008) The Metabolism of Anammox. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0021315]