Integrated mechanisms of cellular behavior : cell biology and biological physics of the slime mold Physarum polycephalum

Abstract

In its natural habitat, the plasmodial slime mold Physarum polycephalum forms extensive transport networks that can reach up to square meters in surface area. Under laboratory conditions, small spherical microplasmodia can be produced, which are only several hundred micrometers in diameter. These fragments can be used to study the reorganization of the network, the morphology of which depends on environmental factors. When nutrients are scarce, P. polycephalum forms fan-shaped, polarized mesoplasmodia with an internal vein system instead of a stationary network with reticulated external tubes. Mesoplasmodia are migrating, autonomous and unconnected subunits, which represent a starvation-induced foraging strategy. This thesis demonstrates that the number of mitochondria correlates with the metabolic state of the cell: In the absence of glucose, the slime mold is forced to switch to different metabolic pathways, which occur inside the mitochondria. A catabolic cue which stimulates mitochondrial biogenesis is discussed. A detailed and quantitative ultrastructural description of the three main morphotypes, macro-, meso-, and microplasmodia, is provided in this thesis. These investigations provide the basis for physical models of the system. Furthermore, the present work discusses the unique motility mechanisms of mesoplasmodia: At the posterior end, lateral contraction waves pump endoplasm through the veins towards the extending front. The internal flow channel system forms a cascade of forks, which acts as a low-pass filter and causes the isotropic extension of the cellular front. This effect is analyzed by a lumped parameter model, based on the analogy of hydro-dynamic phenomena to electric circuits. The direction of locomotion is controlled via an asymmetry in the elasticity of the actin cortex. A softness gradient exists along the anterior-posterior axis, with the front being the most elastic. The slime mold is capable of constructing networks optimized for transport, and exhibits other sophisticated and complex behaviors such as decision-making, efficient foraging, and memory. The structure of the cell and its dynamics are strongly interconnected. Large-scale patterns and other phenomena, which can be observed on the entire network, are based on locally occurring cellular and molecular processes. The interplay of these mechanistic interactions, and especially the resulting intracellular fluid flow, is hypothesized to underlie the information processing which is the basis of complex behavior in P. polycephalum. The ultrastructure of the cell is the substrate on which cellular computing takes place. Therefore, an understanding of the unique cell biology of the slime mold is necessary to study emergent phenomena such as minimal cognition.