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Fibers point the way to a regenerating hydra’s extremities

DEC 10, 2020
The location of topological defects in the orientation of the fibers indicates where the developing animal’s mouth and foot emerge.

The freshwater animal Hydra has long captivated biologists for its ability to regenerate. Cut off a fragment of the centimeter-long tubular creature and within a few days that fragment will transform into a functioning organism, having regrown a foot for anchoring to surfaces and a mouth and tentacles for consuming prey. Though many researchers have explored the biochemistry underlying hydra morphogenesis, Yonit Maroudas-Sacks, Erez Braun, Kinneret Keren , and their colleagues at the Technion–Israel Institute of Technology are focusing on the mechanical aspects of the process. They show in a new study that the nematic organization of supracellular actin fibers in hydras plays a prominent role in defining the animals’ body plan during regeneration.

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A schematic (left side) and a micrograph (right side) of fiber orientation in a mature hydra reveal local topological defects.

Yonit Maroudas-Sacks and Kinneret Keren

The fibers in mature hydras are aligned parallel to the organisms’ body axis. When the scientists analyzed the fibers, they found specific points—defects—around which the local fiber orientation rotates by either a full or half revolution. The defects carry what’s known as topological charge. The total defect charge of a closed spheroid is +2; for example, consider a globe with lines of longitude that converge to form two +1 defects at the poles. Mature hydras also have spheroid topology and thus +2 charge: As shown in the figure, two +1 defects are located at the tips of the mouth and foot. (Each tentacle also has a +1 defect at the tip that is canceled out by two –1/2 defects on the sides of its base.) However, unlike a globe’s lines of longitude, a hydra’s actin fibers, which consume energy to contract and expand, make up an active nematic system. Previous observations in other active nematic systems have shown that topological defects often foretell noteworthy phenomena.

Using hydras whose fibers are genetically engineered to glow when exposed to blue light, the researchers cut off a slice of tissue and tracked the changes in fiber orientation as the organism regrew. The fragment quickly folded into a spheroid, and as the hours went by, the researchers monitored the appearance and evolution of a series of +1, +1/2, and –1/2 defects. An early +1 defect, the researchers found, would remain in place and typically serve as the site of mouth formation. The +1/2-charge defects would move across the developing hydra and either cancel with a –1/2 defect or merge with another +1/2 to form a +1 at the location where the animal’s foot would sprout.

The results show that topological defect dynamics can predict the locations of a developing hydra’s head and foot long before either feature starts to emerge. Maroudas-Sacks, Braun, Keren, and colleagues emphasize that they have not uncovered any causal mechanism by which the fiber dynamics facilitates the organisms’ regeneration. Still, their work suggests that an intricate interaction between biochemistry and mechanics is at play. (Y. Maroudas-Sacks et al., Nat. Phys., 2020, doi:10.1038/s41567-020-01083-1 .)

More about the authors

Andrew Grant, agrant@aip.org

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