Characterization of gliding motility in Flexibacter polymorphus

Abstract

Motility of the marine gliding bacterium Flexibacter polymorphus was studied by using microcinematographic techniques. Following adhesion to a glass surface, multicellular filaments and individual cells usually began to glide within a few seconds at a speed of approximately 12 micron per second (at 23 degrees C). Adhesion to the glass surface was evidently mediated by multitudes of extremely fine extracellular fibrils. Gliding velocity was independent of filament length but directly related to electron-transport activity and substratum temperature in the range 3-35 degrees C. The rate of gliding was inversely related to medium viscosity, suggesting that the locomotor apparatus functions at constant torque. Forward motion was occasionally interrupted by direction reversals, somersaults (observed primarily in single cells of short filaments), or spinning of filaments tethered by one pole. The frequency of direction reversal was found to be an inverse function of filament length. Translational motility was invariably accompanied by sinistral revolution about the longitudinal axis of a filament. The sense and pitch of revolution were constant among filaments of different length. Polystyrene microspheres or India ink particles adsorbed to gliding cells were actively displaced in either direction, their movement tracing either a regular zigzag or helical path along the filament surface. Because microspheres were also observed to move on nonmotile filaments, particle translocation was evidently not obligatorily linked to gliding locomotion. Multiple particles adsorbed to a single filament often moved independently. The data are consistent with a motility mechanism involving limited motion in numerous mechanically independent (yet functionally coordinated) domains on the cell surface.

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

“…So-called ' strands ', as integral parts of the ' belt ', were found to be situated within the periplasmic space and in direct contact with the outer membrane, as was shown by ' in situ ' freeze-fracture studies of M. fulvus (Freese et al, 1997). This is consistent with the helicity, inferred from light microscopical studies of movement patterns of latex beads and ink particles of cytophagas and flexibacters (Lapidus & Berg, 1982 ;Ridgway & Lewin, 1988 ;Beatson & Marshall, 1994) or the appearance of slime threads that are helically wrapped around gliding filaments (Reichenbach, 1980 ;Halfen & Castenholz, 1970). These observations fit the presented ultrastructural data of dynamic states of actively gliding cells.…”

“…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.…”

“…If the adhesive zones of these force vectors have the same intensity of contact with the substratum, the translocating forces will neutralize each other and no net movement will occur. Ridgway & Lewin (1988) have already mentioned this problem. A simple solution is to postulate an uncoupling of those adhesive zones from the substratum which are oppositely oriented to the direction of cell locomotion.…”

The Screw-Like Movement of a Gliding Bacterium Is Powered by Spiral Motion of Cell-Surface Adhesins

“…SprB provides the adhesive, and rotary motors power the motion (8). As is evident from experiments or models presented by us and others (4,5,9,10,(19)(20)(21)(22), mobile cell-surface components are essential for gliding. The biochemical features of spiral tracks on which such components are loaded and their mode of integration with the rotary motor are not known.…”

Acetate acts as a protonophore and differentially affects bead movement and cell migration of the gliding bacterium Cytophaga johnsonae (Flavobacterium johnsoniae)

“…This putative relationship of bead movement to gliding ability has however been questioned by us and others because of contradictory observations (Ridgway & Lewin, 1988;Gorski et al, 1991). As the present study reveals, cells grown in or on media containing acetate at concentrations from 35 to 50 mM failed to move attached beads over their surfaces, while colony enlargement (spreading), which is a result of cell migration on the agar surface, was normal.…”