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The mechanics of flow, contractility and adhesion in soft-bodied locomotion

  • Author(s): Zhang, Shun
  • Advisor(s): del Álamo, Juan Carlos
  • et al.

Soft organisms including unicellular amoebae, slime molds and invertebrates without exoskeleton use similar physical mechanisms to adhere to and crawl over surfaces. Despite the wide range of length scales covered by these organisms (10 −5 m – 10 −1 m), and the variety of biological processes involved in the regulation of force generation, all these organisms apply waves of traction (i.e. shear) stresses on their substrate. Given this remarkable evolutionary conservation of the mechanics of soft adhesive locomotion, its study is relevant to a broad number of areas in medicine, ecology and engineering.

Soft adhesive locomotion has been studied theoretically and experimentally for over a century. However, given that most organisms control their size very tightly, the impossibility of decoupling lengthscale dependence from organism dependence has made it difficult to experimentally test theoretical hypotheses. In this work, we focused on the multinucleated slime mold Physarum polycephalum because it is possible to prepare motile amoeboid specimens of this organism with sizes spanning two orders of magnitude (10 −5 m – 10 −2 m). Given its relatively large size and simple structure, Physarum relies on periodic back-and-forth intracellular flows (a.k.a. shuttle streaming) to transport chemical signals such as Ca 2+ . In turn, these signals regulate the generation of contractile forces that drive intracellular flow and facilitate locomotion.

The main goal of this thesis was to study the dynamics and interplays of these biophysical processes, and their roles in the onset of locomotion and persistent directional migration. To this end, we combined measurements of traction force, fragment morphology, endoplasmic and ectoplasmic velocity, ectoplasmic microrheology properties and endoplasmic Ca 2+ concentration with experimental manipulations of cell-substrate adhesion, cortical strength and cell size. In parallel, we worked closely with mathematicians to develop a model of a motile fragment which includes forces from the viscous cytosol, a poro-elastic, contractile cytoskeleton and adhesive interactions with the substrate.

Our results suggest that the onset of locomotion is governed by an interfacial instability which is strongly affected by fragment size, cell-substrate adhesion and cortical strength. We also found that most migrating Physarum fragments exhibit two types of wave patterns in endoplasmic flow, contractility and chemical signaling. Slow-moving fragments display standing wave patterns similar to amoeboid cells such as leukocytes or Dictyostelium. Fastmoving fragments exhibit traveling wave patterns of traction stress, which are conserved in larger organisms such as annelids or gastropods, and are reminiscent of leg density waves in myriapod locomotion. We show that traveling waves of traction stress provide robust propulsive forces in the presence of heterogeneous friction from the environment, and require tight coordination between contractility and substrate adhesion.

We studied this hypothesis in more detail by investigating the mechanics of locomotion of the flatworm Schistosoma mansoni (the most prevalent human endoparasite) under varying levels of confinement, representative of the environments this flatworm encounters in its migratory route from the liver to the intestine. Our results reveal that S. mansoni migrates by exerting standing waves of traction stresses with its suckers under no or gentle confinement, but transitions to exerting traveling waves of traction stress along its body when crawling through in highly restrictive conditions.

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