Ultrafast epithelial contractions provide insights into contraction speed limits and tissue integrity

Significance We report the fastest epithelial contractility observed to date in the primitive invertebrate Trichoplax adhaerens: Single-cell contraction events reduce cells’ apical area by 50% in one second, at least an order of magnitude faster than other examples. Typically, epithelial contractions enable embryonic systems to change shape during development. Their contractility machinery (actomyosin) is working against high load to achieve dramatic tissue deformation. Here we show that the same machinery can achieve the fast contraction we observe in T. adhaerens, in the lack of load. We also show that unique cell and tissue architecture indeed minimizes the load on a contracting cell. Finally, we suggest a physiological role for these contractions: maintaining the integrity of such a minimalistic tissue. By definition of multicellularity, all animals need to keep their cells attached and intact, despite internal and external forces. Cohesion between epithelial cells provides this key feature. To better understand fundamental limits of this cohesion, we study the epithelium mechanics of an ultrathin (∼25 μm) primitive marine animal Trichoplax adhaerens, composed essentially of two flat epithelial layers. With no known extracellular matrix and no nerves or muscles, T. adhaerens has been claimed to be 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 known in any metazoan, to be found in T. adhaerens dorsal epithelium (50% shrinkage of apical cell area within one second, at least an order of magnitude faster than other 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 nonmuscle 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 resist external stresses while avoiding tissue rupture (“active cohesion”), a concept that can be further applied to engineering of active materials.