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Cell communication in the blink of an eye

The bodies of unicellular organisms called protists can contract extremely fast. Analysis reveals that the flow of surrounding fluid during contraction triggers a chain reaction of contraction of neighbouring protists.
Pavel Tomancak is at the Max Planck Institute of Molecular Cell Biology and Genetics, Dresden 01307, Germany.
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Passing information reliably and rapidly across large distances is crucial for the survival of cells in complex environments. Multicellular organisms have evolved ways to pass signals along neurons at speeds of 100 metres per second. In the unicellular world, organisms rely on their external medium when transmitting signals between cells. Writing in Nature, Mathijssen et al.1 report that when unicellular organisms called protists undergo rapid cellular contraction, the fluid in which the organisms live is stirred up, and the resulting fluid flow can trigger the ultra-fast propagation of contraction behaviour across the protist population. Contraction can be accompanied by the release of toxins as a form of defence2. The ability to trigger a population-level wave of contractions might be crucial for survival of protists in a perilous aquatic environment full of predators.

The hero of our story is a protist called Spirostomum ambiguum (Fig. 1). Although small by our standards, its length of 1.3 mm makes it a giant among unicellular organisms. Ever since the biologist Ernst Haeckel reported classic studies of protists in the late nineteenth century3, S. ambiguum has been a topic of fascination, particularly because it can contract to about 40% of its original length at a speed 100 times faster than the blink of an eye4,5. Although biologists have come a long way towards understanding the cellular and molecular mechanisms underlying this contraction68, it has remained a relatively neglected subject in biological research.

Figure 1 | The spread of a wave of contraction across a protist population. a, The protist Spirostomum ambiguum lives in aquatic environments and has the capacity to contract to less than half its normal length4,5. Mathijssen et al.1 studied this phenomenon, and report that when this five-millisecond contraction occurs, it generates flows in the surrounding fluid. b, If these flows are sensed by neighbouring S. ambiguum cells, this causes them to contract. c, The contraction can thus rapidly spread through the cell population.

Now Mathijssen and colleagues have explored this topic from a biophysical viewpoint, and their results remind us of how incredibly fast this process is. Using high-speed video microscopy that can capture 10,000 frames per second, the authors filmed the contractions of thousands of S. ambiguum cells, and quantified their contraction speeds comprehensively.

They find that, during its 5-millisecond contraction, the protist accelerates to reach the equivalent of a gravitational force (g force) of 14g. This is highly impressive, considering that pilots in the Master Class group of the Red Bull Air Race (a Formula One racing equivalent for aeroplanes) are disqualified if they exceed 12g, because a pilot who experiences such forces is at risk of losing consciousness. Yet such g forces pose no problems for S. ambiguum. After the rapid contraction, the protist relaxes comparatively slowly, within about 1 second, and can repeat the cycle again and again.

After quantifying the key parameters of the contraction, Mathijssen and colleagues studied the phenomenon in more depth as they sought to understand its effects in the microscopic world and determine the implications. The authors observed that the contraction generates long-range fluid flows around the organism. When they used beads to visualize the flows, they found that they look like vortices that expand over time. Using well-established equations that describe fluid motion9, the authors recapitulated this flow pattern in a computer simulation. This showed that, in a sufficiently liquid medium, the contraction could generate flow that facilitated the dispersal of material around the protist.

But what triggers the contraction? Biologists had thought of this behaviour as a type of ‘startle’ response, perhaps a reaction to the presence of a predator. However, the exact mechanism had remained elusive. Mathijssen and colleagues propose that the trigger for contraction could be flows in the surrounding fluid generated by the organisms themselves, or by predators.

To test their hypothesis, they constructed an apparatus in which individual S. ambiguum cells were exposed to fluid flows at increasing velocities. Using fluid-dynamics methods10, the authors could relate the velocity of the flow that triggers a contraction to the level of tension that such flows induce in biological membranes. They find a remarkable similarity between the level of flow-induced tension that triggers contraction and the tension required to open mechanosensitive ion channels in cell membranes11. It has been suggested that protists use mechanosensitive channels to sense liquid flows12, and this convergence of theory and experimental work suggests that, once flows reach a certain threshold of magnitude, a contraction is triggered.

At this point, however, the happy union of biology and physics ends. This is because, to satisfy a biologist that such a mechanism is at play, evidence would be required that depletion of these mechanosensitive channels in S. ambiguum cells affects the organisms’ ability to react to the liquid flow. Such manipulations are not currently feasible in S. ambiguum, and so, for now, we must regard this mechanism as not definitively proven.

Regardless of the exact molecular details of how cells contract, Mathijssen and colleagues’ experiments have clearly established that flows can trigger the contraction. Given their observation that the contraction itself generates flows, the authors then asked what happens when many S. ambiguum cells come together in close proximity. Can they trigger each other’s contractions by means of the flows they generate? Remarkably, they can. S. ambiguum cells cultured in vitro tend to self-assemble into clusters, and the authors report that, when the cells reach a certain density, the protists exhibit a striking collective phenomenon: one cell spontaneously contracts, triggering contractions in its neighbours and thereby propagating a wave of contraction through the colony (Fig. 1).

These waves travel at remarkably high speeds, of 0.25 m s−1. The authors used further powerful theoretical frameworks1315 to simulate the triggering and propagation of the waves, generating different simulations depending on the orientation, shape and density of the S. ambiguum cells. They compared these theoretical analyses with their experimental results, and established the threshold cellular density at which S. ambiguum colonies are likely to generate fast collective contractions.

But the million-dollar question remains: what is this collective contraction useful for? The authors show, through simulations, that one possible function of waves of contraction is to enable a synchronized discharge of toxins in response to a predator. The flows generated by a large predator itself, or by a predator’s attempt to eat an individual S. ambiguum16, might generate an initial trigger that induces widespread toxin release by the colony into the surrounding medium. Testing this hypothesis would require targeted genetic manipulations to uncouple the flow-generation and -sensing process from the toxin-release event.

Many protists exhibit rapid contractions, and many cells and organisms, such as bacteria and fishes, generate and sense liquid flows. Investigating the generation and sensing of these flows is likely to be a fruitful topic for future research. lt will be interesting to see how interdisciplinary cooperation between biology and physics continues to shed light on this remarkable signal-propagation process.

doi: 10.1038/d41586-019-02069-7

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