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Miura, Kota (2000): Phototaxis of Dictyostelium discoideum Slugs. Dissertation, LMU München: Fakultät für Biologie



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.