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The more they eat, the more tentacles these sea anemones sprout - Science Magazine

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Starlet sea anemones are the first species known to grow new limbs in response to food availability.

Anniek Stokkermans/European Molecular Biology Laboratory

Almost every school child knows that cats have four legs, humans two, and spiders, a terrifying eight. Their number of limbs is immutable, set by their genetic code. But a new study suggests starlet sea anemones—part of a famously adaptable group of aquatic creatures known as cnidarians—have a leg up on them. They are the first species shown to grow entirely new limbs in response to food.

Starlet sea anemones (Nematostella vectensis) are tiny, flowerlike invertebrates that live in shallow, salty lagoons along the coasts of North America and in parts of the United Kingdom. They start their lives as mobile larvae, before burrowing themselves in fine mud, where they develop their adult form and remain for the rest of their short lives. To feed, they capture small mollusks and crustaceans with venom-filled tentacles and pull them down to their mouths. But scientists never knew why some anemones had as few as four tentacles—and others as many as 24.

To find out, developmental biologist Aissam Ikmi of the European Molecular Biology Laboratory and colleagues raised more than 1000 of the fingernail-size creatures in their lab. While working on another project, Ikmi noticed that the more the anemones were fed, the faster their tentacles appeared—some could sprout new pairs within just a few days. But when feeding slowed, tentacle growth did, too. “From there, we started with the most straightforward hypothesis: Does food matter for them? And then the answer was yes,” he says.

The anemones start with four central buds around their mouths that grow into their first four tentacles. After that, the growth of new tentacles seemed to be driven by the availability of food. When the scientists fed the anemones a normal diet of brine shrimp, it took 5 days to sprout new buds—and an additional 5 days for those buds to reach the length of fully developed tentacles.

To discover what was driving the tentacle growth, Ikmi scoured the literature and found that anemones—similar to other animals, plants, and even yeast—have a cell signaling pathway that links nutritional intake with developmental processes. When the researchers blocked that pathway—known as target of rapamycin—the anemones stopped growing new buds and tentacles, despite being continuously fed, they report this month in Nature Communications.

But, “There is not one recipe to build a structure,” Ikmi says. He discovered that adult-stage tentacles develop differently from the anemone’s first four, and his team identified the gene in muscle cells responsible for growing those starter buds. Using the gene-editing technique CRISPR, the researchers then created mutant anemones lacking the gene. The mutants’ first four tentacle buds developed to maturity, but no additional tentacles followed, even if they were well fed. Without the gene, the anemone simply couldn’t grow new tentacles. What’s more, the muscle cells where the gene is active mark where the next wave of tentacles will grow. And as they grow, neighboring muscle cells activate their own versions of the gene, creating a ripple effect of new buds across the anemone’s body.

“It’s a very exciting study,” says Chiara Sinigaglia, a developmental biologist at the Institute of Functional Genomics of Lyon, who was not involved in the new work. She says the fact that anemones are continuously building their bodies in response to their environment is “one of the very fascinating things about cnidarians.”

Because some anemone species can live for more than 65 years, “they need to continuously adapt their body to changing environmental conditions,” says Jake Warner, a developmental biologist at the University of North Carolina, Wilmington, who was not involved in the study. “Even relatively simple structures, like tentacles, use complicated genetic programs [to do that].”

Sea anemones, Ikmi says, are animals but react more like plants: Because they are usually stuck in one place, they are constantly adapting to their environment. And, like plants, sea anemones grow new body structures instead of storing the energy. This makes them great candidates to study complex organism-environment relationships, scientists suggest. “We don’t know how they are able to live for all these years in a same spot where the environment changes. How they are able to adjust their biology is still an open question,” Ikmi says.

His next steps involve exploring whether feeding-dependent processes are also involved in regeneration and investigating the “unconventional role” of muscles in defining where new tentacles form.

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