ABOVE: Trichoplax adhaerens has no muscles or neurons and no defined shape but still manages coordinated movement.

CREDIT: MANU PRAKASH

Most animals rely on changes in cell shape to move tissues around during development, but these alterations are usually slow and are rare in adult animals. In a case of extreme exception described in October in PNAS, the adult marine invertebrate Trichoplax adhaerens, a critter in the shape of a smashed wad of chewing gum no bigger than a piece of lint, consistently contracts and relaxes the cells on the top of its body at speeds nearly 10 times faster than ever before observed in an animal. Researchers discussed the published work, as well as ongoing studies into the purpose of the super fast cellular contractions, in three presentations at the American Society for Cell Biology (ASCB) annual meeting in San Diego this week.

It’s “astonishing” that a cell can contract so quickly and retain its functional integrity while adhering to the surrounding cells, says Alejandro Sánchez Alvarado, a biologist at the Stowers Institute for Medical Research in Kansas City, Missouri, who did not participate in the work. “That’s a remarkable way of managing force, and [studying this animal] is helping us understand how multicellularity may have arisen as a life form on this planet.”

Trichoplax adhaerens are just a millimeter or two in diameter and flatter than a piece of paper—only about 25 microns thick. This tiny blob of an animal lives in oceans and is thought to be one of the most ancient metazoans. Their bodies are made up of two layers of epithelial cells: the ciliated bottom layer faces the substrate along which they’re moving and the top layer faces open water. So-called fiber cells reside in between the epithelia. They have no muscles, nerves, organs, or extracellular matrix, yet they are capable of directed movement, coordinated secretion of digestive enzymes, and predictable behaviors.

When Stanford University’s Manu Prakash was starting his lab about eight years ago, he wanted to be able to connect the behavior of an animal’s cells with that of the entire organism. Trichoplax fit the bill, thanks to its limited number of cell types and small size that allowed the researchers to view all the cells in a living adult animal at once. Over the years, Prakash’s group has built tracking microscopes to follow the animals as they lumber along glass dishes in seawater. When they recently used a fluorescent dye to visualize the cell membranes, they saw that cells in the top layer of epithelium contracted their surfaces more than 50 percent over the span of a single second—an observation that Prakash describes as “a huge surprise.”

For the PNAS study, Prakash, postdoc Shahaf Armon, and colleagues characterized the shape changes in the epithelial cells. They found that sometimes cells contracted in sequence—generating patterns such as radiating waves—but most often contracted individually. The contractions didn’t result in obvious rearrangements of the cells or ruptures in the tissue. Cell surfaces recovered from the contractions by expanding more slowly than they’d contracted.

The researchers also confirmed previous work showing that actin bundles appear on the surface of Trichoplax cells, as is the case for nonmuscle contractile cells in other animals, and determined that homologs of human myosins were present in the animal’s genome. They performed theoretical calculations that showed the observed cellular movements could be explained by nonmuscle myosin acting on the actin bundles present on the cellular surface. In the study, the team hypothesizes that the rapid contractions and corresponding expansions of the cells’ surfaces allow the animal to cope with external and internal forces without tearing apart.

In the new work Prakash presented at the ASCB meeting Tuesday (December 11), the team found that, while the contractility of the epithelium minimizes ruptures from external forces and movement within the animal, it doesn’t avoid them completely. In the talk and in a corresponding paper they plan to release on bioRxiv, the researchers say the animal uses these tissue tears during asexual reproduction.

In an adult Trichoplax adhaerens autofluorescence appears as green, histone 3 is labeled red, and nuclei are stained blue. Signal overlays are on the right. Karolin von der Chevallerie, Schierwater lab

According to Bernd Schierwater, who studies Trichoplax and related animals at the University of Veterinary Medicine Hannover in Germany and did not participate in the work, it’s “fantastic” to see a mechanistic explanation for the success of the Trichoplax body plan and behaviors, such as locomotion, that researchers have observed for years. “They don’t have any real organs for moving and moving cilia is probably not the [only] way to do it,” he says. “They have to respond fast to any changes in the environment,” so rapid cell contraction is a way to do that.

Going forward, Prakash says, his team will continue to build tools to study Trichoplax and what the animal can reveal about a broad range of biological problems, including how ecology and environment shape biology.

“The likelihood of finding new biology in an organism that’s been chiseled through millions of years of evolution and has not been [well] studied is very high,” says Sánchez Alvarado.

S. Armon et al., “Ultrafast epithelial contractions provide insights into contraction speed limits and tissue integrity,” PNAS, doi:10.1073/pnas.1802934115, 2018.

V.N. Prakash et al., “Epithelial tissue fracture dynamics govern fast and extreme plastic shape changes in Trichoplax adhaerens,” Mol Biol Cell, 28:191, abstract #M119, 2018.