Phototaxis of Dictyostelium discoideum Slugs

During the slug stage of cellular slime mold Dictyostelium
discoideum, up to 105 cells coordinate their movement and migrate
as a single organism. Slugs have a cylindrical shape with tip and
tail; their morphological polarity corresponds to the polarity of
migration. A large body of results suggest that cyclic AMP-mediated
cell-cell signaling is the mechanism coordinating multicellular
movement. Waves of cyclic AMP generated at the anterior tip
propagate towards the tail and induce the chemotactic movement of
cells toward the tip. Slugs exhibit highly sensitive environmental
reactions: phototaxis, chemotaxis and thermotaxis. Although many
studies have investigated how Dictyostelium slugs move toward a
light source, the mechanism of phototaxis is still unclear. It has
been known that slugs turn towards the light at the anterior end.
In addition, previous research identified mutations and drug
treatments that interfere with phototaxis but the strategy for
analyzing phototaxis has been limited to low resolution both
temporarily and spatially. In this thesis methods have been
developed to analyze phototactic behavior on two different scales,
the slug level and cellular level. The analyses revealed dynamic
features of slug behavior during phototaxis which have not been
previously described. Following light irradiation slugs moved with
approximately 50% higher speed; they showed prominent serpentine
movement of their tip as if they were scanning and correcting
migration direction; they elongated and decreased the diameter of
their body; and their tip remained lifted off the substrate for
long periods. The analysis of cell movement during phototactic
turning showed that the cell movement pattern was unlike any
predicted from earlier hypotheses. Some cells in the anterior zone
moved away from the light source across the slug, thus increasing
the volume on the “dark” side (“asymmetric cell accumulation”) and
bending the anterior zone like a lever-arm toward the light source.
Furthermore, it was discovered that light irradiation enhances
secretion of cyclic AMP from the slug and that light interferes
with cyclic AMP cell-cell signaling during other multicellular
stages as well. A model for phototaxis has been proposed based on
these results. Laterally irradiated light is focused on the distal
side of the slug by a lens effect and locally induces cyclic AMP
release. Some cells accumulate chemotactically on the side away
from the light source and cause a bending of the anterior zone
towards the light source. Since cell movement within the slug is
organized by cyclic AMP waves, light induced cyclic AMP release
interferes with the endogenous signaling pattern. The consequence
is an overall change in the shape and the behavior of slug. The
mechanism by which light induces the release of cyclic AMP from
slug cells may involve a histidine kinase phosphorelay pathway,
since such a pathway is known to be functional in Dictyostelium and
is used for environmental responses in many other organisms.