Analysis of the Frz signal transduction system of <i>Myxococcus xanthus</i> shows the importance of the conserved C‐terminal region of the cytoplasmic chemoreceptor FrzCD in sensing signals

Bustamante, Vı́ctor H.; Martínez-Flores, Irma; Vlamakis, Hera; Zusman, David R.

doi:10.1111/j.1365-2958.2004.04221.x

Cited by 109 publications

(228 citation statements)

References 54 publications

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“…In this study, we used the Frizilator model for the intracellular reversal clock, because it is based on the frz chemosensory system, which has been shown to control cell reversals (19,31). This model is built on interactions and covalent modifications involving FrzF (a methyltransferase that may also be involved in signal input), FrzCD (a chemoreceptor which is subject to methylation and demethylation), and FrzE (a kinase͞response regulator fusion protein).…”

Section: Discussionmentioning

confidence: 99%

“…However, the model we constructed does not depend on the detailed biochemistry of the regulatory system; it is based only on the first property: that the clock is a limit cycle oscillation with an asymmetric wave form for the component receiving the contact signal (FrzF in the Frizilator model) (19). Cell contact has been shown to mediate intercell signaling and to effect the reversal cycle (9,30,31). The asymmetry of the clock wave form (property 1) is fulfilled by the Frizilator model.…”

Section: Discussionmentioning

confidence: 99%

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Accordion waves inMyxococcus xanthus

Sliusarenko

Neu

Zusman

et al. 2006

Proc. Natl. Acad. Sci. U.S.A.

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Myxococcus xanthus are Gram-negative bacteria that glide on solid surfaces, periodically reversing their direction of movement. When starved, M. xanthus cells organize their movements into waves of cell density that sweep over the colony surface. These waves are unique: Although they appear to interpenetrate, they actually reflect off one another when they collide, so that each wave crest oscillates back and forth with no net displacement. Because the waves reflect the coordinated back and forth oscillations of the individual bacteria, we call them ''accordion'' waves. The spatial oscillations of individuals are a manifestation of an internal biochemical oscillator, probably involving the Frz chemosensory system. These internal ''clocks,'' each of which is quite variable, are synchronized by collisions between individual cells using a contactmediated signal-transduction system. The result of collision signaling is that the collective spatial behavior is much less variable than the individual oscillators. In this work, we present experimental observations in which individual cells marked with GFP can be followed in groups of unlabeled cells in monolayer cultures. These data, together with an agent-based computational model demonstrate that the only properties required to explain the ripple patterns are an asymmetric biochemical limit cycle that controls direction reversals and asymmetric contact-induced signaling between cells: Head-to-head signaling is stronger than head-to-tail signaling. Together, the experimental and computational data provide new insights into how populations of interacting oscillators can synchronize and organize spatially to produce morphogenetic patterns that may have parallels in higher organisms.cell movement ͉ gliding ͉ morphogenesis ͉ myxobacteria ͉ pattern formation

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Accordion waves inMyxococcus xanthus

Sliusarenko

Neu

Zusman

et al. 2006

Proc. Natl. Acad. Sci. U.S.A.

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“…M. xanthus strains DZ2 (wild type), DZ4483 (⌬frzF), DZ4482 (⌬frzG), DZ4486 ( frzCD C ), and DZ10547 (pilA::gfp/pilAϩ) were used in this study (24,39). E. coli strain ␤2155 was used as prey (40).…”

Section: Methodsmentioning

confidence: 99%

“…E. coli strain ␤2155 was used as prey (40). For routine culturing, M. xanthus was grown in CYE broth and E. coli in LB broth (24,41). Kanamycin was supplied when appropriate at 100 g/ml and DAP at 150 g/ml.…”

Section: Methodsmentioning

confidence: 99%

“…The homologs in the M. xanthus Frz pathway that modify the FrzCD receptor are FrzF and FrzG, respectively (20). While cells lacking FrzF reverse direction of movement very rarely in comparison to wild type, a deletion of frzG does not lead to any obvious defect in the reversal frequency (24). To determine the impact of the Frz pathway on multicellular structures, we examined the wild-type, ⌬frzF, and ⌬frzG strains during gliding, fruiting body formation, and rippling behaviors (Fig.…”

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Predataxis behavior inMyxococcus xanthus

Berleman

Scott

Chumley

et al. 2008

Proc. Natl. Acad. Sci. U.S.A.

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Spatial organization of cells is important for both multicellular development and tactic responses to a changing environment. We find that the social bacterium, Myxococcus xanthus utilizes a chemotaxis (Che)-like pathway to regulate multicellular rippling during predation of other microbial species. Tracking of GFPlabeled cells indicates directed movement of M. xanthus cells during the formation of rippling wave structures. Quantitative analysis of rippling indicates that ripple wavelength is adaptable and dependent on prey cell availability. Methylation of the receptor, FrzCD is required for this adaptation: a frzF methyltransferase mutant is unable to construct ripples, whereas a frzG methylesterase mutant forms numerous, tightly packed ripples. Both the frzF and frzG mutant strains are defective in directing cell movement through prey colonies. These data indicate that the transition to an organized multicellular state during predation in M. xanthus relies on the tactic behavior of individual cells, mediated by a Che-like signal transduction pathway.chemotaxis ͉ morphogenesis ͉ predation ͉ rippling ͉ chemosensory

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Cell Interactions Guide the Swarming and Fruiting Body Development of Myxobacteria

Kaiser

2009

Bacterial Signaling

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Analysis of the Frz signal transduction system of Myxococcus xanthus shows the importance of the conserved C‐terminal region of the cytoplasmic chemoreceptor FrzCD in sensing signals

Cited by 109 publications

References 54 publications

Accordion waves inMyxococcus xanthus

Accordion waves inMyxococcus xanthus

Predataxis behavior inMyxococcus xanthus

Cell Interactions Guide the Swarming and Fruiting Body Development of Myxobacteria

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