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Anaerobic ammonium-oxidizing bacteria: unique microorganisms with exceptional properties - PubMed

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Anaerobic ammonium-oxidizing bacteria: unique microorganisms with exceptional properties

Laura van Niftrik et al. Microbiol Mol Biol Rev. 2012 Sep.

Abstract

Anaerobic ammonium-oxidizing (anammox) bacteria defy many microbiological concepts and share numerous properties with both eukaryotes and archaea. Among their most intriguing characteristics are their compartmentalized cell plan and archaeon-like cell wall. Here we review our current knowledge about anammox cell biology. The anammox cell is divided into three separate compartments by bilayer membranes. The anammox cell consists of (from outside to inside) the cell wall, paryphoplasm, riboplasm, and anammoxosome. Not much is known about the composition or function of both the anammox cell wall and the paryphoplasm compartment. The cell wall is proposed to be proteinaceous and to lack both peptidoglycan and an outer membrane typical of Gram-negative bacteria. The function of the paryphoplasm is unknown, but it contains the cell division ring. The riboplasm resembles the standard cytoplasmic compartment of other bacteria; it contains ribosomes and the nucleoid. The anammoxosome occupies most of the cell volume and is a so-called "prokaryotic organelle" analogous to the eukaryotic mitochondrion. This is the site where the anammox reaction takes place, coupled over the curved anammoxosome membrane, possibly giving rise to a proton motive force and subsequent ATP synthesis. With these unique properties, anammox bacteria are food for thought concerning the early evolution of the domains Bacteria, Archaea, and Eukarya.

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Figures

Fig 1
Fig 1

The biological nitrogen cycle. Black arrows, anaerobic reactions; white arrows, aerobic reactions; gray arrows, both aerobic and anaerobic reactions.

Fig 2
Fig 2

Cellular compartmentalization in Planctomycetes. (Partly based on reference with kind permission from Springer Science+Business Media.)

Fig 3
Fig 3

Structures of three characteristic ladderane lipids. I, ladderane fatty acid containing ring system Y; II, ladderane monoalkyl glycerol ether containing ring system X; III, ladderane glycerol ether/ester containing both ring systems X and Y. Lipids containing ladderane moieties X and Y are abundant membrane lipids in anammox bacteria. (Adapted from reference with kind permission from Springer Science+Business Media.)

Fig 4
Fig 4

Postulated anaerobic ammonium oxidation coupled to the anammoxosome membrane in anammox bacteria resulting in a proton motive force and subsequent ATP synthesis via membrane-bound ATPases. Heme-containing enzymes are shown in gray. bc1, cytochrome bc1 complex; cyt, cytochrome; HDH, hydrazine dehydrogenase; HZS, hydrazine synthase; NirS, nitrite reductase; Q, coenzyme Q; a, anammoxosome compartment; r, riboplasm compartment. (Adapted from reference with permission of the publisher. Copyright 2010 Blackwell Publishing Ltd.)

Fig 5
Fig 5

Experimental evidence for the anammoxosome compartment of anammox bacteria being a dedicated energy generator. (A) Immunogold localization of an anammox hydroxylamine oxidoreductase-like protein shows its location in the anammoxosome compartment in rehydrated cryosections of “Candidatus Kuenenia stuttgartiensis.” a, anammoxosome; r, riboplasm; p, paryphoplasm. Scale bar, 200 nm. (B) Cytochrome peroxidase staining localizes cytochrome c proteins to the anammoxosome in chemically fixed and Epon-embedded thin sections of “Candidatus Kuenenia stuttgartiensis.” Intense staining occurs in close proximity to the anammoxosome membrane, as outlined by the dashed lines. Scale bar, 200 nm. (Adapted from reference .) (C and D) Immunogold localization of the catalytic beta subunit of the F-ATPase-1 gene cluster localizes this ATPase to the outermost membrane and the anammoxosome membrane in rehydrated cryosections of “Candidatus Kuenenia stuttgartiensis.” Scale bar, 250 nm. (Adapted from reference with permission of the publisher. Copyright 2010 Blackwell Publishing Ltd.)

Fig 6
Fig 6

Transmission electron micrographs and electron tomography model of different high-pressure-frozen, freeze-substituted, and Epon-embedded anammox bacteria. (A) “Candidatus Kuenenia stuttgartiensis” cell showing tubule-like structures (inset) inside the anammoxosome. a, anammoxosome; r, riboplasm; p, paryphoplasm. (Adapted from reference .) (B) “Candidatus Anammoxoglobus propionicus” cell showing glycogen storage (black arrow) and iron-containing anammoxosome particles (white arrow). The inset shows a glycogen-stained “Candidatus Kuenenia stuttgartiensis” cell. (Adapted from reference .) (C) “Candidatus Brocadia fulgida” cell showing riboplasmic particles (black arrow) and iron-containing anammoxosome particles (white arrow). (Adapted from reference .) (D) “Candidatus Scalindua” sp. cell showing pilus-like cell appendages. (E) “Candidatus Kuenenia stuttgartiensis” cell showing the onset of cell division and the appearance of the cell division ring in the paryphoplasm (black arrows). The white arrow shows glycogen storage particles. (Adapted from reference .) (F) Snapshot of an electron tomography model showing the cell wall (in red) and the cell division ring (in yellow) of a “Candidatus Brocadia fulgida” cell. Scale bars, 200 nm. (Adapted from reference .)

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