Myxococcus xanthus is a Gram-negative bacterium with a complex life cycle that includes vegetative swarming and fruiting-body formation. Social (S)-motility (coordinated movement of large cell groups) requires both type IV pili and fibrils (extracellular matrix material consisting of polysaccharides and protein). Little is known about the role of this extracellular matrix, or fibril material, in pilus-dependent motility. In this study, mutants lacking fibril material and, therefore, S-motility were found to be hyperpiliated. We demonstrated that addition of fibril material resulted in pilus retraction and rescued this phenotype. The fibril material was further examined to determine the component(s) that were responsible for triggering pilus retraction. Protein-free fibril material was found to be highly active in correcting hyperpiliation. However, the amine sugars present in hydrolyzed fibril material, e.g., glucosamine and N-acetylglucosamine (GlcNAc) had no effect on fibril ؊ mutants, but, interestingly, cause hyperpiliation in wildtype cells. In contrast, chitin, a natural GlcNAc polymer, was found to restore pilus retraction in hyperpiliated mutants, indicating that a polysaccharide containing amine sugars is likely required for pilus retraction. These data suggest that the interaction of type IV pili with amine-containing polysaccharides on cell and slime-trail surfaces may trigger pilus retraction, resulting in S-motility and slime-trailing behaviors.gliding motility ͉ type IV pilus ͉ microbial development ͉ biofilm
The complex life cycle of Myxococcus xanthus includes predation, swarming, fruiting-body formation and sporulation. The genome of M. xanthus is large and comprises an estimated 7,400 open reading frames, of which approximately 605 code for regulatory genes. These include eight clusters of chemotaxis-like genes that define eight chemosensory pathways, most of which have dedicated functions. Although many of these chemosensory pathways have a role in controlling motility, at least two of these pathways control gene expression during development.
The bacterium Myxococcus xanthus has two motility systems: S motility, which is powered by type IV pilus retraction, and A motility, which is powered by unknown mechanism(s). We found that A motility involved transient adhesion complexes that remained at fixed positions relative to the substratum as cells moved forward. Complexes assembled at leading cell poles and dispersed at the rear of the cells. When cells reversed direction, the A-motility clusters relocalized to the new leading poles together with S-motility proteins. The Frz chemosensory system coordinated the two motility systems. The dynamics of protein cluster localization suggest that intracellular motors and force transmission by dynamic focal adhesions can power bacterial motility.During the exhibition of gliding motility, bacteria move across solid surfaces without the use of flagella (1). Glidingmotility is important for biofilm formation and bacterial virulence. Motility in Myxococcus xanthus, a Gram-negative rod-shaped bacterium, relies on two separate but coordinated motility engines. S motility is powered by type IV pili that are assembled at the leading cell pole; movement is produced as the pili bind to surface exopolysaccharides and are retracted, thereby pulling the cell forward (2). A motility, on the other hand, is not associated with pili or other obvious structures and is not well understood.To investigate the A-motility system, we studied AglZ, a protein that is essential for A motility but dispensable for S motility (fig. S1, A and B) (3). AglZ is similar to FrzS, an Smotility protein that oscillates from one cell pole to the other when cells reverse direction (4) ( fig. S1A) S2, B and C). We followed AglZ-YFP localization using time-lapse video microscopy: In fully motile cells, AglZ-YFP was localized in ordered clusters spanning the cell length; in stalled cells, it was localized at the leading cell pole (fig . S3).To study the link between the localization of AglZ-YFP and motility, we focused our observations on AglZ-YFP in fully motile cells. These cells showed an ordered array of AglZ-YFP clusters spanning the cell body (Fig. 1A). As cells moved forward, AglZ-YFP clusters maintained fixed positions with respect to the agar substrate rather than to their relative positions in the cell (Fig. 1A). We analyzed the clusters by taking line scans of the fluorescence intensity along motility paths for successive movie frames (Fig. 1B). To identify the position of peaks in multiple frames, we calculated a thresholded line-scan average (Fig. 1B) (5). This analysis not only located the positions of clusters shown in Fig. 1A, but also had the sensitivity to find other common peaks that were difficult to identify when viewing images with the eye. In every cell that was examined (n = 30), the AglZ-YFP clusters remained fixed relative to the substratum. The only AglZ-YFP clusters that moved relative to the cell body were located at the leading pole, which suggests that new sites were assembled at that pole. The number of clusters pe...
Myxococcus xanthus, a Gram-negative bacterium, has a complex life cycle that includes fruiting body formation. Frizzy (frz) mutants are unable to aggregate normally, instead forming frizzy filamentous aggregates. We have found that these mutants are defective in the control of cell reversal during gliding motility. Wild-type cells reverse their direction of gliding about every 6.8 min; net movement occurs since the interval between reversals can vary widely. The frzA-C, -E and -F mutants reverse their direction of movement very rarely, about once every 2 hr. These mutants cannot aggregate normally and give rise to frizzy filamentous colonies on fruiting agar or motility agar. In contrast, frzD mutants reverse their direction of movement very frequently, about once every 2.2 min; individual cells show little net movement and form smooth-edged "nonmotile" type colonies. Genetic analysis of thefiD locus shows that mutations in this locus can be dominant to the wild-type allele and that its gene product(s) must interact with the other frz gene products. Our results suggest that the frz genes are part of a system responsible for directed movement of this organism.Myxococcus xanthus is a Gram-negative rod-shaped bacterium that exhibits a complex life cycle consisting of a vegetative phase and a developmental phase (1-3). During the vegetative phase, cells move as large units called "swarms" or "hunting groups," which prey on other microorganisms or utilize organic substrates in their path. The mechanism of movement used by these bacteria is termed "gliding motility," which is usually described as movement in the direction of the long axis of the cells at a solid-liquid or an air-liquid interface (4). Since bacteria that exhibit gliding motility do not produce flagella or any other obvious motility organelle, several novel mechanisms have been proposed to explain this mechanism of movement (4-7). When M. xanthus cells are starved on a solid surface at high cell density, the developmental phase is initiated. Cells glide towards specific sites to form fruiting bodies, large aggregates or raised mounds in which sporulation later occurs. In M. xanthus, the mounds of myxospores are called fruiting bodies.As part of our studies of development in M. xanthus, we isolated a large number of mutants that were defective in fruiting body formation (8). One class of nonfruiting mutants were called "frizzy" since these cells, when plated on fruiting agar, formed frizzy filament-like aggregates in contrast to discrete mounds (9). The cells within the filaments sporulated normally. Since nonfruiting mutants of M. xanthus show only a limited number of phenotypes (8), we became interested in these relatively infrequent but distinctive aggregation-defective mutants. Transposon TnS insertions linked to a frizzy (frz) mutation were isolated (10) and used to map the various mutants in our collection (9). A search through 36 mutants exhibiting the frizzy phenotype showed that all were linked to the same Tn5 insertion sites. Three-fact...
Dual motility systems are common in the microbial world. Many flagellated bacteria (e.g., Vibrio and Proteus) are able to produce two types of flagella under different conditions (1-6). Most of these bacteria inhabit very complex environments and their multiple motility systems have different selective advantages that enable them to adapt to a variety of physiological and ecological environments. One of the best understood examples is Vibrio parahaemolyticus. When the bacterium is grown in liquid, it produces a single sheathed polar flagellum that is used for swimming; when grown on a solidified medium, it produces numerous unsheathed lateral flagella that are responsible for swarming over the solid surface (5, 7-9). Myxococcus xanthus is a gliding bacterium that can move on a solid surface without flagella (for recent reviews, see refs. 10 and 11). The mechanism of gliding motility is still largely unknown; however, genetic and morphological analyses suggest that M. xanthus also contains dual motility systems: (i) system A is required for the movement of single cells or small groups of cells (Fig. lj) and has at least 21 genetic loci; (ii) system S is mainly involved in the movement of cells in groups (Fig. lk) and has at least 10 genetic loci (12)(13)(14). Although the genes for A-and S-motility (12-17) and the cell surface structure related to A-and S-motility (18-22) have been partially characterized, little is known about the physiological differences of the two motility systems in M.xanthus.In this paper, we report that A-motility and S-motility show different selective advantages on different surfaces: A-motility allows cells to move better than S-motility on relatively firm and dry surfaces, whereas S-motility allows cells to move much better on relatively soft and wet surfaces. These results show that, like flagellated bacteria, the dual motility systems in gliding bacteria allow cells to adapt to a variety of physiological and ecological environments.
Although flagella are the best-understood means of locomotion in bacteria [1], other bacterial motility mechanisms must exist as many diverse groups of bacteria move without the aid of flagella [2-4]. One unusual structure that may contribute to motility is the type IV pilus [5,6]. Genetic evidence indicates that type IV pili are required for social gliding motility (S-motility) in Myxococcus, and twitching motility in Pseudomonas and Neisseria [6,7]. It is thought that type IV pili may retract or rotate to bring about cellular motility [6,8], but there is no direct evidence for the role of pili in cell movements. Here, using a tethering assay, we obtained evidence that the type IV pilus of Myxococcus xanthus functions as a motility apparatus. Pili were required for M. xanthus cells to adhere to solid surfaces and to generate cellular movement using S-motility. Tethered cells were released from the surface at intervals corresponding to the reversal frequency of wild-type cells when gliding on a solid surface. Mutants defective in the control of directional movements and cellular reversals (frz mutants) showed altered patterns of adherence that correlate reversal frequencies with tethering. The behavior of the tethered cells was consistent with a model in which the pili are extruded from one cell pole, adhere to a surface, and then retract, pulling the cell in the direction of the adhering pili. Cellular reversals would result from the sites of pili extrusion switching from one cell pole to another and are controlled by the frz chemosensory system.
Myxococcus xanthus is a Gram-negative bacterium that glides over surfaces without the aid of flagella. Two motility systems are used for locomotion: social-motility, powered by the retraction of type IV pili, and adventurous (A)-motility, powered by unknown mechanism(s). We have shown that AgmU, an A-motility protein, is part of a multiprotein complex that spans the inner membrane and periplasm of M. xanthus. In this paper, we present evidence that periplasmic AgmU decorates a looped continuous helix that rotates clockwise as cells glide forward, reversing its rotation when cells reverse polarity. Inhibitor studies showed that the AgmU helix rotation is driven by proton motive force (PMF) and depends on actin-like MreB cytoskeletal filaments. The AgmU motility complex was found to interact with MotAB homologs. Our data are consistent with a mechanochemical model in which PMFdriven motors, similar to bacterial flagella stator complexes, run along an endless looped helical track, driving rotation of the track; deformation of the cell surface by the AgmU-associated proteins creates pressure waves in the slime, pushing cells forward.
SummaryThe Frz chemosensory system controls directed motility in Myxococcus xanthus by regulating cellular reversal frequency. M. xanthus requires the Frz system for vegetative swarming on rich media and for cellular aggregation during fruiting body formation on starvation media. The Frz signal transduction pathway is formed by proteins that share homology with chemotaxis proteins from enteric bacteria, which are encoded in the frzA-F putative operon and the divergently transcribed frzZ gene. FrzCD, the Frz system chemoreceptor, contains a conserved C-terminal module present in methyl-accepting chemotaxis proteins (
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