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6 Gliding Motility of

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Abstract:

is one of the diverse bacteria that display gliding motility, involving two mechanisms, called adventurous (A) and social (S) gliding motility. The genetic and phenotypic analysis of mutants defective in gliding motility has shown that gliding motility is more complex than flagellum-dependent motility. The first molecular insights about the mechanisms of gliding motility were gleaned from the results of genetic studies performed by Hodgkin and Kaiser, who used chemical mutagens to generate mutations that affected gliding. The phenotypes of gliding mutants can be measured in terms of the differences in their velocities of gliding. The more detailed molecular genetic analysis of the two mechanisms of gliding motility in has been facilitated by the use of transposon mutagenesis. cells that have a functional A gliding system are able to move as isolated cells on a solid surface. The majority of mutations that abolish S motility affect the production of type IV pili (TFP), the exopolysaccharide (EPS) component of fibrils, or the lipopolysaccharide (LPS) moiety of O-antigen. The function of EPS in social motility has been elucidated by phenotypic analysis of mutants of lacking EPS, a secreted polymer comprised primarily of -acetylglucosamine (GlcNAc) and glucosamine (GlcN). has a complex life cycle. In the presence of adequate nutrients, the cells undergo vegetative growth and divide, but when the cells are starved of nutrients, they aggregate and form fruiting bodies containing myxospores.

Citation: Hartzell P, Shi W, Youderian P. 2008. 6 Gliding Motility of , p 103-122. In Whitworth D (ed), Myxobacteria. ASM Press, Washington, DC. doi: 10.1128/9781555815677.ch6

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Gene Expression and Regulation
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Type IV Pili
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Flagellar Motility
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Figures

Image of Figure 1
Figure 1

Wild-type cells use A and S gliding simultaneously to move over surfaces. (A) After 3 days of growth on 0.3% agar supplemented with Casitone–Tris–potassium phosphate–magnesium (CTPM), colonies of the wild-type strain display a characteristic wavelike pattern on 0.3% agar surface. Cells of the wild-type strain DK1622 (1.5 × 10 cells) were spotted on rich medium and incubated at 32°C for 3 days. The photograph of a portion of the colony was taken using a Nikon SMZU microscope (P. Hartzell). (B) Three individual cells (1), groups of cells (2), and phase-bright slime trails (3) are visible at the edge of a colony growing on rich medium with 1.5% agar.

Citation: Hartzell P, Shi W, Youderian P. 2008. 6 Gliding Motility of , p 103-122. In Whitworth D (ed), Myxobacteria. ASM Press, Washington, DC. doi: 10.1128/9781555815677.ch6
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Image of Figure 2
Figure 2

Genetic studies identify different classes of gliding mutants. The wild-type strain uses A and S motility to produce large colonies (AS, top panel) that spread over the agar surface. A single mutation in an S gene, including , , , or , results in a colony (AS, middle panel, left) with reduced spreading compared with the wild-type colony, which typically has a glossy, mounded core. At higher magnification, isolated cells can be seen at the colony edge. A single mutation in an A gene, including , , or , results in a colony (AS, middle panel, right) with reduced spreading compared with the wild-type colony. At higher magnification, no isolated cells can be seen at the colony edge. Introduction of a mutation in an A gliding gene into the S mutant and vice versa yields a colony (AS, bottom panel) that is devoid of motility. Cells of the double mutants do not move when viewed by time-lapse videomicroscopy at 30-s intervals, and the colonies possess a smooth edge. Single mutations in and give a similar colony phenotype. Photographs were taken using a Nikon SMZU microscope (P. Hartzell).

Citation: Hartzell P, Shi W, Youderian P. 2008. 6 Gliding Motility of , p 103-122. In Whitworth D (ed), Myxobacteria. ASM Press, Washington, DC. doi: 10.1128/9781555815677.ch6
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Image of Figure 3
Figure 3

The two gliding systems enable cells to adapt to different environments. The ability of cells to move over different agar surfaces supplemented with nutrients was quantified by measuring the spreading area (in square millimeters) after 5 days. Cells that lack A motility but retain S motility are able to spread on 0.3% agar, yet move poorly on 1.5% agar. The converse is true for cells that lack S motility, yet retain A motility. Black and gray bars indicate the colony surface area on 0.3 and 1.5% agar, respectively. The ratio of spreading on 0.3/1.5% agar surfaces for each strain is listed to the right of the bars. Data for DZ2 (on charcoal-yeast extract medium) are taken from Shi and Zusman (1993); all other values are from , and , for cells grown on CTPM medium.

Citation: Hartzell P, Shi W, Youderian P. 2008. 6 Gliding Motility of , p 103-122. In Whitworth D (ed), Myxobacteria. ASM Press, Washington, DC. doi: 10.1128/9781555815677.ch6
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Figure 4

Slime secretion (through slime nozzles) may be important for A motility. (A) Electron micrograph of a negatively stained isolated cell envelope of DK1622, an AS strain, showing one of the cell poles. The nozzles are visible as ring-shaped structures, which are clustered at the poles (long arrow). Along the rest of the cell surface, the density of nozzles is much smaller (short arrows). The inset shows a higher magnification of the nozzle array in the region indicated by the long arrow. Scale bars are 0.2 μm and 50 nm (inset). (B) A gallery of electron micrographs of negatively stained isolated nozzles from DK1622. In these top views, each cylindrically symmetric nozzle has an outer diameter of 14 nm, with a central hole of 6 nm. The diameter is similar to those of corresponding structures found in cyanobacteria, suggesting that the remainder of the nozzle may be of similar size. (C) Schematic illustration of the arrangement and location of the different cellular structures involved in gliding motility in . Nozzles are clustered at the two cell poles and pili at one pole. S motility is generated by the pili, which extend, attach to nearby cells, and then retract, pulling the cells together. The authors propose that A motility is driven by the secretion of mucilage from the nozzles (indicated as small circles). As the mucilage adheres to the substrate, further secretion drives the cell in the opposite direction. The observed reversals of movement would be caused by alternation of the active polar nozzle cluster. (D) Cartoon illustrating the proposed layout of the nozzles in the polar region shown in panel A. The nozzle cross sections shown are drawn with the same geometry as those found in cyanobacteria. Figure reprinted from with permission.

Citation: Hartzell P, Shi W, Youderian P. 2008. 6 Gliding Motility of , p 103-122. In Whitworth D (ed), Myxobacteria. ASM Press, Washington, DC. doi: 10.1128/9781555815677.ch6
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Figure 5

The interaction between EPS and TFP stimulates retraction of pili. (A) The interaction between TFP and EPS in wild-type cells enables TFP retraction and S motility. (B) The absence of EPS in EPS mutants abolishes the EPS interaction with TFP, resulting in overpiliation and defects in S motility. (C) The interaction between TFP and EPS present in slime trails guides cells along these trails.

Citation: Hartzell P, Shi W, Youderian P. 2008. 6 Gliding Motility of , p 103-122. In Whitworth D (ed), Myxobacteria. ASM Press, Washington, DC. doi: 10.1128/9781555815677.ch6
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Figure 6

Tgl stimulation. Stimulated recipient cells became motile and swarmed outward, while the donor strain remained nonmotile. The donor was found inside the original edge of the colony. A mutant carrying an A mutation (AS strain DK8602) was mixed with another nonmotile mutant strain (DK8601) and spotted on agar. (A) At 0 h, the mixed colony had a smooth edge (black arrowhead) because there were no motile cells (scale bar, 500 μm). (B) After several hours, the donor cells activated S motility in the mutant recipient cells by stimulation. The outward swarming of the stimulated recipients after 4 days is indicated by the arrowhead. This motility was transient; it lasted only 1 week. (C) Phase-contrast image of DK8601 (GFP donor cells) mixed 1:1 with a mixture of DK8607 (GFP recipient cells) and DK8602 (GFP recipient cells) at a 1:50 ratio. The original colony edge is indicated by the arrowhead. (D) Epifluorescent image of the field shown in panel C. The original colony edge is indicated by the dashed line. (E) Phase-contrast image of DK8602 (GFP recipient cells) mixed 1:1 with a mixture of DK8606 (GFP donor cells) and DK8601 (GFP donor cells) at a 1:50 ratio. (F) Epifluorescent image of panel E. Reprinted with permission from (Nudleman et al., 2005).

Citation: Hartzell P, Shi W, Youderian P. 2008. 6 Gliding Motility of , p 103-122. In Whitworth D (ed), Myxobacteria. ASM Press, Washington, DC. doi: 10.1128/9781555815677.ch6
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Figure 7

The MglA protein interacts with multiple protein partners to regulate gliding. MglA is related to monomeric GTPases, which cycle between active, GTP-bound, and inactive, GDP-bound states. MglB (triangle) is predicted to regulate the activity of MglA, perhaps by acting as an exchange factor. MglA has been shown to interact with MasK and AglZ. A mutation in suppresses the nonmotile phenotype of the mutation and restores S motility (Thomasson et al., 2002). AglZ, a coiled-coil protein required for A motility, was recovered from a yeast two-hybrid library probed with MglA as bait (Yang et al., 2004).

Citation: Hartzell P, Shi W, Youderian P. 2008. 6 Gliding Motility of , p 103-122. In Whitworth D (ed), Myxobacteria. ASM Press, Washington, DC. doi: 10.1128/9781555815677.ch6
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Tables

Generic image for table
Table 1

Genes known to be required for A motility

Citation: Hartzell P, Shi W, Youderian P. 2008. 6 Gliding Motility of , p 103-122. In Whitworth D (ed), Myxobacteria. ASM Press, Washington, DC. doi: 10.1128/9781555815677.ch6
Generic image for table
Table 2

Genes known to be required for S motility

Citation: Hartzell P, Shi W, Youderian P. 2008. 6 Gliding Motility of , p 103-122. In Whitworth D (ed), Myxobacteria. ASM Press, Washington, DC. doi: 10.1128/9781555815677.ch6

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