Spatial Simulations of Myxobacterial Development

Holmes, Antony B.; Kalvala, Sara; Whitworth, David E.

doi:10.1371/journal.pcbi.1000686

Cited by 29 publications

(41 citation statements)

References 38 publications

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“…Traffic jam aggregation model reproduces some but not all features of aggregation. Developmental aggregation of M. xanthus has been the subject of significant attention by the modeling community, and multiple mathematical models of aggregation have been published (4,8,19,20,21). Nevertheless, few of these models explicitly study dynamic aspects of aggregation, such as the merging or dispersal of aggregates or changes in the distribution of aggregates on an agar surface.…”

Section: Resultsmentioning

confidence: 99%

“…The nature of our inquiry required us to use a model of aggregation on a length scale at which multiple fruiting bodies will be formed (1 by 1 or 2 by 2 mm). Because of these constraints, we were not able to adopt any of the more sophisticated three-dimensional models of aggregation (4,20), as it would not be computationally feasible.…”

Section: Resultsmentioning

confidence: 99%

“…Under standard experimental conditions, a typical swarm of several million cells will produce hundreds of fruiting bodies over an area of less than 1 cm 2 . The principles underlying self-organization in swarming cannot be understood solely by available experimental approaches; thus, mathematical modeling has been used extensively to explore these emergent behaviors (4,7,8,18,19,20,21,25,26). These models have successfully uncovered sets of intercellular interactions that lead to patterns similar to those observed experimentally in M. xanthus.…”

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confidence: 99%

“…Furthermore, the process through which this ordered placement occurs is not reproduced in the traffic jam model for the formation of fruiting bodies. 4 , and 1.5% agar. Cells were harvested between Klett 80 and 120, when they were in mid-log phase.…”

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confidence: 99%

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Quantifying Aggregation Dynamics during Myxococcus xanthus Development

et al. 2011

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Under starvation conditions, a swarm of Myxococcus xanthus cells will undergo development, a multicellular process culminating in the formation of many aggregates called fruiting bodies, each of which contains up to 100,000 spores. The mechanics of symmetry breaking and the self-organization of cells into fruiting bodies is an active area of research. Here we use microcinematography and automated image processing to quantify several transient features of developmental dynamics. An analysis of experimental data indicates that aggregation reaches its steady state in a highly nonmonotonic fashion. The number of aggregates rapidly peaks at a value 2-to 3-fold higher than the final value and then decreases before reaching a steady state. The time dependence of aggregate size is also nonmonotonic, but to a lesser extent: average aggregate size increases from the onset of aggregation to between 10 and 15 h and then gradually decreases thereafter. During this process, the distribution of aggregates transitions from a nearly random state early in development to a more ordered state later in development. A comparison of experimental results to a mathematical model based on the traffic jam hypothesis indicates that the model fails to reproduce these dynamic features of aggregation, even though it accurately describes its final outcome. The dynamic features of M. xanthus aggregation uncovered in this study impose severe constraints on its underlying mechanisms.

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Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

mentioning

confidence: 99%

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confidence: 99%

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Quantifying Aggregation Dynamics during Myxococcus xanthus Development

et al. 2011

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“…The soil organism Myxococcus xanthus actively swarms away from the point of inoculation through a process termed gliding motility, which is mediated by two types of motility: A motility that occurs through an unknown mechanism, and S motility, which is powered by tfp retraction (4,5). M. xanthus swarming is a complex multicellular process that has been extensively studied, and in recent years a number of mathematical models have been developed to describe this behavior (6)(7)(8)(9).…”

mentioning

confidence: 99%

Self-organization of bacterial biofilms is facilitated by extracellular DNA

Gloag¹,

Turnbull²,

Huang

et al. 2013

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

250

269

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Twitching motility-mediated biofilm expansion is a complex, multicellular behavior that enables the active colonization of surfaces by many species of bacteria. In this study we have explored the emergence of intricate network patterns of interconnected trails that form in actively expanding biofilms of Pseudomonas aeruginosa. We have used high-resolution, phase-contrast time-lapse microscopy and developed sophisticated computer vision algorithms to track and analyze individual cell movements during expansion of P. aeruginosa biofilms. We have also used atomic force microscopy to examine the topography of the substrate underneath the expanding biofilm. Our analyses reveal that at the leading edge of the biofilm, highly coherent groups of bacteria migrate across the surface of the semisolid media and in doing so create furrows along which following cells preferentially migrate. This leads to the emergence of a network of trails that guide mass transit toward the leading edges of the biofilm. We have also determined that extracellular DNA (eDNA) facilitates efficient traffic flow throughout the furrow network by maintaining coherent cell alignments, thereby avoiding traffic jams and ensuring an efficient supply of cells to the migrating front. Our analyses reveal that eDNA also coordinates the movements of cells in the leading edge vanguard rafts and is required for the assembly of cells into the "bulldozer" aggregates that forge the interconnecting furrows. Our observations have revealed that large-scale self-organization of cells in actively expanding biofilms of P. aeruginosa occurs through construction of an intricate network of furrows that is facilitated by eDNA.collective behavior | t4p | type IV pili | tfp | swarming

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An Evo‐Devo Perspective on Multicellular Development of Myxobacteria

et al. 2017

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The transition to multicellularity, recognized as one the major transitions in evolution, has occurred independently several times. While multicellular development has been extensively studied in zygotic organisms including plant and animal groups, just a few aggregative multicellular organisms have been employed as model organisms for the study of multicellularity. Studying different evolutionary origins and modes of multicellularity enables comparative analyses that can help identifying lineage-specific aspects of multicellular evolution and generic factors and mechanisms involved in the transition to multicellularity. Among aggregative multicellular organisms, myxobacteria are a valuable system to explore the particularities that aggregation confers to the evolution of multicellularity and mechanisms shared with clonal organisms. Moreover, myxobacteria species develop fruiting bodies displaying a range of morphological diversity. In this review, we aim to synthesize diverse lines of evidence regarding myxobacteria development and discuss them in the context of Evo-Devo concepts and approaches. First, we briefly describe the developmental processes in myxobacteria, present an updated comparative analysis of the genes involved in their developmental processes and discuss these and other lines of evidence in terms of co-option and developmental system drift, two concepts key to Evo-Devo studies. Next, as has been suggested from Evo-Devo approaches, we discuss how broad comparative studies and integration of diverse genetic, physicochemical, and environmental factors into experimental and theoretical models can further our understanding of myxobacterial development, phenotypic variation, and evolution.

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Spatial Simulations of Myxobacterial Development

Cited by 29 publications

References 38 publications

Quantifying Aggregation Dynamics during Myxococcus xanthus Development

Quantifying Aggregation Dynamics during Myxococcus xanthus Development

Self-organization of bacterial biofilms is facilitated by extracellular DNA

An Evo‐Devo Perspective on Multicellular Development of Myxobacteria

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