Interconnected Cavernous Structure of Bacterial Fruiting Bodies (original) (raw)
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Aggregation during Fruiting Body Formation in Myxococcus xanthus Is Driven by Reducing Cell Movement
Journal of Bacteriology, 2007
When starved, Myxococcus xanthus cells assemble themselves into aggregates of about 10(5) cells that grow into complex structures called fruiting bodies, where they later sporulate. Here we present new observations on the velocities of the cells, their orientations, and reversal rates during the early stages of fruiting body formation. Most strikingly, we find that during aggregation, cell velocities slow dramatically and cells orient themselves in parallel inside the aggregates, while later cell orientations are circumferential to the periphery. The slowing of cell velocity, rather than changes in reversal frequency, can account for the accumulation of cells into aggregates. These observations are mimicked by a continuous agent-based computational model that reproduces the early stages of fruiting body formation. We also show, both experimentally and computationally, how changes in reversal frequency controlled by the Frz system mutants affect the shape of these early fruiting bodies.
Phase transitions during fruiting body formation in Myxococcus xanthus
The formation of a collectively moving group benefits individuals within a population in a variety of ways such as ultra-sensitivity to perturbation, collective modes of feeding, and protection from environmental stress. While some collective groups use a single organizing principle, others can dynamically shift the behavior of the group by modifying the interaction rules at the individual level. The surface-dwelling bacterium Myxococcus xanthus forms dynamic collective groups both to feed on prey and to aggregate during times of starvation. The latter behavior, termed fruiting-body formation, involves a complex, coordinated series of density changes that ultimately lead to three-dimensional aggregates comprising hundreds of thousands of cells and spores. This multi-step developmental process most likely involves several different single-celled behaviors as the population condenses from a loose, two-dimensional sheet to a three-dimensional mound. Here, we use high-resolution microsc...
Phase transitions during fruiting body formation in Myxococcus
2014
The formation of a collectively moving group benefits individuals within a popula-tion in a variety of ways such as ultra-sensitivity to perturbation, collective modes of feeding, and protection from environmental stress. While some collective groups use a single organizing principle, others can dynamically shift the behavior of the group by modifying the interaction rules at the individual level. The surface-dwelling bac-terium Myxococcus xanthus forms dynamic collective groups both to feed on prey and to aggregate during times of starvation. The latter behavior, termed fruiting-body for-mation, involves a complex, coordinated series of density changes that ultimately lead to three-dimensional aggregates comprising hundreds of thousands of cells and spores. This multi-step developmental process most likely involves several different single-celled behaviors as the population condenses from a loose, two-dimensional sheet to a three-dimensional mound. Here, we use high-resolution micr...
Cell behavior and cell–cell communication during fruiting body morphogenesis in Myxococcus xanthus
Journal of Microbiological Methods, 2003
Formation of spatial patterns of cells from a mass of initially identical cells is a recurring theme in developmental biology. The dynamics that direct pattern formation in biological systems often involve morphogenetic cell movements. An example is fruiting body formation in the gliding bacterium Myxococcus xanthus in which an unstructured population of identical cells rearranges into an asymmetric, stable pattern of multicellular fruiting bodies in response to starvation. Fruiting body formation depends on changes in organized cell movements from swarming to aggregation. The aggregation process is induced and orchestrated by the cell-surface associated 17 kDa C-signal protein. C-signal transmission depends on direct contact between cells. Evidence suggests that C-signal transmission is geometrically constrained to cell ends and that productive C-signal transmission only occurs when cells engage in end-to-end contacts. Here, we review recent progress in the understanding of the pattern formation process that leads to fruiting body formation. Gliding motility in M. xanthus involves two polarly localized gliding machines, the S-machine depends on type IV pili and the A-machine seems to involve a slime extrusion mechanism. Using time-lapse video microscopy the gliding motility parameters controlled by the C-signal have been identified. The C-signal induces cells to move with increased gliding speeds, in longer gliding intervals and with decreased stop and reversal frequencies. The combined effect of the C-signal dependent changes in gliding motility behaviour is an increase in the net-distance travelled by a cell per minute. The identification of the motility parameters controlled by the C-signal in combination with the contact-dependent C-signal transmission mechanism have allowed the generation of a qualitative model for C-signal induced aggregation. In this model, the directive properties of the C-signal are a direct consequence of the contactdependent signal-transmission mechanism, which is a local event involving direct contact between cells that results in a global organization of cells. This pattern formation process does not depend on a diffusible substance. Rather it depends on a cellsurface associated signal to direct the cells appropriately.
A New Mechanism for Collective Migration in Myxococcus xanthus
Journal of Statistical Physics, 2007
Myxobacteria exhibit a complex life cycle characterized by a sequence of cell patterns that culminate in the formation of three-dimensional fruiting bodies. This paper provides indications that the specific cell shape of myxobacteria might play an important role in the different morphogenetic processes during the life cycle. We introduce a new mechanism for collective migration that can explain the formation of aligned cell clusters in myxobacteria. This mechanism does not depend on cell cooperation, and in particular it does not depend on diffusive signals guiding cell motion. A Cellular Potts Model (CPM) that captures the rod cell shape, cell stiffness and active motion of myxobacteria is presented. By means of numerical simulations of model cell populations where cells interact via volume exclusion, we provide evidence of a purely mechanical mechanism for collective migration, which is controlled by the cells' length-to-width aspect ratio.
Spatial Simulations of Myxobacterial Development
PLoS Computational Biology, 2010
Many bacteria exhibit multicellular behaviour, with individuals within a colony coordinating their actions for communal benefit. One example of complex multicellular phenotypes is myxobacterial fruiting body formation, where thousands of cells aggregate into large three-dimensional structures, within which sporulation occurs. Here we describe a novel theoretical model, which uses Monte Carlo dynamics to simulate and explain multicellular development. The model captures multiple behaviours observed during fruiting, including the spontaneous formation of aggregation centres and the formation and dissolution of fruiting bodies. We show that a small number of physical properties in the model is sufficient to explain the most frequently documented population-level behaviours observed during development in Myxococcus xanthus.
Pattern formation by a cell surface-associated morphogen in Myxococcus xanthus
Proceedings of the National Academy of Sciences, 2002
In response to starvation, an unstructured population of identical Myxococcus xanthus cells rearranges into an asymmetric, stable pattern of multicellular fruiting bodies. Central to this pattern formation process are changes in organized cell movements from swarming to aggregation. Aggregation is induced by the cell surface-associated C-signal. To understand how aggregation is accomplished, we have analyzed how C-signal modulates cell behavior. We show that C-signal induces a motility response that includes increases in transient gliding speeds and in the duration of gliding intervals and decreases in stop and reversal frequencies. This response results in a switch in cell behavior from an oscillatory to a unidirectional type of behavior in which the net-distance traveled by a cell per minute is increased. We propose that the C-signal-dependent regulation of the reversal frequency is essential for aggregation and that the remaining C-signal-dependent changes in motility parameters contribute to aggregation by increasing the net-distance traveled by starving cells per minute. In our model for symmetry-breaking and aggregation, C-signal transmission is a local event involving direct contacts between cells that results in a global organization of cells. This pattern formation mechanism does not require a diffusible substance or other actions at a distance. Rather it depends on contact-induced changes in motility behavior to direct cells appropriately
Bacterial populations provide interesting examples of how relatively simple signalling mechanisms can result in complex behaviour of the colony. A well studied model is myxobacteria; cells can coordinate themselves to form intricate rippling patterns and fruiting bodies using localised signalling. Our work attempts to understand and model this emergent behaviour. We developed an off-lattice Monte Carlo simulation of cell motility and show it can be used to generate both rippling and fruiting body formations. Keywords fruiting • Monte Carlo • morphogenesis • myxobacteria • rippling 1 Introduction Myxobacteria are Gram negative, soil dwelling bacteria, distinguished by a complex and social life cycle involving multicellular development [5,6]. In response to starvation, cells pass through several developmental stages over a 72 h period, culminating in the formation of fruiting bodies, large multicellular aggregates of approximately 100,000 cells, within which dormant cell-types called myxospores are formed (Fig. 1). The first of these stages is the rippling phase, occurring approximately 4 h into starvation; the population self-organises into mobile bands of cells, which reflect off one another, giving the appearance of travelling waves [9, 24] (See Fig. 2). It is thought that rippling is an emergent property of an increased reversal frequency, brought about by C-signal, a