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Collective intercellular communication through ultra-fast hydrodynamic trigger waves

By Arnold J. T. M. Mathijssen, Joshua Culver, M. Saad Bhamla, Manu Prakash

Posted 26 Sep 2018
bioRxiv DOI: 10.1101/428573 (published DOI: 10.1038/s41586-019-1387-9)

The biophysical relationships between sensors and actuators have been fundamental to the development of complex life forms; abundant flows are generated and persist in aquatic environments by swimming organisms, while responding promptly to external stimuli is key to survival. Here, akin to a chain reaction, we present the discovery of hydrodynamic trigger waves in cellular communities of the protist Spirostomum ambiguum, propagating hundreds of times faster than the swimming speed. Coiling its cytoskeleton, Spirostomum can contract its long body by 50% within milliseconds, with accelerations reaching 14g-forces. Surprisingly, a single cellular contraction (transmitter) is shown to generate long-ranged vortex flows at intermedi- ate Reynolds numbers, which can trigger neighbouring cells, in turn. To measure the sensitivity to hydrodynamic signals (receiver), we further present a high-throughput suction-flow device to probe mechanosensitive ion channel gating by back-calculating the microscopic forces on the cell mem- brane. These ultra-fast hydrodynamic trigger waves are analysed and modelled quantitatively in a universal framework of antenna and percolation theory. A phase transition is revealed, requiring a critical colony density to sustain collective communication. Our results suggest that this signalling could help organise cohabiting communities over large distances, influencing long-term behaviour through gene expression, comparable to quorum sensing. More immediately, as contractions release toxins, synchronised discharges could also facilitate the repulsion of large predators, or conversely immobilise large prey. We postulate that beyond protists numerous other freshwater and marine organisms could coordinate with variations of hydrodynamic trigger waves.

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