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Review
, 45, 21-39

Uncovering the Mystery of Gliding Motility in the Myxobacteria

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Review

Uncovering the Mystery of Gliding Motility in the Myxobacteria

Beiyan Nan et al. Annu Rev Genet.

Abstract

Bacterial gliding motility is the smooth movement of cells on solid surfaces unaided by flagella or pili. Many diverse groups of bacteria exhibit gliding, but the mechanism of gliding motility has remained a mystery since it was first observed more than a century ago. Recent studies on the motility of Myxococcus xanthus, a soil myxobacterium, suggest a likely mechanism for gliding in this organism. About forty M. xanthus genes were shown to be involved in gliding motility, and some of their protein products were labeled and localized within cells. These studies suggest that gliding motility in M. xanthus involves large multiprotein structural complexes, regulatory proteins, and cytoskeletal filaments. In this review, we summarize recent experiments that provide the basis for this emerging view of M. xanthus motility. We also discuss alternative models for gliding.

Figures

Figure 1
Figure 1
Interactions observed for proteins involved in gliding motility. Interactions identified from affinity pull-down and cross-linking experiments are shown with dashed lines, and interactions demonstrated by both biochemistry and in vivo genetic studies are shown with solid lines.
Figure 2
Figure 2
AglZ and AgmU clusters (indicated by white arrows) appear stationary as cells move forward. Gliding cells expressing AglZ-YFP or AgmU-mCherry were imaged by fluorescence microscopy at frequent intervals. (a) AglZ-YFP clusters appear to remain stationary with respect to the substratum as cells glide forward; this behavior is reminiscent of focal adhesion proteins in eukaryotic cells (adapted from Reference 56). (b) Cytoplasmic clusters of AgmU-mCherry appear similar to AglZ clusters (adapted from Reference 60).
Figure 3
Figure 3
Membrane/periplasm-associated AgmU decorates a closed helical loop that rotates as cells glide forward. (a) Deconvolved images of one fixed cell expressing AgmU::mCherry show that AgmU localizes along a looped helical track. (b) 3D reconstructions of the AgmU helix from three individual cells. (c) Time-lapse images of the rotating AgmU-mCherry helix in a cell moving on agar surface. (d ) agmU-mCherry pilA cells were suspended in 1% methylcellulose and the rotation was visualized by merging one frame (red; left panel ) with a frame recorded 2 s later ( green; middle panel ). In the merged images, neither the conformation nor the helical pitch of the AgmU helix changed, but a clear color shift is evident, indicating a rotational movement. (e) Polar view of the rotation of AgmU helix in 1% methylcellulose. All panels are adapted from Reference .
Figure 4
Figure 4
Nozzle structures and slime secretion in Myxococcus xanthus. (a) Electron micrograph of ribbon-like materials secreted from the cell pole. (b) Electron micrograph of the nozzle structures near the cell pole. Both panels are adapted from Reference , with the permission from Elsevier.
Figure 5
Figure 5
The focal adhesion model for gliding motility. In this model, large focal adhesion complexes penetrate the cell envelope, stick to the substratum at one end, and connect to cytoskeletal filaments at the other end. Motor proteins push backward (marked by small arrows) against those focal adhesion complexes, pushing the cells forward.
Figure 6
Figure 6
The helical rotor model. In this model, flagella motor homologs carry different protein cargos and ride on a looped helical track. (a,b) The high-drag cargos deform the cell envelope at the ventral side of cells, where the thrust is exerted. (c) The motors carrying high-drag cargos slow down at the sites of surface distortion, collecting in traffic jams that appear as stationary periodic clusters in the observations of AgmU and AglZ. All the panels are adapted from Reference .

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