A three-dimensional model of myxobacterial fruiting-body formation (original) (raw)

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...

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.

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.

ON MODELING COMPLEX COLLECTIVE BEHAVIOR IN MYXOBACTERIA

Advances in Complex Systems, 2006

This paper reviews recent progress in modeling collective behaviors in myxobacteria using lattice gas cellular automata approach (LGCA). Myxobacteria are social bacteria that swarm, glide on surfaces and feed cooperatively. When starved, tens of thousands of cells change their movement pattern from outward spreading to inward concentration; they form aggregates that become fruiting bodies. Cells inside fruiting bodies differentiate into round, nonmotile, environmentally resistant spores. Traditionally, cell aggregation has been considered to imply chemotaxis, a long-range cell interaction. However, myxobacteria aggregation is the consequence of direct cell-contact interactions, not chemotaxis. In this paper, we review biological LGCA models based on local cell-cell contact signaling that have reproduced the rippling, streaming, aggregating and sporulation stages of the fruiting body formation in myxobacteria.

Dynamic-energy-budget-driven fruiting-body formation in myxobacteria

2010

We develop an interacting particle model to simulate the life cycle of myxobacteria, which consists of two main stages-the swarming stage and the development ͑fruiting body formation͒ stage. As experiments have shown that the phase transition from swarming to development stage is triggered by starvation, we incorporate into the simulation a system of ordinary differential equations ͑ODEs͒ called the dynamic energy budget, which controls the uptake and use of energy by individuals. This inclusion successfully automates the phase transition in our simulation. Only one parameter, namely, the food density, controls the entire simulation of the life cycle.

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.

Role of streams in myxobacteria aggregate formation

Physical Biology - PHYS BIOL, 2004

Cell contact, movement and directionality are important factors in biological development (morphogenesis), and myxobacteria are a model system for studying cell–cell interaction and cell organization preceding differentiation. When starved, thousands of myxobacteria cells align, stream and form aggregates which later develop into round, non-motile spores. Canonically, cell aggregation has been attributed to attractive chemotaxis, a long range interaction, but there is growing evidence that myxobacteria organization depends on contact-mediated cell–cell communication. We present a discrete stochastic model based on contact-mediated signaling that suggests an explanation for the initialization of early aggregates, aggregation dynamics and final aggregate distribution. Our model qualitatively reproduces the unique structures of myxobacteria aggregates and detailed stages which occur during myxobacteria aggregation: first, aggregates initialize in random positions and cells join aggrega...