Envelope structure of four gliding filamentous cyanobacteria

Abstract

The cell walls of four gliding filamentous Oscillatoriaceae species comprising three different genera were studied by freeze substitution, freeze fracturing, and negative staining. In all species, the multilayered gramnegative cell wall is covered with a complex external double layer. The first layer is a tetragonal crystalline S-layer anchored on the outer membrane. The second array is formed by parallel, helically arranged surface fibrils with diameters of 8 to 12 nm. These fibrils have a serrated appearance in cross sections. In all cases, the orientation of the surface fibrils correlates with the sense of revolution of the filaments during gliding, i.e., clockwise in both Phormidium strains and counterclockwise in Oscillatoria princeps and Lyngbya aeruginosa. The lack of longitudinal corrugations or contractions of the surface fibrils and the identical appearances of motile and nonmotile filaments suggest that this structure plays a passive screw thread role in gliding. It is hypothesized that the necessary propulsive force is generated by shear forces between the surface fibrils and the continuing flow of secreted extracellular slime. Furthermore, the so-called junctional pores seem to be the extrusion sites of the slime. In motile cells, these pores exhibit a different staining behavior than that seen in nonmotile ones. In the former, the channels of the pores are filled with electron-dense material, whereas in the latter, the channels appear comparatively empty, highly contrasting the peptidoglycan. Finally, the presence of regular surface structures in other gliding prokaryotes is considered an indication that comparable structures are general features of the cell walls of gliding microbes.Many multicellular, filamentous cyanobacteria move on solid surfaces by a type of motility described as gliding. Gliding is not exclusive to cyanobacteria but rather is widespread among prokaryotes (for a review, see references 3 and 20). It is unknown whether gliding motility is in all cases based on a common mechanism.Gliding of the nonpolar, filamentous cyanobacteria appears as a slow uniform motion, occasionally interrupted by reversals (13). Neither wriggling nor contraction nor peristaltic alterations of the filamentous trichomes are detectable by light microscopy (38). Members of the Oscillatoriaceae translocate in a highly coordinated manner. Translational movements are accompanied in most species by revolution around the long axis of the filament (4). While moving, the trichomes secrete slime which is left behind as a twisted and collapsed thin tube (20). The sense of revolution is unique and species specific (46), as evinced by the handedness of the rotation.The lack of flagella or of other plausible locomotive organelles is puzzling. Electron microscopic studies have so far failed to identify motor structures common among gliders. A number of unusual structures have been described which may or may not be related to this peculiar type of motility. This list comprises spinning discs (37), fibrils within the ce...

Oscillin, an extracellular, Ca2+‐binding glycoprotein essential for the gliding motility of cyanobacteria

“…Based on these findings, we have proposed previously that the fibrils play an important passive role in gliding by providing a screw thread surface, which guides the rotation of the filament (Hoiczyk and Baumeister, 1995). The biochemical analysis of oscillin presented in this paper further strengthens this hypothesis.…”

“…Two frequently suggested mechanisms are submicroscopical contractions of helically arranged fibrils within the cell walls or the extrusion of mucilage (Hä der and Hoiczyk, 1992). A reinvestigation of the cell walls of four gliding filamentous cyanobacteria comprising three different genera (Phormidium, Oscillatoria and Lyngbya) has shown that all species possess similar parallel arrays of 10-12 nm diameter fibrils on their outer surface (Hoiczyk and Baumeister, 1995). In all species studied so far, the orientation of these surface fibrils correlates with the sense of revolution of the filaments during gliding.…”

Fungal lectin of Peltigera canina induces chemotropism of compatible Nostoc cells by constriction-relaxation pulses of cyanobiont cytoskeleton

“…47 The lack of peripheral, motile organelles in mature, vegetative cells of Nostoc recently isolated from the lichen thallus suggests that their movement can be catalogs as chemotropism induced by the lichen lectin 17 since chemotaxis necessarily implies motile organelles. Filamentous cyanobacteria, including short, broken filaments and Nostoc hormogonia, move by gliding on a surface 48,49 being this gliding generated for forces of slime extrusion and surface waves. 50 Movement occurs in a direction parallel to the cell's long axis, is associated with the production of polysaccharide slime and requires attachment of the cell to a surface.…”

Cell rejuvenation and social behaviors promoted by LPS exchange in myxobacteria

“…The cells were fixed by gently covering the plate with 0.5% glutaraldehyde and incubating at room temperature for 45 min. Cells were collected by centrifugation, and the cell pellet was washed three times with 20 mM Hepes buffer (pH 7.5), cryo-fixated by high-pressure freezing using a Leica EM-PACT2 system, and freeze-substituted according to standard protocols (52). Briefly, the frozen cells were kept for 80 h in pure acetone containing 2% osmium tetroxide at −87°C, warmed stepwise (10°C/h) to room temperature, and washed with acetone to remove excess fixative.…”