Phototaxis during the slug stage of Dictyostelium discoideum: a model study

Abstract

During the slug stage, the cellular slime mould Dictyostelium discoideum moves towards light sources. We have modelled this phototactic behaviour using a hybrid cellular automata/partial di¡erential equation model. In our model, individual amoebae are not able to measure the direction from which the light comes, and di¡erences in light intensity do not lead to di¡erentiation in motion velocity among the amoebae. Nevertheless, the whole slug orientates itself towards the light. This behaviour is mediated by a modi¢cation of the cyclic AMP (cAMP) waves. As an explanation for phototaxis we propose the following mechanism, which is basically characterized by four processes: (i) light is focused on the distal side of the slug as a result of the so-called`lens-e¡ect'; (ii) di¡erences in luminous intensity cause di¡erences in NH 3 concentration; (iii) NH 3 alters the excitability of the cell, and thereby the shape of the cAMP wave; and (iv) chemotaxis towards cAMP causes the slug to turn. We show that this mechanism can account for a number of other behaviours that have been observed in experiments, such as bidirectional phototaxis and the cancellation of bidirectionality by a decrease in the light intensity or the addition of charcoal to the medium.

Collective cell migration in development

“…The mechanisms might involve local changes in the speed of cAMP wave propagation, resulting in local changes of cell movement and the steering of the slug towards or away from light and temperature gradients. The photoreceptors and thermoreceptors that might modulate cAMP relay remain to be identified (Fisher et al, 1997;Maree et al, 1999;Miura and Siegert, 2000). Although the study of this simple organism has shed considerable light on the mechanisms that underlie collective cell migration, many detailed questions -especially with respect to the relative importance of signalling pathways and direct cell-cell interactions -remain to be resolved.…”

Dynamic mechanisms of blood vessel growth

“…The simulation results of the Hogeweg group at Utrecht University on the development of the cellular slime mould, Dictyostelium discoideum, have nevertheless shown that even apparently intentional behaviours (like phototaxis [1]) can arise from the uncoordinated interactions of a few cell types interacting via a few simple biophysical mechanisms. While the mechanisms (adhesion, chemotaxis, diffusion, light capture, stimulated secretion and stochastic differentiation) individually are incapable of producing complex behaviours and while single cells exhibiting combinations of these mechanisms are also very limited in their behaviours, the combination of multiple mechanisms and many cells can produce genuinely emergent complex behaviours.…”

How amoeboids self-organize into a fruiting body: Multicellular coordination in Dictyostelium discoideum

“…We have previously used the same model formalism, including the same processes of differential adhesion, cAMP signaling, and chemotaxis, to explain the aggregation of single amoebae into a mound and a moving slug (1), as well as to unravel the mechanisms behind thermotaxis and phototaxis, which direct a slug to a suitable site for culmination (2,3). These model studies together with the results reported in this paper demonstrate that the entire process of morphogenesis, except for the initiation and termination of the slug stage, can unfold without any need to change the parameters of these processes.…”

“…4, all prestalk and prespore cells produce NH 3 , which can also diffuse into the air. The inhibiting effect of NH 3 (n) on the cAMP dynamics is incorporated by increasing the value of parameter a ,n , which defines the excitability of the cell (see ref.…”

“…We have modeled the process of culmination by using a hybrid stochastic cellular automata (CA)͞partial differential equation model (1)(2)(3). Individual cells are modeled as a group of connected automata-i.e., the basic scale of the model is subcellular.…”