Coherent directed movement toward food modeled in
            <i>Trichoplax</i>
            , a ciliated animal lacking a nervous system

Smith, Carolyn L.; Reese, Thomas S.; Govezensky, Tzipe; Barrio, Rafael A.

doi:10.1073/pnas.1815655116

Cited by 56 publications

(49 citation statements)

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“…Their trajectories resemble those of random walkers (Ueda et al 1999). However, in the presence of a focal concentration of food, they exhibit chemotaxis, moving preferentially in the direction of the food (Smith et al 2019). Chemotaxis toward a focal concentration of glycine also has been reported (Heyland et al 2014).…”

Section: Feeding Behaviormentioning

confidence: 72%

“…Chemotaxis toward a focal concentration of glycine also has been reported (Heyland et al 2014). Chemotaxis has been proposed to arise from directed movement of the ciliated VEC, each independently sensing and responding to the chemoattractant (Smith et al 2019).…”

Section: Feeding Behaviormentioning

confidence: 91%

“…They possess just six morphologically distinct cell types (Smith et al 2014), fewer than any other animals except some larval or parasitic animals. Although they lack neurons and muscles, they display coordinated behavior during feeding (Smith et al 2015) and are capable of chemotaxis (Smith et al 2019).…”

Section: Introductionmentioning

confidence: 99%

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Insights into the evolution of digestive systems from studies of Trichoplax adhaerens

Smith

Mayorova

2019

Cell Tissue Res

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Trichoplax, a member of the phylum Placozoa, is a tiny ciliated marine animal that glides on surfaces feeding on algae and cyanobacteria. It stands out from other animals in that it lacks an internal digestive system and, instead, digests food trapped under its lower surface. Here we review recent work on the phenotypes of its six cell types and their roles in digestion and feeding behavior. Phylogenomic analyses place Placozoa as sister to Eumetazoa, the clade that includes Cnidaria and Bilateria. Comparing the phenotypes of cells in Trichoplax to those of cells in the digestive epithelia of Eumetazoa allows us to make inferences about the cell types and mode of feeding of their ancestors. From our increasingly mechanistic understanding of feeding in Trichoplax, we get a glimpse into how primitive animals may have hunted and consumed food prior to the evolution of neurons, muscles, and internal digestive systems.

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Section: Feeding Behaviormentioning

confidence: 72%

Section: Feeding Behaviormentioning

confidence: 91%

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Insights into the evolution of digestive systems from studies of Trichoplax adhaerens

Smith

Mayorova

2019

Cell Tissue Res

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“…In an effort to distill this essential discussion, we reformulated this central question as a competition between edge-formation and neighbor exchange mediated by cell-cell junction forming kinetics in a disordered model of an active tissue inspired by adhesive granular matter. In order to ground our model in experiments, we identify some key observable features that characterize epithelial tissues in the T. adhaerens : these include cell size, cell spatial distribution, distributed traction mediated propulsion 28, 29 and non-confluence. Our experimental observations encouraged us to reconsider the often useful assumptions: (i) local cell mechanical uniformity, (ii) tissue confluence, and (iii) the surface energy of cell-cell interactions constructed from a seperation of timescales (Extended Data Fig.…”

Section: Figurementioning

confidence: 99%

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

Prakash

Bull

2019

Preprint

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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...

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“…With this model setup, we consider collective cell movement as an emergent driver of multicellularity. Collective movement is important in simpler multicellular organisms [21–23] as well as in many processes within complex multicellular organisms, such as embryogenesis, tissue repair and cancer [24, 25], and has been modelled extensively [26–32]. In our model, cells perform chemotaxis towards the source of a noisy, shallow chemokine gradient.…”

Section: Introductionmentioning

confidence: 99%

Evolution of multicellularity by collective integration of spatial information

Colizzi

Vroomans

Merks

2020

Preprint

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10At the origin of multicellularity, cells may have evolved aggregation in 11 response to predation, for functional specialisation or to allow large-scale 12 integration of environmental cues. These group-level properties emerged 13 from the interactions between cells in a group, and determined the selection 14 pressures experienced by these cells. 15 We investigate the evolution of multicellularity with an evolutionary 16 model where cells search for resources by chemotaxis in a shallow, noisy 17 gradient. Cells can evolve their adhesion to others in a periodically chang-18 ing environment, where a cell's fitness solely depends on its distance from 19 the gradient source. 20 We show that multicellular aggregates evolve because they perform chemo-21 taxis more efficiently than single cells. Only when the environment changes 22 too frequently, a unicellular state evolves which relies on cell dispersal. Both 23 strategies prevent the invasion of the other through interference competition, 24 creating evolutionary bi-stability. Therefore, collective behaviour can be an 25 emergent selective driver for undifferentiated multicellularity. 26 1 1 Introduction 27The evolution of multicellularity is a major transition in individuality, from au-28 tonomously replicating cells to groups of interdependent cells forming a higher-29 level of organisation [1, 2]. It has evolved independently several times across the 30 tree of life [3, 4]. Comparative genomics suggests [5], and experimental evolution 31 confirms [6, 7] that the increase of cell-cell adhesion drives the early evolution 32 of (undifferentiated) multicellularity. Increased cell adhesion may be temporally 33 limited and/or may be triggered by environmental changes (e.g. in Dictyostelids 34 and Myxobacteria [8, 9]). Moreover, multicellular organisation may come about 35 either by aggregation of genetically distinct cells or by incomplete separation after 36 cell division [8, 10]. 37The genetic toolkit and the cellular components that allow for multicellularity 38 -including adhesion proteins -pre-date multicellular species and are found in 39 their unicellular relatives [8,[11][12][13]. Aggregates of cells can organise themselves 40 by exploiting these old components in the new multicellular context, allowing 41 them to perform novel functions (or to perform old functions in novel ways) that 42 may confer some competitive advantage over single cells. Greater complexity can 43 later evolve by coordinating the division of tasks between different cell lineages 44 of the same organism (e.g. in the soma-germline division of labour), giving rise 45 to embryonic development. Nevertheless, the properties of early multicellular 46 organisms are defined by self-organised aggregate cell dynamics, and the space of 47 possible multicellular outcomes and emergent functions resulting from such self-48 organisation seems large -even with limited differential adhesion and signalling 49 between cells. However, the evolution of emergent functions as a consequence of 50 ad...

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Coherent directed movement toward food modeled in Trichoplax , a ciliated animal lacking a nervous system

Cited by 56 publications

References 56 publications

Insights into the evolution of digestive systems from studies of Trichoplax adhaerens

Insights into the evolution of digestive systems from studies of Trichoplax adhaerens

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

Evolution of multicellularity by collective integration of spatial information

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