Cell compartmentalisation in planctomycetes: novel types of structural organisation for the bacterial cell

Abstract

The organisation of cells of the planctomycete species Pirellula marina, Isosphaera pallida, Gemmata obscuriglobus, Planctomyces maris and "Candidatus Brocadia anammoxidans" was investigated based on ultrastructure derived from thin-sections of cryosubstituted cells, freeze-fracture replicas, and in the case of Gemmata obscuriglobus and Pirellula marina, computer-aided 3-D reconstructions from serial sections of cryosubstituted cells. All planctomycete cells display a peripheral ribosome-free region, termed here the paryphoplasm, surrounding the perimeter of the cell, and an interior region including any nucleoid regions as well as ribosome-like particles, bounded by a single intracytoplasmic membrane (ICM), and termed the pirellulosome in Pirellula species. Immunogold labelling and RNase-gold cytochemistry indicates that in planctomycetes all the cell DNA is contained wholly within the interior region bounded by the ICM, and the paryphoplasm contains no DNA but at least some of the cell's RNA. The ICM in Isosphaera pallida and Planctomyces maris is invaginated such that the paryphoplasm forms a major portion of the cell interior in sections, but in other planctomycetes it remains as a peripheral zone. In the anaerobic ammonium-oxidising ("anammox" process) chemoautotroph "Candidatus Brocadia anammoxidans" the interior region bounded by ICM contains a further internal single-membrane-bounded region, the anammoxosome. In Gemmata obscuriglobus, the interior ICM-bounded region contains the nuclear body, a double-membrane-bounded region containing the cell's nucleoid and all genomic DNA in addition to some RNA. Shared features of cell compartmentalisation in different planctomycetes are consistent with the monophyletic nature of the planctomycetes as a distinct division of the Bacteria. The shared organisational plan for the planctomycete cell constitutes a new type not known in cells of other bacteria.

Taxonomic heterogeneity within the Planctomycetales as derived by DNA–DNA hybridization, description of Rhodopirellula baltica gen. nov., sp. nov., transfer of Pirellula marina to the genus Blastopirellula gen. nov. as Blastopirellula marina comb. nov. and emended description of the genus Pirellula

“…Analysis of cross-sections of strain SH 1 T as well as SH 796 (Gade et al, 2004) revealed several small structures in addition to a large central one. This microscopic appearance differs from that of the pirellulosome structure described for Pirellula staleyi and B. marina (Lindsay et al, 2001).…”

Proteomic analysis of carbohydrate catabolism and regulation in the marine bacteriumRhodopirellula baltica

“…As observed with other described Planctomycetes, cells of R. baltica contain membrane-separated intracytoplasmic compartments [31]. The internal region is termed pirellulosome and contains the riboplasm with ribosome-like particles and the condensed nucleoid (Fig.…”

Potential roles of anaerobic ammonium and methane oxidation in the nitrogen cycle of wetland ecosystems

“…Ladderanes have been applied as biomarkers for anammox abundance in anoxic waters of the Black Sea (Kuypers et al 2003), oxygen depleted zones of the ocean (Kuypers et al 2003;Hamersley et al 2007;Jaeschke et al 2009a), and in marine sediments ). One of the major octaheme cyctochrome c proteins of anammox bacteria (hydroxylamine or hydrazine oxidoreductase) was found to reside in the anammoxosome by immunogold labeling (Lindsay et al 2001) and cytochemical staining (van Niftrik et al 2008a, b). Recently, the genome of the wastewater anammox bacterium Kuenenia stuttgartiensis was elucidated using a metagenomic approach.…”