Quantifying Aggregation Dynamics during Myxococcus xanthus Development

Zhang, Haiyang; Angus, Stuart; Tran, Michael; Xie, Chunyan; Igoshin, Oleg A.; Welch, Roy D.

doi:10.1128/jb.05188-11

Cited by 23 publications

(30 citation statements)

References 27 publications

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“…S3 C and D). These results are in agreement with another report indicating that simulations driven solely by local cell density fail to correctly reproduce the number, growth rate, and size of aggregates (21).…”

Section: Resultssupporting

confidence: 93%

“…Previous hypotheses of the mechanistic basis for aggregation predicted that decreased cell movement inside aggregates was the major driver of aggregate growth (21,24,31,32,38). We tested the hypothesis that the observed decrease in cell movement at the higher cell densities inside aggregates is sufficient to drive aggregation by incorporating density dependence into the simulations.…”

Section: Resultsmentioning

confidence: 98%

“…Within 1 h, towers begin to form spatially stable aggregation centers. Although some aggregates mature into spore-filled fruiting bodies, many initially stable aggregates disseminate back into the biofilm (21). Few data exist on the cues and cell behaviors that lead to these emergent behaviors.…”

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confidence: 99%

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Data-driven modeling reveals cell behaviors controlling self-organization during Myxococcus xanthus development

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Schüttler

Igoshin

et al. 2017

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

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Collective cell movement is critical to the emergent properties of many multicellular systems, including microbial self-organization in biofilms, embryogenesis, wound healing, and cancer metastasis. However, even the best-studied systems lack a complete picture of how diverse physical and chemical cues act upon individual cells to ensure coordinated multicellular behavior. Known for its social developmental cycle, the bacterium Myxococcus xanthus uses coordinated movement to generate three-dimensional aggregates called fruiting bodies. Despite extensive progress in identifying genes controlling fruiting body development, cell behaviors and cell-cell communication mechanisms that mediate aggregation are largely unknown. We developed an approach to examine emergent behaviors that couples fluorescent cell tracking with datadriven models. A unique feature of this approach is the ability to identify cell behaviors affecting the observed aggregation dynamics without full knowledge of the underlying biological mechanisms. The fluorescent cell tracking revealed large deviations in the behavior of individual cells. Our modeling method indicated that decreased cell motility inside the aggregates, a biased walk toward aggregate centroids, and alignment among neighboring cells in a radial direction to the nearest aggregate are behaviors that enhance aggregation dynamics. Our modeling method also revealed that aggregation is generally robust to perturbations in these behaviors and identified possible compensatory mechanisms. The resulting approach of directly combining behavior quantification with data-driven simulations can be applied to more complex systems of collective cell movement without prior knowledge of the cellular machinery and behavioral cues.agent-based simulation | image processing | emergent behavior | fluorescent imaging | cell communication C ollective cell migration is essential for many developmental processes, including fruiting body development of myxobacteria (1) and Dictyostelium (2), embryonic gastrulation (3, 4), and neural crest development (5). Conversely, cancer cell metastases represent detrimental migratory events that disseminate dysfunctional cells (6). In all these processes, a population of cells leaves its current location and migrates in a coordinated manner to new locations where motility becomes reduced. Remarkable progress has been made in studying the intracellular machinery of these organisms (7). Much less is known about the systemlevel coordination of cell migration. Cell movement in these systems is a 3D, dynamic process coordinated by a combination of diverse physical and chemical cues acting on the cells (3,5,8). Recent developments in tracking individual cell movement in vivo have provided unprecedented detail and revealed surprising levels of heterogeneity (5, 7). Reverse engineering of how these individual cell movements lead to collective migration patterns has proved difficult. Whereas computational models are able to test whether a given set of ad hoc assumptions lead to e...

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Section: Resultssupporting

confidence: 93%

Section: Resultsmentioning

confidence: 98%

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Data-driven modeling reveals cell behaviors controlling self-organization during Myxococcus xanthus development

Cotter

Schüttler

Igoshin

et al. 2017

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

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“…A good example is the process of fruiting body formation in Myxococcus xanthus during the development stage, which can be induced by starvation. It was found that this densitydependent process closely resembles phase separation in passive systems (76). More specifically, it can be described by the phenomena of coarsening, nucleation and growth, and spinodal decomposition observed in material science.…”

Section: Individual Cells Versus Collective Behaviormentioning

confidence: 99%

Recent Advances and Future Prospects in Bacterial and Archaeal Locomotion and Signal Transduction

et al. 2017

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The structure and function of two-component and chemotactic signaling and different aspects related to the motility of bacteria and archaea are key research areas in modern microbiology. Escherichia coli is the traditional model organism used to study chemotaxis signaling and motility. However, the recent study of a wide range of bacteria and even some archaea with different lifestyles has provided new insight into the ecophysiology of chemotaxis, which is essential for the establishment of different pathogens or beneficial bacteria in a host. The expanded range of model organisms has also permitted the study of chemosensory pathways unrelated to chemotaxis, multiple chemotaxis pathways within an organism, and new types of chemoreceptors. This research has greatly benefitted from technical advances in the field of cryomicroscopy, which continues to reveal with increasing resolution the complexity and diversity of large protein complexes like the flagellar motor or chemoreceptor arrays. In addition, sensitive instruments now allow an increasing number of experiments to be conducted at the single-cell level, thereby revealing information that is beginning to bridge the gap between individual cells and population behavior. Evidence has also accumulated showing that bacteria have evolved different mechanisms for surface sensing, which appears to be mediated by flagella and possibly type IV pili, and that the downstream signaling involves chemosensory pathways and two-component-system-based processes. Herein, we summarize the recent advances and research tendencies in this field as presented at the latest Bacterial Locomotion and Signal Transduction (BLAST XIV) conference.KEYWORDS chemotaxis, flagella, flagellar motility, signal transduction, two-component regulatory systems T he capacity to sense and respond to changes in environmental cues is an essential feature of the prokaryotic lifestyle. As a consequence, bacteria and archaea have evolved an array of different molecular mechanisms that permit the detection of signals in order to generate appropriate cellular responses. These responses are mediated primarily by one-and two-component systems, as well as chemosensory signaling pathways (1-4). Whereas the former systems mediate changes primarily at the transcriptional level, chemosensory pathways form the basis for chemotaxis, the directed movement of prokaryotes in compound gradients. The study of signaling processes is not only of fundamental interest but may also contribute to the tackling of one of the central clinical problems, which is the increasing amount of antibiotic-resistant pathogens. There is now a significant amount of data indicating that interference with signal transduction systems, motility, and chemotaxis can be an alternative strategy to weaken or block pathogens (5, 6).In

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“…xanthus has been studied largely as a model organism to understand cellular motility and the development of self-organized swarming groups that aggregate to form sporulating fruiting bodies. Upon starvation, M. xanthus glides in a well-choreographed manner to aggregate into clusters containing roughly 10 6 cells, which then develop into M. xanthus fruiting bodies (8)(9)(10)(11)(12)(13). M. xanthus does not move by flagella but displays two distinct motility phenotypes described as A motility and S motility.…”

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Cell Division Resets Polarity and Motility for the Bacterium Myxococcus xanthus

et al. 2014

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e Links between cell division and other cellular processes are poorly understood. It is difficult to simultaneously examine division and function in most cell types. Most of the research probing aspects of cell division has experimented with stationary or immobilized cells or distinctly asymmetrical cells. Here we took an alternative approach by examining cell division events within motile groups of cells growing on solid medium by time-lapse microscopy. A total of 558 cell divisions were identified among approximately 12,000 cells. We found an interconnection of division, motility, and polarity in the bacterium Myxococcus xanthus. For every division event, motile cells stop moving to divide. Progeny cells of binary fission subsequently move in opposing directions. This behavior involves M. xanthus Frz proteins that regulate M. xanthus motility reversals but is independent of type IV pilus "S motility." The inheritance of opposing polarity is correlated with the distribution of the G protein RomR within these dividing cells. The constriction at the point of division limits the intracellular distribution of RomR. Thus, the asymmetric distribution of RomR at the parent cell poles becomes mirrored at new poles initiated at the site of division. Many approaches to study cell division utilize traits that readily allow the distinction of two progeny cells. For example, cells displaying "asymmetrical" division traits allow the clear distinction of numerous characteristics that can then be monitored while deciphering other unknowns. Caulobacter bacteria are among the best studied with this distinction (1), but other biological examples include: preneuron neuroblast brain cells, budding Saccharomyces cerevisiae, germ line cells of male Drosophila, endospore development by Bacillus species, and Mycobacterium species subjected to environmental nutrient stress (2, 3). While such explicitly distinct examples may be rare, nearly all types of cells display some asymmetrical properties when functioning properly. There are numerous examples of distinctive asymmetrical and polarized attributes of cells (4). However, one difficulty that remains in characterizing asymmetrical properties in biology is distinguishing the timing and order of those intra-and intercellular attributes that are transient in nature. Alternative to studying asymmetric cell types that can be readily differentiated, other research strategies to probe stages of division often examine stationary or immobilized cells.Myxococcus xanthus is one of many myxobacteria, common soil microbes that grow readily in environments rich in complex organics, such as those containing decaying plants (5) or other bacteria (6). M. xanthus cells exhibit a symmetric morphology. The specific mechanism and dynamics of M. xanthus cell division, like those of most nonmodel organisms, are not entirely known. M. xanthus is among many bacteria lacking a clear MinCD system that drives the recruitment of FtsZ for division. It is known that the middle of M. xanthus cells is marked by PomZ, w...

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Quantifying Aggregation Dynamics during Myxococcus xanthus Development

Cited by 23 publications

References 27 publications

Data-driven modeling reveals cell behaviors controlling self-organization during Myxococcus xanthus development

Data-driven modeling reveals cell behaviors controlling self-organization during Myxococcus xanthus development

Recent Advances and Future Prospects in Bacterial and Archaeal Locomotion and Signal Transduction

Cell Division Resets Polarity and Motility for the Bacterium Myxococcus xanthus

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