Further characterization and in situ localization of chain-like aggregates of the gliding bacteria Myxococcus fulvus and Myxococcus xanthus

Abstract

For the first time, chain-like aggregates, called "strands," have been enriched from crude cell wall preparations of liquid-grown vegetative cells of two strains of Myxococcus xanthus. These strands are highly isomorphic to macromolecular structures, previously described for Myxococcus fulvus (Lünsdorf and Reichenbach, J. Gen. Microbiol. 135:1633-1641, 1989). The strands are morphologically composed of ring elements, consisting of six or more peripheral protein masses and possibly three small central masses. The ring elements are linked by two parallel strings of filamentous proteins, called elongated elements, which keep the ring elements at a constant distance. The overall dimensions of the ring elements are 16.6 ؎ 1.0 nm (n ‫؍‬ 55) for M. xanthus Mx x48 and 16.4 ؎ 1.5 nm (n ‫؍‬ 37) for M. xanthus DK 1622. The distance between the ring elements, as a measure of the length of the elongated elements, is 16.6 ؎ 1.1 nm (n ‫؍‬ 59) for strain Mx x48 and 15.5 ؎ 0.6 nm (n ‫؍‬ 41) for strain DK 1622. Characteristically, the strands and oligomeric forms thereof show a strict association with the outer membrane. In situ studies of freeze-fractured cells of M. fulvus showed ring elements, isomorphic to those described for M. xanthus, within the periplasm; they appeared in parallel rows just below the outer membrane but not in direct contact with the cytoplasmic membrane. A three-dimensional model summarizes the morphological data. It is hypothesized that the chain-like strands, as building blocks of a more complex belt-like continuum, represent the peripheral part of the gliding machinery, which transforms membrane potential energy into mechanical work.

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

“…So-called ' strands ', composed of ' rings ' and ' elongated elements ', were described as fragments from mechanically broken cells and they were shown to end up in a so-called ' belt ', about 300 nm in width, which was wrapped around the cell. Similar ' strands ' were found in M. xanthus (Freese et al, 1997). It is assumed that by conformational changes of ' rings ' relative towards the ' elongated elements ' along the ' strands ' of the ' belt ', gliding motility of M. fulvus is performed.…”

“…We suppose these circularly closed ' bands ' or ' belts ' to be directly associated with the peripheral part of the gliding machinery within the periplasmic space. 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).…”

“…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.…”

Gliding motility in cyanobacteria: observations and possible explanations

“…However, the lack of a plausible locomotive organelle and the occurrence of gliding movements in various organisms has, until now, challenged a general explanation. Consequently, a number of mechanisms have been proposed that include contractile elements (Halfen and Castenholz 1971), extrusion of slime (Hoiczyk and Baumeister 1998), rotary motors (Pate and Chang 1979), sulfonolipids (Abbant et al 1986), chainlike aggregates (Freese et al 1997), and anchorage sites of the cell surface (Lapidus and Berg 1982). In fact, it seems likely that gliding in different bacteria is based on different mechanisms and that even cyanobacteria use more than one mechanism.…”

The Junctional Pore Complex and the Propulsion of Bacterial Cells

“…Electron micrographs of Myxococcus cells reveal helical filamentous structures wrapping the periplasmic space [Burchard et al, 1977;Lunsdorf and Reichenbach, 1989;Freese et al, 1997;Lunsdorf and Schairer, 2001]. These filaments have been implicated in gliding motility, and recent experiments suggest that they are responsible for morphological changes, such as twisted forms, in actively gliding myxobacteria; these twisted morphologies are not observed in non-motile mutants [Lunsdorf and Schairer, 2001].…”