"Frizzy" genes of Myxococcus xanthus are involved in control of frequency of reversal of gliding motility.

Abstract

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...

A biochemical oscillator explains several aspects ofMyxococcus xanthusbehavior during development

“…1a. On the other hand, a null mutation of FrzG does not produce a nonreversing phenotype, and the mutants are still able to coordinate their motion to form fruiting bodies (20,24); this observation excludes feedback (C in Fig. 1a).…”

“…C-signaling mutants are defective in aggregation and do not display developmental changes in reversal frequencies (12,13,16,17). Mutational studies show that myxobacterial Frz (''frizzy'') proteins modulate reversal frequencies in growing cells and affect their aggregation abilities (20)(21)(22)(23). Frz system components have many sequence homologies with those of the chemosensory signal transduction pathway (Che system) of E. coli (24).…”

Identification of a developmental chemoattractant in Myxococcus xanthus through metabolic engineering

“…surfaces along linear paths and reverse their direction of movement once every 6.8 min (24). Suppression of direction reversals in response to a chemoattractant is analogous to E. coli excitation (6,25).…”

Waves and aggregation patterns in myxobacteria

“…The ''frizzy'' (Frz) system of genes is homologous to chemosensory genes in enteric bacteria (15), and mutations in those genes affect the cell's reversal frequency (16). C-signal is required to trigger waves and streams at different stages of development via the Frz system.…”