Fluctuations and differential contraction during regeneration of Hydra vulgaris tissue toroids

TL;DR

This study investigates the mechanical processes and fluctuations involved in Hydra vulgaris tissue regeneration, emphasizing the role of actin structures and force dynamics in tissue folding and regeneration.

Contribution

It reveals the mechanical self-organization mechanisms and actin-driven force fluctuations underlying Hydra tissue regeneration, independent of biochemical signaling.

Findings

Mechanical fluctuations increase during tissue folding.

Actin ring contraction drives tissue folding dynamics.

Switching from tissue-bound to migrating cells occurs after folding failure.

Abstract

We studied regenerating bilayered tissue toroids dissected from Hydra vulgaris polyps and relate our macroscopic observations to the dynamics of force-generating mesoscopic cytoskeletal structures. Tissue fragments undergo a specific toroid-spheroid folding process leading to complete regeneration towards a new organism. The time scale of folding is too fast for biochemical signalling or morphogenetic gradients which forced us to assume purely mechanical self-organization. The initial pattern selection dynamics was studied by embedding toroids into hydro-gels allowing us to observe the deformation modes over longer periods of time. We found increasing mechanical fluctuations which break the toroidal symmetry and discuss the evolution of their power spectra for various gel stiffnesses. Our observations are related to single cell studies which explain the mechanical feasibility of the folding process. In addition, we observed switching of cells from a tissue bound to a migrating state after folding failure as well as in tissue injury. We found a supra-cellular actin ring assembled along the toroid's inner edge. Its contraction can lead to the observed folding dynamics as we could confirm by finite element simulations. This actin ring in the inner cell layer is assembled by myosin- driven length fluctuations of supra-cellular {\alpha}-actin structures (myonemes) in the outer cell-layer.