Motility induced fracture reveals a ductile to brittle crossover in the epithelial tissues of a simple animal

Abstract

8Animals are characterized by their movement, and their tissues are continuously subjected to dynamic force loading while they crawl, walk, run or swim 1 . Tissue mechanics fundamentally determine the ecological niches that can be endured by a living organism 2 . While epithelial tissues provide an important barrier function in animals, they are subjected to extreme strains during day to day physiological activities, such as breathing 1 , feeding 3 , and defense response 4 . However, failure or inability to withstand to these extreme strains can result in epithelial fractures 5, 6 and associated diseases 7, 8 . From a materials science perspective, how properties of living cells and their interactions prescribe larger scale tissue rheology and adaptive response in dynamic force landscapes remains an important frontier 9 . Motivated by pushing tissues to the limits of their integrity, we carry out a multi-modal study of a simple yet highly dynamic organism, the Trichoplax Adhaerens 10-12 , across four orders of magnitude in length (1 µm to 10 mm), and six orders in time (0.1 sec to 10 hours). We report the discovery of abrupt, bulk epithelial tissue fractures (∼10 sec) induced by the organism's own motility. Coupled with rapid healing (∼10 min), this discovery accounts for dramatic shape change and physiological asexual division in this early-divergent metazoan. We generalize our understanding of this phenomena by codifying it in a heuristic model, highlighting the fundamental questions underlying the debonding/bonding criterion in a soft-active-living material by evoking the concept of an 'epithelial alloy'. Using a suite of quantitative experimental and numerical techniques, we demonstrate a force-driven ductile to brittle material transition governing the morphodynamics of tissues pushed to the edge of rupture. This work contributes to an important discussion at the core of developmental biology 13-17 , with important applications to an emerging paradigm in materials and tissue engineering 5, 18-20 , wound healing and medicine 8, 21, 22 . 9 Tissues are the paragon example of a 'smart material'. Cells within a tissue may dynamically 10 reconfigure under stress 15, 23 , exhibit superelastic responses by localizing strain 19 , contract to actively 11 avoid rupture 10 , locally reinforce regions of tissue through recruitment 24 and other forms of mechanically 12 regulated feedback 25, 26 . Harnessing these properties promises valuable insights for synthetic adaptable 13 materials 18, 20, 27 . Many of these phenomena illustrate the role of mechanical feedback in service of tissues 14 maintaining their integrity under large strains. Here, we address the question -how do cellular tissues 15 behave on the threshold of failure? What determines if a tissue fractures or if it flows? We investigate this 16 question in a 'minimal tissue system' that is capable of highly adaptive and fast plastic deformation. 17 We experimentally study the dynamic epithelial tissues in the marine animal, the Trichoplax adhaerens. 1...

Embryonic tissues as active foams

“…The existence of bistability between configurations having small spaces between cells and configurations with large extracellular 'holes', could lead to hysteretic behavior and discontinuous transitions between these states if cells in tissues slowly change control parameters (average cortical tension or adhesion) during development. While most embryonic tissues likely avoid this regime, as it could lead to epithelial fracture and loss of its barrier function, recently reported dynamics and fracture of epithelial monolayers in the organism Trichoplax Adhaerens display features of this structural transition 9 .…”

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