Collective regulation of cell motility using an accurate density-sensing system

D’Alessandro, Joseph; Mas, Lauriane; Aubry, Laurence; Rieu, Jean-Paul; Rivière, Charlotte; Anjard, Christophe

doi:10.1098/rsif.2018.0006

Cited by 12 publications

(11 citation statements)

References 30 publications

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“…P- cells do not move; they emit signal at a constant strain-specific rate γ and sense it with a strain-specific sensitivity threshold θ. The assumption that P -cells do not move is consistent with experimental results showing a reduced movement of vegetative cells at high density (D’Alessandro et al, 2018). Within each time step dt , P -cells that sense a local signal density higher than the strain-specific sensitivity threshold θ, may become aggregating A -cells with a strain-specific probability λdt .…”

Section: Methodssupporting

confidence: 86%

Eco-evolutionary significance of 'loners'

Rossine

Martínez-García

Sgro

et al. 2018

Preprint

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Loners, individuals out-of-sync with a coordinated majority, occur frequently in nature. 20 Are loners incidental byproducts of large-scale synchronization attempts or are they part of a 21 mosaic of life-history strategies? Here, we provide the first empirical evidence of naturally 22 occurring heritable variation in loner behavior, using the social amoeba Dictyostelium discoideum. 23 Moreover, we show that Dictyostelium loners-cells that do not join the multicellular life-stage-24 result from a dynamic population-partitioning process. Underlying this partitioning, we find 25 evidence that each cell makes a stochastic, signal-based decision resulting in an imperfectly 26 synchronized multicellular development affected by both abiotic (environmental porosity) and 27 biotic (strain-specific signaling) factors. Finally, we predict that when strains differing in their 28 partitioning behavior co-occur, cross-signaling impacts slime-mold diversity across spatio-29 temporal scales. Loners are therefore critical to understanding collective and social behaviors, 30 multicellular development, and ecological dynamics in D. discoideum. More broadly, across taxa, 31 imperfect synchronization might be adaptive by enabling diversification of life-history strategies. 32 33 Collective behaviors, in which a large number of individuals exhibit some degree of behavioral 34 synchronization, are frequent across the tree of life and across spatio-temporal scales: from 35 microbial aggregates to the great wildebeest migration, from locust swarming to synchronized 36 bamboo flowering, from fish schooling to mechanical adaptation in honeybee clusters (Couzin &

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Section: Methodssupporting

confidence: 86%

Eco-evolutionary significance of 'loners'

Rossine

Martínez-García

Sgro

et al. 2018

Preprint

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“…Measurements of aerokinesis in homogenous environments were performed using a homemade glass-duralumin environmental chamber to perform random motility assays ( d’Alessandro et al, 2018 ; Golé et al, 2011 ).…”

Section: Methodsmentioning

confidence: 99%

Hypoxia triggers collective aerotactic migration in Dictyostelium discoideum

Cochet‐Escartin

Demircigil

Hirose

et al. 2021

eLife

Self Cite

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Using a self-generated hypoxic assay, we show that the amoeba Dictyostelium discoideum displays a remarkable collective aerotactic behavior. When a cell colony is covered, cells quickly consume the available oxygen (O2) and form a dense ring moving outwards at constant speed and density. To decipher this collective process, we combined two technological developments: porphyrin-based O2 -sensing films and microfluidic O2 gradient generators. We showed that Dictyostelium cells exhibit aerotactic and aerokinetic response in a low range of O2 concentration indicative of a very efficient detection mechanism. Cell behaviors under self-generated or imposed O2 gradients were modeled using an in silico cellular Potts model built on experimental observations. This computational model was complemented with a parsimonious ‘Go or Grow’ partial differential equation (PDE) model. In both models, we found that the collective migration of a dense ring can be explained by the interplay between cell division and the modulation of aerotaxis.

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“…Consistent with our experimental design, we started with a population of cells immediately after food exhaustion and assumed them to be in a preaggregating state, P. Following experimental results that show a reduced mobility of vegetative cells in crowded populations [22], we assume that P-cells do not move. P-cells emit extracellular signaling molecules at a strain-specific rate γ.…”

Section: An Abiotically Modulated Quorum-based Stochastic Process Canmentioning

confidence: 99%

Eco-evolutionary significance of “loners”

et al. 2020

View full text Add to dashboard Cite

Loners-individuals out of sync with a coordinated majority-occur frequently in nature. Are loners incidental byproducts of large-scale coordination attempts, or are they part of a mosaic of life-history strategies? Here, we provide empirical evidence of naturally occurring heritable variation in loner behavior in the model social amoeba Dictyostelium discoideum. We propose that Dictyostelium loners-cells that do not join the multicellular life stagearise from a dynamic population-partitioning process, the result of each cell making a stochastic, signal-based decision. We find evidence that this imperfectly synchronized multicellular development is affected by both abiotic (environmental porosity) and biotic (signaling) factors. Finally, we predict theoretically that when a pair of strains differing in their partitioning behavior coaggregate, cross-signaling impacts slime-mold diversity across spatiotemporal scales. Our findings suggest that loners could be critical to understanding collective and social behaviors, multicellular development, and ecological dynamics in D. discoideum. More broadly, across taxa, imperfect coordination of collective behaviors might be adaptive by enabling diversification of life-history strategies.

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Collective regulation of cell motility using an accurate density-sensing system

Cited by 12 publications

References 30 publications

Eco-evolutionary significance of 'loners'

Eco-evolutionary significance of 'loners'

Hypoxia triggers collective aerotactic migration in Dictyostelium discoideum

Eco-evolutionary significance of “loners”

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