Evidence that gliding motility in prokaryotic cells is driven by rotary assemblies in the cell envelopes

Pate, Jack L.; Chang, Li-Yen Edward

doi:10.1007/bf02601737

Cited by 115 publications

(112 citation statements)

References 23 publications

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“…Previous studies indicated that proton motive force (PMF) powers gliding of Flavobacterium and related gliding bacteria (21)(22)(23)(24). To determine whether the SprB motion is powered by PMF, we examined the effects of carbonyl cyanide m-chlorophenylhydrazone (CCCP), a PMF uncoupler, on SprB motion.…”

Section: Resultsmentioning

confidence: 99%

Helical flow of surface protein required for bacterial gliding motility

Nakane

Satô

Wada

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

126

153

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Cells of Flavobacterium johnsoniae and of many other members of the phylum Bacteroidetes exhibit rapid gliding motility over surfaces by a unique mechanism. These cells do not have flagella or pili; instead, they rely on a novel motility apparatus composed of Gld and Spr proteins. SprB, a 669-kDa cell-surface adhesin, is required for efficient gliding. SprB was visualized by electron microscopy as thin 150-nm-long filaments extending from the cell surface. Fluorescence microscopy revealed movement of SprB proteins toward the poles of the cell at ∼2 μm/s. The fluorescent signals appeared to migrate around the pole and continue at the same speed toward the opposite pole along an apparent left-handed helical closed loop. Movement of SprB, and of cells, was rapidly and reversibly blocked by the addition of carbonyl cyanide m-chlorophenylhydrazone, which dissipates the proton gradient across the cytoplasmic membrane. In a gliding cell, some of the SprB protein appeared to attach to the substratum. The cell body moved forward and rotated with respect to this point of attachment. Upon reaching the rear of the cell, the attached SprB often was released from the substratum, and apparently recirculated to the front of the cell along a helical path. The results suggest a model for Flavobacterium gliding, supported by mathematical analysis, in which adhesins such as SprB are propelled along a closed helical loop track, generating rotation and translation of the cell body.cell motility | proton motive force | immunofluorescence microscopy | continuous track | left-handed helix C ells of Flavobacterium johnsoniae, and of many other members of the phylum Bacteroidetes, move rapidly over surfaces at speeds of 1-3 μm/s by gliding motility (1). These cells lack flagella and pili, and the mechanism of cell movement is poorly understood. Flavobacterium gliding is thought to rely on motors embedded in the cell envelope that propel large cell-surface adhesins such as SprB and related proteins (2). Deletion of sprB results in dramatic reduction in motility. Twelve Gld proteins also are required for gliding (3

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Section: Resultsmentioning

confidence: 99%

Helical flow of surface protein required for bacterial gliding motility

Nakane

Satô

Wada

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

126

153

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“…Insufficient resolution power is obtained by conventional light microscopy to observe the far submicron details that represent features of the actual gliding process. Until now, insights into the mode of action of gliding motility have been attempted to be obtained by the observation of latex beads that move along and around gliding cells (Pate & Chang, 1979 ;Lapidus & Berg, 1982 ;Ridgway & Lewin, 1988 ;Beatson & Marshall, 1994 H. L U $ NSDORF and H. U. SCHAIRER observed patterns of bead movement are directly correlated with the gliding process and its underlying molecular machinery (Lapidus & Berg, 1982). However, Ridgway & Lewin (1988) and Gorski et al (1991) have contradicted this strict association.…”

Section: Discussionmentioning

confidence: 99%

“…However, its design at the macromolecular level could not be elucidated and high-resolution electron microscopy data at this level remain fragmentary (Pate & Chang, 1979 ;Lu$ nsdorf & Reichenbach, 1989 ;Freese et al, 1997). In particular, the question of how the gliding machinery is organized at the septa of filamentous gliding bacteria is enigmatic.…”

Section: Discussionmentioning

confidence: 99%

“…Several models have been proposed which offer diverse mechanomacromolecular and physico-chemical solutions of how bacterial gliding motility is established (Burchard, 1981(Burchard, , 1984Castenholz, 1982 ;Pate, 1988 ;Dworkin, 1996 ;Spormann, 1999). From the literature, it can be learned that gliding motility is a rather complex phenomenon, based on and influenced by an intrinsic apparatus responsible for mechanical work (Burchard et al, 1977 ;Pate & Chang, 1979 ;Lu$ nsdorf & Reichenbach, 1989), motility-supporting extracellular slime (Humphrey et al, 1979 ;Sutherland & Thomson, 1975 ;Sutherland, 1979 ;Gorski et al, 1993), components of the outer membrane (Gorski et al, 1992 ;Abbanat et al, 1986) and surface active compounds (Keller et al, 1983).…”

Section: Introductionmentioning

confidence: 99%

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Frozen motion of gliding bacteria outlines inherent features of the motility apparatus

Lünsdorf

Schairer

2001

Microbiology

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High-resolution data of actively gliding wild-type bacteria of four different species and of four different gliding mutants of Myxococcus xanthus were obtained from scanning electron micrographs. By shock freezing and freeze drying, motility-associated surface patterns could be fixed and consequently distinct intermediate states of motion could be observed for the first time. It is shown that these topographic patterns are immediately lost when gliding motility is stopped by blocking the respiratory chain with potassium cyanide or sodium azide. From the surface topography, the mode of action of the gliding apparatus of all four bacterial species examined can be described as a twisted circularly closed ' band '. During gliding, groups of nodes of the supertwisted apparatus show evidence of travelling like waves along the trichomes. However, the spacing between the nodes is not constant but varies within a certain range. This indicates that they are flexibly modulated as a consequence of the gliding state of the individual trichome.

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“…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 cell or the cell wall (2,47), chain-like strands (31), anchorage sites of the cell surface (29), contractile surface appendages (33), cellular inclusions (rhapidosomes) (9), and extruded extracellular material (10,41).…”

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confidence: 99%

Envelope structure of four gliding filamentous cyanobacteria

1995

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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...

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Evidence that gliding motility in prokaryotic cells is driven by rotary assemblies in the cell envelopes

Cited by 115 publications

References 23 publications

Helical flow of surface protein required for bacterial gliding motility

Helical flow of surface protein required for bacterial gliding motility

Frozen motion of gliding bacteria outlines inherent features of the motility apparatus

Envelope structure of four gliding filamentous cyanobacteria

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