Collective intercellular communication through ultra-fast hydrodynamic trigger waves

The biophysical relationships between sensors and actuators(1-5) have been fundamental to the development of complex life forms. Swimming organisms generate abundant flows that persist in aquatic environments(6-13), and responding promptly to external stimuli is key to survival(14-19). 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 reaction(20-22)-hundreds of times faster than their swimming speed. By coiling its cytoskeleton, Spirostomum can contract its long body by 60% within milliseconds(23), 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 channels(24) 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 theory(25,26), 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 sensing(16)). In more immediate terms, because contractions release toxins(27), 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.