Rippling Patterns in Aggregates of Myxobacteria Arise from Cell-Cell Collisions

Börner, Uwe; Deutsch, Andreas; Reichenbach, Hans; Bär, Markus

doi:10.1103/physrevlett.89.078101

Cited by 81 publications

(101 citation statements)

References 32 publications

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“…Most have been cellular automata models (25)(26)(27)32) or continuum models based on delayed-feedback mechanisms (33). The model developed here was tailored to our monolayer experimental system.…”

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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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%

Accordion waves inMyxococcus xanthus

Sliusarenko

Neu

Zusman

et al. 2006

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

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“…Therefore, the negative feedback oscillator has a built-in refractory period. The necessity of the refractory period is one of the main predictions of the mathematical models for rippling (3)(4)(5).…”

Section: Resultsmentioning

confidence: 99%

“…A mathematical model for these waves and for the swirling aggregations that follow has been published (3,4). Alternative models of rippling sharing similar ingredients have been developed (5)(6)(7).…”

mentioning

confidence: 99%

A biochemical oscillator explains several aspects ofMyxococcus xanthusbehavior during development

Igoshin

Goldbeter²,

Kaiser³

et al. 2004

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

105

112

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During development, Myxococcus xanthus cells produce a series of spatial patterns by coordinating their motion through a contactdependent signal, the C-signal. C-signaling modulates the frequency at which cells reverse their gliding direction. It does this by interacting with the Frz system (a homolog of the Escherichia coli chemosensory system) via a cascade of covalent modifications. Here we show that introducing a negative feedback into this cascade results in oscillatory behavior of the signaling circuit. The model explains several aspects of M. xanthus behavior during development, including the nonrandom distribution of reversal times, and the differences in response of the reversal frequency to both moderate and high levels of C-signaling at different developmental stages. We also propose experiments to test the model.

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“…9 The second term corresponds to the compressibility of the cells and prevents cell disappearance; V(σ) is the volume in lattice sites of cell σ, V t its target volume, and λ V (τ) the strength of the volume constraint. 10 Instead of the surface-adhesion coefficients J(τ, τ′), we can use surface tensions γ(τ, τ′), defined as (11) Negative surface tensions correspond to mixing or dispersing cells, while positive surface tensions correspond to cell sorting. 9 Although we use a 2D model, the neighborhood description also applies in 3D.…”

Section: The Ggh Biofilm Modelmentioning

confidence: 99%

Simulation of single-species bacterial-biofilm growth using the Glazier-Graner-Hogeweg model and the CompuCell3D modeling environment

Popławski

Shirinifard²,

Swat³

et al. 2008

Mathematical Biosciences and Engineering

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The CompuCell3D modeling environment provides a convenient platform for biofilm simulations using the Glazier-Graner-Hogeweg (GGH) model, a cell-oriented framework designed to simulate growth and pattern formation due to biological cells' behaviors. We show how to develop such a simulation, based on the hybrid (continuum-discrete) model of Picioreanu, van Loosdrecht, and Heijnen (PLH), simulate the growth of a single-species bacterial biofilm, and study the roles of cellcell and cell-field interactions in determining biofilm morphology. In our simulations, which generalize the PLH model by treating cells as spatially extended, deformable bodies, differential adhesion between cells, and their competition for a substrate (nutrient), suffice to produce a fingering instability that generates the finger shapes of biofilms. Our results agree with most features of the PLH model, although our inclusion of cell adhesion, which is difficult to implement using other modeling approaches, results in slightly different patterns. Our simulations thus provide the groundwork for simulations of medically and industrially important multispecies biofilms.

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Rippling Patterns in Aggregates of Myxobacteria Arise from Cell-Cell Collisions

Cited by 81 publications

References 32 publications

Accordion waves inMyxococcus xanthus

Accordion waves inMyxococcus xanthus

A biochemical oscillator explains several aspects ofMyxococcus xanthusbehavior during development

Simulation of single-species bacterial-biofilm growth using the Glazier-Graner-Hogeweg model and the CompuCell3D modeling environment

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