Ultra-fast cellular contractions in the epithelium ofT. adhaerensand the “active cohesion” hypothesis

Abstract

AbstractBy definition of multi-cellularity, all animals need to keep their cells attached and intact, despite internal and external forces. Cohesion between epithelial cells provides this key feature. In order to better understand fundamental limits of this cohesion, we study the epithelium mechanics of an ultra-thin (~25 um) primitive marine animalTrichoplax adhaerens, composed essentially of two flat epithelial layers. With no known extra-cellular-matrix and no nerves or muscles,T. adhaerenswas claimed the “simplest known living animal”, yet is still capable of coordinated locomotion and behavior. Here we report the discovery of the fastest epithelial cellular contractions to date to be found inT. adhaerensdorsal epithelium (50% shrinkage of apical cell area within one second, at least an order of magnitude faster than known examples). Live imaging reveals emergent contractile patterns that are mostly sporadic single-cell events, but also include propagating contraction waves across the tissue. We show that cell contraction speed can be explained by current models of non-muscle actin-myosin bundles without load, while the tissue architecture and unique mechanical properties are softening the tissue, minimizing the load on a contracting cell. We propose a hypothesis, in which the physiological role of the contraction dynamics is to avoid tissue rupture (“active cohesion”), a novel concept that can be further applied to engineering of active materials.One Sentence SummaryWe report the fastest epithelial cell contractions known to date, show they fit the kinematics arising from current cytoskeletal models, and suggest the extreme tissue dynamics is a means to actively avoid rupture.