Anisotropic stretch biases the self-organization of actin fibers in multicellular Hydra aggregates

During development, groups of cells generate shape by coordinating their mechanical properties through an interplay of self-organization and pre-patterning. However, how mechanics participate in self-organized pattern formation remains unknown. To study this, we used the regenerative abilities of the cnidarian Hydra vulgaris , which displays a striking planar pattern of actin fibers at the organism scale. Cellular aggregates formed from dissociated Hydra cells initially lose all actin polarity yet can regenerate a long-range actin pattern within a week. We quantified the appearance of the actin pattern with orientational (nematic) and positional (smectic) order parameters and showed that the actin organization evolves over days from a disordered to an ordered state. During the first hours, the actin meshwork displayed spatial heterogeneity in the orientational order parameter, and ordered domains progressively grew and fused. To better understand the mechanism driving the ordering, we perturbed the tissue’s physical constraints. We showed that while topology and geometry do not have a direct effect, stretch can strongly bias the orientation of the actin meshwork within hours. Surprisingly, although the Wnt gradient is expected to play an essential role in the actin alignment, the stretch-associated alignment bias happened without a Wnt enrichment. This showed the role of tissue mechanics in the alignment of the actin fibers. Overall, we characterized the physical properties of a mechanochemical self-organization process from cells to a functional organism.