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Signalling centre vortices coordinate collective behaviour in social amoebae

Hugh Z Ford, Angelika Manhart, Jonathan R Chubb
doi: https://doi.org/10.1101/2022.01.07.475371
Hugh Z Ford
1Laboratory for Molecular Cell Biology and Department of Cell and Developmental Biology, University College London, United Kingdom
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Angelika Manhart
2Department of Mathematics, University College London, United Kingdom
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Jonathan R Chubb
1Laboratory for Molecular Cell Biology and Department of Cell and Developmental Biology, University College London, United Kingdom
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  • For correspondence: j.chubb@ucl.ac.uk
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Abstract

Self-sustaining signalling waves provide a source of information in living systems. A classic example is the rotating spiral waves of cAMP (chemoattractant) release that encode Dictyostelium morphogenesis. These patterns remain poorly characterised due to limitations in tracking the signalling behaviour of individual cells in the context of the whole collective. Here, we have imaged Dictyostelium populations over millimetre length scales and track the emergence, structure, progression and biological effects of cAMP waves by monitoring the signalling states and motion of individual cells. Collective migration coincides with a decrease in the period and speed of waves that stem from an increase in the rotational speed and curvature of spiral waves. The dynamics and structure of spiral waves are generated by the vortex motion of the spiral tip. Spiral tip circulation spatially organises a small group of cells into a ring pattern, which also constrains spiral tip motion. Both the cellular ring and tip path gradually contract over time, resulting in the acceleration of spiral rotation and change in global wave dynamics. Aided by mathematical modelling, we show that this contraction is due to an instability driven by a deflection in cell chemotaxis around the spiral tip cAMP field, resulting in a deformation of the cellular ring pattern towards its centre. That is, vortex contraction modulates the source of information which, upon dissemination (excitable signal relay) and decoding (chemotaxis), triggers morphogenesis. By characterising rotating spiral waves at this level of detail, our results describe a mechanism by which information generated by a self-sustaining signal, and disseminated across the population, is modulated at the organisational source.

Competing Interest Statement

The authors have declared no competing interest.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-ND 4.0 International license.
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Posted January 09, 2022.
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Signalling centre vortices coordinate collective behaviour in social amoebae
Hugh Z Ford, Angelika Manhart, Jonathan R Chubb
bioRxiv 2022.01.07.475371; doi: https://doi.org/10.1101/2022.01.07.475371
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Signalling centre vortices coordinate collective behaviour in social amoebae
Hugh Z Ford, Angelika Manhart, Jonathan R Chubb
bioRxiv 2022.01.07.475371; doi: https://doi.org/10.1101/2022.01.07.475371

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