Fluctuations and differential contraction during regeneration ofHydra vulgaristissue toroids

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 singlecell 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 * This paper is dedicated to Malcolm Steinberg.

Structural Inheritance of the Actin Cytoskeletal Organization Determines the Body Axis in Regenerating Hydra

“…In this case, the folded spheroid essentially maintains the polarity and fiber organization that it had in the parent animal and is thus likely to regenerate into an animal with normal morphology. In the second scenario, the ring buckles, as previously described (Krahe et al, 2013), and closes into a spheroid, in which the tissue is substantially deformed compared to its original layout in the parent animal ( Figure S4B). In this case, the resulting spheroid contains regions with distinct ectodermal fiber orientations as in spheroids formed from open rings and will likely regenerate abnormally.…”

“…Importantly, it is possible to follow the whole morphogenesis process in individual regenerating Hydra to get a holistic view of the pattern formation process (Gierer, 2012;Hobmayer et al, 2000;Seybold et al, 2016). The initial step in regeneration from tissue segments is the folding of the bilayer into a hollow spheroid (Bode and Bode, 1984;Krahe et al, 2013). The resulting spheroids undergo extensive shape fluctuations as they develop into small Hydra.…”

Mechanochemical Symmetry Breaking in Hydra Aggregates

“…Although corresponding timescales are within the range of viscoelastic processes, previous studies showed that purely elastic models reproduce Hydra tissue behavior (e.g., Krahe et al. ( 38 ), Mombach et al. ( 39 ), and Kücken et al.…”

How Hydra Eats

“…Relatedly, this study illustrates the benefits of expanding our repertoire of biological model systems to encompass the marvelous diversity presented by the tree of life. Nonstandard model organisms such as Hydra, Ciona, Trichoplax, and more broadly the vast array of creatures that cohabit our planet present evolutionary experiments, in which biological truths obscured by the idiosyncrasies of standard model organisms may be readily discerned (13)(14)(15)(16). Further, rapid improvements in genome sequencing and genetic manipulation are opening up new classes of organisms to sophisticated experiments that until recently could only be accomplished in a few species.…”