Combined structural and chemical analysis of the anammoxosome: a membrane-bounded intracytoplasmic compartment in anammox bacteria.

Anammox bacteria have unique intracellular membranes that divide their cytoplasm into three separate compartments. The largest and innermost cytoplasmic compartment, the anammoxosome, is hypothesized to be the locus of all catabolic reactions in the anammox metabolism. Electron tomography showed that the anammoxosome and its membrane were highly folded. This finding was confirmed by a transmission electron microscopy study using different sample preparation methods. Further, in this study electron-dense particles were observed and electron tomography showed that they were confined to the anammoxosome compartment. Energy dispersive X-ray analysis revealed that these particles contained iron. The functional significance of a highly folded anammoxosome membrane and intracellular iron storage particles are discussed in relation to their possible function in energy generation.

[1]  J R Kremer,et al.  Computer visualization of three-dimensional image data using IMOD. , 1996, Journal of structural biology.

[2]  K. Tokuyasu A TECHNIQUE FOR ULTRACRYOTOMY OF CELL SUSPENSIONS AND TISSUES , 1973, The Journal of cell biology.

[3]  W. Liesack,et al.  Chemical composition of the peptidoglycan-free cell envelopes of budding bacteria of the Pirella/Planctomyces group , 1986, Archives of Microbiology.

[4]  J. Fuerst The planctomycetes: emerging models for microbial ecology, evolution and cell biology. , 1995, Microbiology.

[5]  J. G. Kuenen,et al.  Copyright � 1995, American Society for Microbiology Anaerobic Oxidation of Ammonium Is a Biologically Mediated Process , 1994 .

[6]  P. Walther,et al.  Freeze substitution of high‐pressure frozen samples: the visibility of biological membranes is improved when the substitution medium contains water , 2002, Journal of microscopy.

[7]  J. G. Kuenen,et al.  Anaerobic ammonium oxidation by anammox bacteria in the Black Sea , 2003, Nature.

[8]  Dmitrij Frishman,et al.  Deciphering the evolution and metabolism of an anammox bacterium from a community genome , 2006, Nature.

[9]  Harvey T. McMahon,et al.  Membrane curvature and mechanisms of dynamic cell membrane remodelling , 2005, Nature.

[10]  G. Moore,et al.  Effect of phosphate on bacterioferritin-catalysed iron(II) oxidation , 2004, JBIC Journal of Biological Inorganic Chemistry.

[11]  R. Frankel,et al.  Fe2+ and phosphate interactions in bacterial ferritin from Azotobacter vinelandii. , 1992, Biochemistry.

[12]  D. Studer,et al.  High pressure freezing comes of age. , 1989, Scanning microscopy. Supplement.

[13]  J. G. Kuenen,et al.  The anaerobic oxidation of hydrazine: a novel reaction in microbial nitrogen metabolism. , 1998, FEMS microbiology letters.

[14]  D. Canfield,et al.  Anaerobic ammonium oxidation (anammox) in the marine environment. , 2005, Research in microbiology.

[15]  J. G. Kuenen,et al.  Missing lithotroph identified as new planctomycete , 1999, Nature.

[16]  S. Andrews Iron storage in bacteria. , 1998, Advances in microbial physiology.

[17]  M. Kessel,et al.  Iron storage in Mycoplasma capricolum , 1980, Journal of bacteriology.

[18]  M. Lindsay,et al.  Pirellulosomes: a new type of membrane-bounded cell compartment in planctomycete bacteria of the genus Pirellula. , 1997, Microbiology.

[19]  Marc Strous,et al.  The anammoxosome: an intracytoplasmic compartment in anammox bacteria. , 2004, FEMS microbiology letters.

[20]  Adri C. T. van Duin,et al.  Linearly concatenated cyclobutane lipids form a dense bacterial membrane , 2002, Nature.

[21]  B. Lai,et al.  Mixed-Valence Cytoplasmic Iron Granules Are Linked to Anaerobic Respiration , 2006, Applied and Environmental Microbiology.

[22]  E. Melo,et al.  The genetic organization of Desulfovibrio desulphuricans ATCC 27774 bacterioferritin and rubredoxin‐2 genes: involvement of rubredoxin in iron metabolism , 2001, Molecular microbiology.

[23]  P. Hirsch,et al.  Cell wall studies on budding bacteria of the Planctomyces/Pasteuria group and on a Prosthecomicrobium sp. , 1984, Archives of Microbiology.

[24]  Marc Strous,et al.  Structural identification of ladderane and other membrane lipids of planctomycetes capable of anaerobic ammonium oxidation (anammox) , 2005, The FEBS journal.

[25]  A. J. Kalb,et al.  The composition and the structure of bacterioferritin of Escherichia coli. , 1981, The Biochemical journal.

[26]  S. de Vries,et al.  Involvement of a novel hydroxylamine oxidoreductase in anaerobic ammonium oxidation. , 2000, Biochemistry.

[27]  P. Harrison,et al.  Cloning, sequencing, and mapping of the bacterioferritin gene (bfr) of Escherichia coli K-12 , 1989, Journal of bacteriology.

[28]  Marc Strous,et al.  Cell compartmentalisation in planctomycetes: novel types of structural organisation for the bacterial cell , 2001, Archives of Microbiology.

[29]  J. G. Kuenen,et al.  Metabolic pathway of anaerobic ammonium oxidation on the basis of 15N studies in a fluidized bed reactor. , 1997, Microbiology.

[30]  J. J. Heijnen,et al.  The sequencing batch reactor as a powerful tool for the study of slowly growing anaerobic ammonium-oxidizing microorganisms , 1998, Applied Microbiology and Biotechnology.

[31]  E. V. van Donselaar,et al.  Immunogold Labeling of Cryosections from High‐Pressure Frozen Cells , 2007, Traffic.

[32]  C. Mannella Structure and dynamics of the mitochondrial inner membrane cristae. , 2006, Biochimica et biophysica acta.

[33]  E. Reynolds THE USE OF LEAD CITRATE AT HIGH pH AS AN ELECTRON-OPAQUE STAIN IN ELECTRON MICROSCOPY , 1963, The Journal of cell biology.

[34]  K. Zierold Effects of cadmium on electrolyte ions in cultured rat hepatocytes studied by X-ray microanalysis of cryosections. , 1997, Toxicology and applied pharmacology.

[35]  Mollenhauer Hh PLASTIC EMBEDDING MIXTURES FOR USE IN ELECTRON MICROSCOPY. , 1964 .

[36]  S. Andrews,et al.  Bacterial iron homeostasis. , 2003, FEMS microbiology reviews.