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The Toxin That Helps Oyster Mushrooms Devour Worm Flesh

Consider the oyster mushroom. It’s a mild thing, a pert, often creamy-colored whorl of fungus that goes well with thyme sautéed in butter. But among scientists who study mushrooms, it has earned a reputation for activities more sinister than you’d expect from a fungus found in fine dining. The oyster mushroom is a carnivore.

The mushroom’s usual diet of damp logs is low in nitrogen. To get that essential element, it feeds on microscopic nematodes, a type of worm. When a worm makes the mistake of passing over the fungus, the oyster mushroom paralyzes and kills it, devouring the animal’s nitrogen-rich flesh with root-like tendrils called hyphae.

Outside the animal kingdom, Venus flytraps, pitcher plants and others are well known for their macabre meal-making. But fungi, too, have an appetite for flesh, and it’s not just the oyster mushroom, although it is the only carnivorous fungus you’ll generally find in your grocery store. Some fungi craft sticky nets laced with tempting scents to snare their prey. Others create deadly collars that constrict as the worm struggles, immobilizing the prey as the fungus’s hyphae, penetrate its body. Some even release tiny sickle-shape spores that, when swallowed by a nematode, wreak havoc from within.

The scenarios all end with the worm’s body invaded by the threads of its hungry captor.

The oyster mushroom’s weapon of choice seems to be a toxin: Worms that touch the fungus are paralyzed, and their cells fall apart as they succumb to the hyphae. In a paper published Wednesday in the journal Science Advances, researchers report that they’ve identified the substance, which is contained in globes that they compare to lollipops. To the scientists’ surprise, it is a fairly common molecule, rather than an exotic, highly evolved substance. But to the hapless worms, it’s deadly.

Fluorescence imaging of mitochondria in nematode skin tissue before and after exposing them to oyster mushrooms.Credit…Ching-Han Lee

Before they knew the toxin’s identity, the researchers were familiar with its effects, said Yen-Ping Hsueh, a researcher at the Institute of Molecular Biology of the Academia Sinica in Taiwan, and an author of the new paper. In 2020, the team described how toxins get into worms’ bodies through the sensitive tips of the creature’s small sensing organs.

“They really paralyze the worms within a minute,” Dr. Hsueh said. “It’s very dramatic.”

Once the toxin reaches the worm’s neurons and muscle cells, it destabilizes the normal flow of ions across the cells’ membranes, causing catastrophic failure.

For their latest paper, Dr. Hsueh and her colleagues used ultraviolet rays and a chemical that causes mutations on oyster mushrooms and looked for individuals whose touch did not kill worms. They found that all of these fungal mutants lacked small globes called toxocysts that hang like fruit from the hyphae. These, they reasoned, must be where the substance was kept.

But attempts to pinpoint the toxin by harvesting the toxocysts from non-mutant mushrooms failed, and the researchers only understood why when they found that physically disturbing the globes made them harmless to worms. The substance must be volatile — floating away in the air as soon as it is released.

A scanning electron microscopy image of toxocysts on an oyster mushroom.Credit…Yi-Yun Lee

Using a machine to analyze the air above disturbed toxocysts revealed a single molecule: 3-octanone. That was surprising, Dr. Hsueh said. 3-octanone is a relatively commonplace substance made by plants and fungi. It is also a common ingredient in fragrances and flavors. But applying the substance to worms made it clear 3-octanone had all the gruesome effects of a brush with an oyster mushroom. They had found their culprit.

Nematode worms have been known to destroy the roots of crops, and antiworm substances from nature have inspired drugs like ivermectin, the antiparasite medication that made headlines during the height of the pandemic. Because 3-octanone is volatile, it is unlikely it could be used as a pesticide against worms — it would just drift away. Furthermore, the oyster mushroom only goes to the trouble to make toxocysts when it is in a nitrogen-poor environment. So oyster mushrooms likely could not serve as a form of natural pesticide alongside crops slathered with nitrogen-rich fertilizers.

But perhaps, Dr. Hsueh said, understanding how the oyster mushroom came to use this substance as a toxin and what triggers the creation of toxocysts could open the door to a new kind of pest control. If oyster mushrooms could be made to arm themselves, even in the richness of a fertilized field, we might someday see their talents for destruction deployed on our behalf — and not just in the service of making themselves plumper and tastier for our plates.

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