Summary

When hungry worms encounter bad-tasting chemicals, they stop eating and spit. To make this switch possible, a muscle in their mouths does two different things simultaneously, splitting up its activity in a way that scientists have never seen before.

When a worm spits, molecular signals surge in a small section (green) in the forward-facing ends of muscle cells located at the front of the mouth. Credit: Steven Sando et al./eLife 2021

Muscle cells can multitask.

In tiny, transparent worms, one type of muscle cell can partition itself so that two areas act independently, a new study reveals. One cell region contracts while a second region undergoes rhythmic contractions and relaxations.

Scientists have generally thought that each muscle cell contracts in a uniform motion. The collective action of constellations of muscle cells then produces the movements a creature needs to flee a predator, consume a meal, or type an email.

But Howard Hughes Medical Institute Investigator H. Robert Horvitz and colleagues discovered a division of labor within one type of worm muscle cell that allows the animal to protect itself from potentially dangerous chemicals. This multitasking cell lets the worms quickly spit out food they have swallowed, study coauthor Steven Sando, Horvitz, and their colleagues report in the journal eLife on July 2, 2021; the full version of their paper was published on August 3.

“This is the first study to show that two compartments within a muscle cell can contract independently, seemingly oblivious to each other,” says Horvitz, a molecular geneticist and neurobiologist at the Massachusetts Institute of Technology.

“Steve’s discovery changes the way we think about the control of behavior, because it suggests that individual muscle cells can be partitioned into smaller functional units,” adds Horvitz, who shared the 2002 Nobel Prize in Physiology or Medicine for identifying genes that control organ development and programmed cell death.

After eating, a worm senses the presence of toxic chemicals and promptly spits out what it has swallowed. To switch from feeding to spitting, specific muscle cells in the mouth perform two functions at once. Credit: Steve Sando

The mechanics of spitting

The roundworm Caenorhabditis elegans gobbles up microbes floating in the water using its tube-like mouth. Muscle cells contract to open a valve at the front of the mouth and to generate suction that pulls in water and microbes. “The worms are like little vacuum cleaners for bacteria,” Sando says. “When the muscle cells relax, the valve closes, causing food to remain trapped in the worm’s mouth.”

Previously, researchers in the lab had observed that when a worm senses noxious chemicals, it stops eating and spits out bubbles and food. Watching through a microscope as these worms spit, Sando noticed that they were holding the front part of their mouths, where the valve is located, open.

Using a laser, he disabled muscle cells lining the mouth and concluded that a single type of cell, called pm3, was responsible for letting the worms spit. By examining the molecular signaling within pm3, Sando showed that the front part of the cell activated independently from the rest.

Sando’s results revealed that when a worm spits, the pm3 muscles perform two actions at once. At the front of pm3, a small region contracts to hold the valve open, and it stays contracted while the remaining 90 percent of the cell contracts and relaxes rhythmically to suck in water and then eject it until the worm has cleansed its palate.

In other experiments, Sando traced the key control of this activity to a single neuron. Based on information it receives from taste-sensing cells, this neuron controls whether the worm eats, spits, or performs some variation on these behaviors.

To make spitting possible, the front end of the multitasking muscle cells (pm3) contracts, opening the valve at the front of the mouth, while the rest of the muscle continues to pump water in and out.
To make spitting possible, the front end of the multitasking muscle cells (pm3) contracts, opening the valve at the front of the mouth, while the rest of the muscle continues to pump water in and out. Credit: Steven Sando

Small feats

While no one has seen this type of muscle cell multitasking before, scientists already knew of a similar strategy that takes place in the worm’s gut, and in ours. As part of digestion, wave-like contractions ripple through cells to push food forward. What Sando’s team saw was different, however: During spitting, one specific region of pm3 underwent sustained contraction, which didn’t propagate to adjacent regions of pm3.

This division of labor may be a strategy that allows the worms to do more with the relatively few cells they possess, says Aravithan Samuel, a biophysicist at Harvard University who was not involved in the study. Like a human, C. elegans is a multicellular organism; however, its body is much simpler, possessing only 959 cells. Even with these limited components, the worm is capable of complex behaviors. “Small creatures can do amazing things,” he says.

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Citation

Steven R. Sando et al., “An hourglass circuit motif transforms a motor program via subcellularly localized muscle calcium signaling and contraction.” eLife. Published online July 2, 2021. doi: 10.7554/eLife.59341

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