Nested Bacterial Boxes: Nuclear and Other Intracellular Compartments in Planctomycetes

Abstract

Bacteria in the phylum Planctomycetes and some related phyla challenge our concept of the typical bacterium as consisting of cells without internal compartments or membrane-bounded organelles. Cells of all species of planctomycetes examined consist of at least two major compartments, and there are two other types of compartmentation in which a third compartment is formed either by a double-membrane envelope around the nucleoid in the case of the aerobic Gemmata obscuriglobus or by a single but potentially energized membrane in the case of the anaerobic ammonium-oxidizing anammox planctomycetes. We examine here the nature of these planctomycete compartments in relation to function and their relationship to the endomembranes defining them, and discuss the implications of the remarkable compartment-confined process of protein uptake in Gemmata, which resembles receptor- and clathrin-mediated endocytosis of eukaryotes. Planctomycetes have implications for our understanding of the evolution of membrane-bounded organelles, of endomembranes, transport across endomembranes and membrane trafficking, and for how the complexity of a eukaryote style of cell organization could have originated.

Structural Studies of Planctomycete Gemmata obscuriglobus Support Cell Compartmentalisation in a Bacterium

“…The confirmation of membrane-bounded compartmentalization of the cytoplasm in a bacterium strengthens the view that planctomycete structure may form a model for understanding how eukaryote compartmentalization evolved, including the nucleus and its envelope [47], [48], [49]. It is entirely consistent with the existence of other remarkable similarities with eukaryote cell biology in this species such as endocytosis-like protein uptake [34].…”

Planctomycetes and macroalgae, a striking association

“…They share with archaea or eukaryotes some distinctive characteristics such as peptidoglycan-less cell walls of proteic nature (Lage, 2013), a complex system of endomembranes forming a unique cell plan (Lage et al, 2013; Santarella-Mellwig et al, 2013), the presence of compartments like the anammoxosome (Van Teeseling et al, 2013), budding reproduction in many of their members (Ward et al, 2006) and the lack of the division protein FtsZ (Pilhofer et al, 2008), endocytosis (Lonhienne et al, 2010) and the presence of membrane coat (MC)—like proteins (Santarella-Mellwig et al, 2010). Some of these features place planctomycetes in the center of the discussion of the eukaryotic cell origin (Devos and Reynaud, 2010; Reynaud and Devos, 2011; Fuerst and Sagulenko, 2013). …”

Evolutionary Cell Biology of Division Mode in the Bacterial Planctomycetes-Verrucomicrobia- Chlamydiae Superphylum

“…The case of Planctomycetes appears to be different. Since early analyses (König et al, 1984; Liesack et al, 1986; Stackebrandt et al, 1986), the absence of PG in Planctomycetes cell walls was not reconsidered, despite several investigations into these bacteria and their structure (Fuerst, 2005, 2013b; Fuerst and Sagulenko, 2013; Sagulenko et al, 2014). Planctomycetal sacculi was purified in the presence of SDS and high temperature, but instead of PG, a proteinaceous cell wall was found (Stackebrandt et al, 1986).…”