Collective intercellular communication through ultra-fast hydrodynamic trigger waves

Arnold J. T. M. Mathijssen, Joshua Culver, M. Saad Bhamla () and Manu Prakash ()
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Arnold J. T. M. Mathijssen: Stanford University
Joshua Culver: Georgia Institute of Technology
M. Saad Bhamla: Georgia Institute of Technology
Manu Prakash: Stanford University

Nature, 2019, vol. 571, issue 7766, 560-564

Abstract: Abstract The biophysical relationships between sensors and actuators1–5 have been fundamental to the development of complex life forms. Swimming organisms generate abundant flows that persist in aquatic environments6–13, and responding promptly to external stimuli is key to survival14–19. Here we present the discovery of ‘hydrodynamic trigger waves’ in cellular communities of the protist Spirostomum ambiguum that propagate—in a manner similar to a chain reaction20–22—hundreds of times faster than their swimming speed. By coiling its cytoskeleton, Spirostomum can contract its long body by 60% within milliseconds23, experiencing accelerations that can reach forces of 14g. We show that a single cellular contraction (the transmitter) generates long-ranged vortex flows at intermediate Reynolds numbers that can, in turn, trigger neighbouring cells (the receivers). To measure the sensitivity to hydrodynamic signals in these receiver cells, we present a high-throughput suction–flow device for probing mechanosensitive ion channels24 by back-calculating the microscopic forces on the cell membrane. We analyse and quantitatively model the ultra-fast hydrodynamic trigger waves in a universal framework of antenna and percolation theory25,26, and reveal a phase transition that requires a critical colony density to sustain collective communication. Our results suggest that this signalling could help to organize cohabiting communities over large distances and influence long-term behaviour through gene expression (comparable to quorum sensing16). In more immediate terms, because contractions release toxins27, synchronized discharges could facilitate the repulsion of large predators or immobilize large prey. We postulate that numerous aquatic organisms other than protists could coordinate their behaviour using variations of hydrodynamic trigger waves.

Date: 2019
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DOI: 10.1038/s41586-019-1387-9

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